Abstract
Owing to the scientific and economic importance, the antagonistic wheat-Puccinia striiformis f. sp. tritici (Pst) pathosystem has been a focus of research over the past five decades. With the recent discovery of barberry as alternate hosts, Pst has been confirmed to be heteroecious, and the roles of the alternate hosts in disease epidemiology and pathogen variation have been studied. Meanwhile, considerable effort has been taken and significant progress has been made to unravel the wheat-Pst interactions. Histological and cytological studies have provided basic information on infection strategies used by the pathogen and defense responses from the host during wheat-Pst interactions and identified cellular components involved in the interactions. Physiological studies demonstrated the essential changes in Pst infected wheat leaves, unraveling the damage of the pathogen and the countermeasures of the host plants. Transcriptome and genome sequencing has revealed the molecular features and dynamics of the wheat-Pst pathosystem. Extensive molecular analyses have led to the identification of major components in the wheat resistance responses. Studies of wheat-Pst interactions have now entered a new phase in which cellular and molecular approaches are being used. In this chapter, we present the achievements made in the histological and cytological study of wheat-Pst interactions as well as physiological plant pathology. Furthermore, the new insights into wheat immunity provided by the sequence resources and advanced genomic technologies were discussed. Overall, this chapter focuses on the cellular biology of the stripe rust fungus and the wheat-Pst interactions, and integrates the emerging data from molecular analyses with the histocytological observations.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abou-Attia MA, Wang X, Al-Attala MN, Xu Q, Zhan G, Kang Z. TaMDAR6 acts as a negative regulator of plant cell death and participates indirectly in stomatal regulation during the wheat-stripe rust fungus interaction. Physiol Plant. 2015;156:262–77.
Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. Genes involved in organ separation in Arabidopsis, analysis of the cup shaped cotyledon mutant. Plant Cell. 1997;9:841–57.
Al-Attala MN, Wang X, Abou-Attia MA, Duan X, Kang Z. A novel TaMYB4 transcription factor involved in the defence response against Puccinia striiformis f. sp. tritici and abiotic stresses. Plant Mol Biol. 2014;84:589–603.
Albrecht V, Weinl S, Balzevic D, D’Angelo C, Batistic O, Kolukisaouglu Ü, Bock R, Schulz B, Harter K, Kudla J. The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J. 2003;36:457–70.
Ali S, Gladieux P, Rahman H, Saqib MS, Fiaz M, Ahmad H, Leconte M, Gautier A, Justesen AF, HovmØller MS, Enjalbert J, Vallavieille-Pope C. Inferring the contribution of sexual reproduction, migration and off-season survival to the temporal maintenance of microbial populations: a case study on the wheat fungal pathogen Puccinia striiformis f. sp. tritici. Mol Ecol. 2014;23:603–17.
Allen RF. Cytological studies of infection of Baart, Kanred, and Mindum wheats by Puccinia graminis tritici. Span J Agric Res. 1923;26:571–604.
Allen RE. A cytological study of Puccinia glumarum on Bromus marginatus and Triticum vulgare. J Agric Res. 1928;36:487–513.
Alonso JM, Stepanova AN, Solano R, Wisman E, Ferrari S, Ausubel FM, Ecker JR. Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc Natl Acad Sci U S A. 2003;100:2992–7.
Antonin W, Holroyd C, Fasshauer D, Pabst S, von Mollard GF, Jahn R. A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. EMBO J. 2000;19:6453–64.
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol. 2004;55:373–99.
Aranda MA, Escaler M, Wang D, Maule AJ. Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proc Natl Sci Acad USA. 1996;93:15289–93.
Artemenko EN, Umnov AM, Chkanikov DI. Changes in the level of indolyl-3-acetic acid and possible paths of it regulation in leaves of wheat infected with stem rust. Sov Plant Physiol (Engl Transl). 1980;27:447–51.
Atkinson GC. The evolutionary and functional diversity of classical and lesser-known cytoplasmic and organellar translational GTPases across the tree of life. BMC Genomics. 2015;16:78.
Atkinson MM, Midland SL, Sims JJ, Keen NT. Syringolide 1 Triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiol. 1996;112:297–302.
Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell. 2003;15:2730–41.
Ayliffe M, Devilla R, Mago R, White R, Talbot M, Pryor A, Leung H. Nonhost resistance of rice to rust pathogens. Mol Plant-Microbe Interact. 2011a;24:1143–55.
Ayliffe M, Jin Y, Kang ZS, Persson M, Steffenson B, Wang SP, Leung H. Determining the basis of nonhost resistance in rice to cereal rusts. Euphytica. 2011b;179:33–40.
Ayliffe M, Singh D, Park R, Moscou M, Pryor T. Infection of Brachypodium distachyon with selected grass rust pathogens. Mol Plant-Microbe Interact. 2013;26:946–57.
Ayres PG. Interactions between environmental stress injury and biotie disease physiology. Annu Rev Phytopathol. 1984;22:53–75.
Azinheira GH, Maria DCS, Talhinhas P, Medeira C, Maia I, Petitot A-S, Fernandez D. Non-host resistance responses of Arabidopsis thaliana to the coffee leaf rust fungus (Hemileia vastatrix). Botany. 2010;88:621–9.
Babaeizad V, Imani J, Kogel K-H, Eichmann R, Hückelhoven R. Over-expression of the cell death regulator BAX inhibitor-1 in barley confers reduced or enhanced susceptibility to distinct fungalpathogens. Theor Appl Genet. 2009;118:455–63.
Baka ZA, Larous L, Losel DM. Distribution of ATPase activity at the host–pathogen interfaces of rust infections. Physiol Mol Plant Pathol. 1995;47:67–82.
Baker CC, Sieber P, Wellmer F, Meyerowitz EM. The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in regulating petal number in Arabidopsis. Curr Biol. 2005;15:303–15.
Bancal MO, Hansart A, Sache I, Bancal P. Modeling fungal sink competitiveness with grains for assimilates in wheat infected by a biotrophic pathogen. Ann Bot. 2012;110:113–23.
Bao YM, Sun SJ, Li M, Li L, Cao WL, Luo J, et al. Overexpression of the Qc-SNARE gene OsSYP71 enhances tolerance to oxidative stress and resistance to rice blast in rice (Oryza sativa L.). Gene. 2012;504:238–44.
Barak M, Trebitsh T. A developmentally regulated GTP binding tyrosine phosphorylated protein A-like cDNA in cucumber (Cucumis sativus L.). Plant Mol Biol. 2007;65:829–37.
Bariana HS, McIntosh RA. Genetics of adult plant stripe rust resistance in four Australian wheats and the French cultivar ‘Hybridede-Bersee’. Plant Breed. 1995;114:485–91.
Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–97.
Batistič O, Kudla J. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network. Planta. 2004;219:915–24.
Batistič O, Kudla J. Plant calcineurin B-like proteins and their interacting protein kinases. Biochim Biophy Acta (BBA) – Mol Cell Res. 2009;1793:985–92
Beck M, Heard W, Mbengue M, Robatzek S. The INs and OUTs of pattern recognition receptors at the cell surface. Curr Opin Plant Biol. 2012;15:367–74.
Benjamins R, Ampudia CS, Hooykaas PJ, Offringa R. PINOID-mediated signaling involves calcium-binding proteins. Plant Physiol. 2003;132:1623–30.
Berlin A, Djurle A, Samils B, Yuen J. Genetic variation in Puccinia graminis collected from oats, rye, and barberry. Phytopathology. 2012;102:1006–12.
Bernstein BW, Bamburg JR. ADF/cofilin: a functional node in cell biology. Trends Cell Biol. 2010;20:187–95.
Beßer K, Jarosch B, Langen G, Kogel KH. Expression analysis of genes induced in barley after chemical activation reveals distinct disease resistance pathways. Mol Plant Pathol. 2001;1:277–86.
Bhattacharya PK, Naylor JM, Shaw M. Nucleic acid and protein changes in wheat leaf nuclei during rust infection. Science. 1965;150:1605–7.
Bhattacharya PK, Shaw M, Naylor JM. The physiology of host–parasite relations. XIX. Further observations on nucleoprotein changes in wheat leaf nuclei during rust infection. Can J Bot. 1968;46:11–6.
Bock JB, Matern HT, Peden AA, Scheller RH. A genomic perspective on membrane compartment organization. Nature. 2001;409:839–41.
Boller T. Ethylene in pathogenesis and disease resistance. In: Mattoo AK, Suttle JC, editors. The plant hormone ethylene. Boca Raton: CRC Press; 1991. p. 293–314.
Boonburapong B, Buaboocha T. Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins. BMC Plant Biol. 2007;7:4.
Botër M, Amigues B, Peart J, Breuer C, Kadota Y, Casais C, Moore G, Kleanthous C, Ochsenbein F, Shirasu K, Guerois R. Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell. 2007;19:3791–804.
Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP. Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA. 2010;107:14502–7
Bowles DJ. Defense-related proteins in higher plants. Annu Rev Biochem. 1990;59:873–907.
Bozkurt O, Unver T, Akkaya MS. Genes associated with resistance to wheat yellow rust disease identified by differential display analysis. Physiol Mol Plant Pathol. 2008;71:251–9.
Bozkurt O, Mcgrann G, MacCormack R, Boyd LA, Akkaya MS. Cellular and transcriptional responses of wheat during compatible and incompatible race-specific interactions with Puccinia striiformis f. sp. tritici. Mol Plant Pathol. 2010;11:625–40.
Brown W. The physiology of host-parasite relations. Bot Rev. 1936;2:236–81.
Burstenbinder K, Rzewuski G, Wirtz M, Hell R, Sauter M. The role of methionine recycling for ethylene synthesis in Arabidopsis. Plant J. 2007;49:238–49.
Buscaill P, Rivas S. Transcriptional control of plant defence responses. Curr Opin Plant Biol. 2014;20:35–46.
Bush DS. Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Biol. 1995;46:95–122.
Bushnell WR. Symptom development in mildewed and rusted tissues. In: Mirocha CJ, Uritani I, editors. The dynamic role of molecular constituents in plant–parasite interaction. St Paul: American Phytopathological Society Press; 1967. p. 21–39.
Bushnell WR. Patterns in the growth, oxygen uptake, and nitrogen content of single colonies of wheat stem rust on wheat leaves. Phytopathology. 1970;60:92–9.
Calonge FD. Chlorophyll and total nitrogen in barley rust infection. Trans Br Mycol Soc. 1967;50:397–401.
Caltrider PG, Ramachandran S, Gottlieb D. Metabolism during germination and function of glyoxylate enzymes in uredospores of rust fungi. Phytopathology. 1963;53:86–92.
Campo S, Peris-Peris C, Siré C, Moreno AB, Donaire L, Zytnicki M, Notredame C, Llave C, San Segundo B. Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol. 2013;199:212–27.
Cao HN, Liu B, Liu TG, Gao L, Chen WQ. Cloning of a heat shock protein gene hsp70 of Puccinia striiformis f.sp.tritici and its expression in response to high-temperature stress. Plant Prot. 2015;41:19–24.
Capozzi F, Casadei F, Luchinat C. EF-hand protein dynamics and evolution of calcium signal transduction: an NMR view. J Biol Inorg Chem. 2006;11:949–62.
Carmona-Gutierrez D, Fröhlich K, Kroemer G, Madeo F. Metacaspases are caspases. Doubt no more. Cell Death Differ. 2010;17:377–8.
Chanda B, Venugopal SC, Kulshrestha S, Navarre DA, Downie B, Vaillancourt L, Kachroo A, Kachroo P. Glycerol-3-phosphate levels are associated with basal resistance to the hemibiotrophic fungus Colletotrichum higginsianum in Arabidopsis. Plant Physiol. 2008;147:2017–29.
Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao Q-M, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P. Glycerol-3- phosphate is a critical mobile inducer of systemic immunity in plants. Nat Genet. 2011;43:421–7.
Chang Q, Liu J, Wang QL, Han LN, Liu J, Li M. Huang LL, Yang JR, Kang ZS. The effect of Puccinia striiformis f. sp. tritici on the levels of water soluble carbohydrates and the photosynthetic rate in wheat leaves. Physiol Mol Plant Pathol. 2013;84:131–7.
Chao QM, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell. 1997;89:1133–44.
Chen XM. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Can J Plant Pathol. 2005;27:314–37.
Chen XM. High-temperature adult-plant resistance, key for sustainable control of stripe rust. Am J Plant Sci. 2013;4:608–27.
Chen XM, Line RF. Gene-Action in wheat cultivars for durable, high-temperature, adult-plant resistance and interaction with race-specific, seedling resistance to Puccinia striiformis. Phytopathology. 1995;85:567–72.
Chen XM, Line RF, Jones SS. Chromosomal location of genes for resistance to Puccinia striiformis in winter wheat cultivars Heines VII, Clement, Moro, Tyee, Tres, and Daws. Phytopathology. 1995;85:1362–7.
Chen H, Xue L, Chintamanani S, Germain H, Lin H, Cui H, Cai R, Zuo J, Tang X, Li X, Guo H, Zhou JM. Ethylene insensitive3 and ethylene insensitive3-like1 repress salicylic acid induction deficient2 expression to negatively regulate plant innate immunity in Arabidopsis. Plant Cell. 2009;21:2527–40.
Chen XM, Penman L, Wan AM, Cheng P. Virulence races of Puccinia striiformis f. sp. tritici in 2006 and 2007 and development of wheat stripe rust and distributions, dynamics, and evolutionary relationships of races from 2000 to 2007 in the United States. Can J Plant Pathol. 2010;32:315–33.
Chen XM, Wang MN, Wan AM, Cheng P, Cheng JJ. Sexual or asexual reproduction, which one is more important for stripe rust. In: Chen W-Q (ed) Disease risk and food security. Proceedings of the 13th international Cereal Rust and Powdery Mildew Conference. Beijing: China Agricultural Science and Technology Press; 2012. pp 36–37
Chen XM, Coram T, Huang XL, Wang MN, Dolezal A. Understanding molecular mechanisms of durable and non-durable resistance to stripe rust in wheat using a transcriptomics approach. Curr Genomics. 2013;14:111–26.
Chen WQ, Wellings C, Chen XM, Kang ZS, Liu TG. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Mol Plant Pathol. 2014;15:433–46.
Chen YE, Cui JM, Su YQ, Yuan S, Yuan M, Zhang HY. Influence of stripe rust infection on the photosynthetic characteristics and antioxidant system of susceptible and resistant wheat cultivars at the adult plant stage. Front Plant Sci. 2015;6:779.
Cheng YL, Zhang HC, Yao JN, Wang XJ, Xu JR, Han QM, Wei GR, Huang LL, Kang ZS. Characterization of non-host resistance in broad bean to the wheat stripe rust pathogen. BMC Plant Biol. 2012;12:96.
Cheng YL, Zhang HC, Yao JN, Han QM, Wang XJ, Huang LL, Kang ZS. Cytological and molecular characterization of non-host resistance in Arabidopsis thaliana against wheat stripe rust. Plant Physiol Biochem. 2013;62:11–8.
Cheng P, Chen XM, See D. Grass hosts harbor more diverse isolates of Puccinia striiformis than cereal crops. Phytopathology. 2016;106:362–71.
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S. CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell. 2003;15:1833–45.
Cheung DSM, Willetts HJ. Changes in proteins and isoenzymes in leaves of wheat when infected by stem rust. Arch Microbiol. 1973;91:365–72.
Chigrin VV, Chumakovskii NN, Zhigalkina TE. Dynamics of ethylene production in the pathogenesis of wheat stem rust. Mikol Fitopatol.1978;12:141–5 (in Russian, transl. by DH Casper)
Choi J, Choi D, Lee S, Ryu CM, Hwang I. Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci. 2011;16:388–94.
Chong J, Harder DE, Rohringer R. Cytochemical studies on Puccinia graminis f. sp. tritici in a compatible wheat host. I. Walls of intercellular hyphal cells and haustorium mother cells. Can J Bot. 1985;63:1713–24.
Chuck G, Candela H, Hake S. Big impacts by small RNAs in plant development. Curr Opin Plant Biol. 2009;12:81–6.
Cloutier S, McCallum B, Loutre C, Banks T, Wicker T, Feuillet C, Keller B, Jordan M. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol Biol. 2007;65:93–106.
Coram TE, Settles ML, Chen XM. Transcriptome analysis of high-temperature adult-plant resistance conditioned by Yr39 during the wheat-Puccinia striiformis f. sp. tritici interaction. Mol Plant Pathol. 2008a;9:479–93.
Coram TE, Wang MN, Chen XM. Transcriptome analysis of the wheat-Puccinia striiformis f. sp. tritici interaction. Mol Plant Pathol. 2008b;9:157–69.
Coram TE, Huang XL, Zhan GM, Settles ML, Chen XM. Meta-analysis of transcripts associated with race-specific resistance to stripe rust in wheat demonstrates common induction of blue copper-binding protein, heat-stress transcription factor, pathogen-induced WIR1A protein, and ent-kaurene synthase transcripts. Funct Integr Genomics. 2010;10:383–92.
Cuvillier O, Pirianov G, Kleuser B, Vanek PG, Coso OA, Gutkind JS, Spiegel S. Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature. 1996;381:800–3.
Dai Y, Wensink PC, Abeles RH. One protein, two enzymes. J Biol Chem. 1999;274:1193–5.
Daly JM, Knoche HW. Hormonal involvement in metabolism of host–parasite interactions. In: Friend J, Threlfall DR, editors. Biochemical sspects of plant–parasite relationships. New York: Academic Press; 1976. p. 117–33.
Daly JM, Knoche HW, Wiese MV. Carbohydrate and lipid metabolism during Germination of uredospores of Puccinia graminis tritici. Plant Physiol. 1967;42:1633–42.
Daly JM, Ludden P, Seevers P. Biochemical comparisons of resistance to wheat stem rust disease controlled by the Sr6 or Sr11 alleles. Physiol Plant Pathol. 1971;1:397–407.
Dangl JL, Jones JD. Plant pathogens and integrated defence responses to infection. Nature. 2001;411:826–33.
de Maio A. Heat shock proteins: facts, thoughts, and dreams. Shock. 1999;11:1–12.
Deikman J. Molecular mechanisms of ethylene regulation of gene transcription. Physiol Plant. 1997;100:561–6.
Dekhuijzen HM, Staples RC. Mobilization factors in uredospores and bean leaves infected with bean rust fungus. Contrib Boyce Thompson Inst. 1968;24:39–52.
Delledonne M, Zeier J, Marocco A, Lamb C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci U S A. 2001;98:13454–9.
Dickson JG, Syamananda R, Flangas AL. The genetic approach to the physiology of parasitism of the corn rust pathogens. Am J Bot. 1959;46:614–20.
Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL. Arabidopsis mutants simulating disease resistance response. Cell. 1994;77:565–77.
Dmochowska-Boguta M, Alaba S, Yanushevska Y, Piechota U, Lasota E, Nadolska-Orczyk A, Karlowski WM, Orczyk W. Pathogen-regulated genes in wheat isogenic lines differing in resistance to brown rust Puccinia triticina. BMC Genomics. 2015;16:742.
Doodson JK, Manners JG, Myers A. Some effects of yellow rust (Puccinia striiformis) on 14carbon assimilation and translocation in wheat. J Exp Bot. 1965;16:304–17.
Dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M, Berry DA, Nosworthy NJ. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev. 2003;83:433–73.
Du H, Zhang L, Liu L, Tang XF, Yang WJ, Wu YM, Huang YB, Tang YX. Biochemical and molecular characterization of plant MYB transcription factor family. Biochemistry. 2009;74:1–11.
Duan YH, Guo J, Wang SJ, Yu XM, Huang LL, Kang AS. Cloning and expression analysis of alanine amino transferase gene TaAlaAT1 in wheat infected with stripe rust fungus. Acta Phys Sin. 2009;39:139–46. (in Chinese)
Duan YH, Guo J, Ding K, Wang SJ, Zhang H, Dai XW, Chen YY, Govers F, Huang LL, Kang ZS. Characterization of a wheat HSP70 gene and its expression in response to stripe rust infection and abiotic stresses. Mol Biol Rep. 2011;38:301–7.
Duan XY, Wang XJ, Fu YP, Tang CL, Li XR, Cheng YL, Feng H, Huang LL, Kang ZS. TaEIL1, a wheat homologue of AtEIN3, acts as a negative regulator in the wheat-stripe rust fungus interaction. Mol Plant Pathol. 2013a;14:728–39.
Duan YH, Guo J, Shi XX, Guan XN, Liu FR, Bai PF, Huang LL, Kang ZS. Wheat hypersensitive-induced reaction genes TaHIR1 and TaHIR3 are involved in response to stripe rust fungus infection and abiotic stresses. Plant Cell Rep. 2013b;32:273–83.
Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci U S A. 2011;108:9166–71.
Duval M, Hsieh T-F, Kim SY, Thomas TL. Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol. 2002;50:237–48.
Dyck PL. Genetics of adult-plant leaf rust resistance in “Chinese Spring” and “Sturdy” wheats. Crop Sci. 1991;31:309.
Edreva A. Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol. 2005;31:105–24.
Ehrlich MA, Ehrlich HG. Fine structure of Puccinia graminis and the transfer of C14 from uredospores to Triticum vulgare. In: Akai S, Ouchi S, editors. Morphological and biochemical events in plant–parasite interaction: Phytopathological Society of Japan; 1971. p. 279–307.
Eichmann R, Dechert C, Kogel K-H, Hückelhoven R. Transient over-expression of barley BAX inhibitor-1 weakens oxidative defence and MLA12-mediated resistance to Blumeria graminis f. sp. hordei. Mol Plant Pathol. 2006;7:543–52.
El Kasmi F, Krause C, Hiller U, Stierhof YD, Mayer U, Conner L, Kong L, Reichardt I, Sanderfoot AA, Jürgens G. SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis. Mol Biol Cell. 2013;24:1593–601.
Ellis JG, Dodds PN, Lawrence GJ. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu Rev Phytopathol. 2007;45:289–306.
Eltayeb AE, Kawano N, Badawi GH, Kaminaka H, Sanekata T, Shibahara T, Inanaga S, Tanaka K. Overexpression of monodehydroascorbate reductase in transgenic Nicotiana benthamiana confers enhanced tolerance to ozone, salt and polyethylene glycol stresses. Planta. 2007;225:1255–64.
Eltelib HA, Badejo AA, Fujikawa Y, Esaka M. Gene expression of monodehydroascorbate reductase and dehydroascorbate reductase during fruit ripening and in response to environmental stresses in acerola (Malpighia glabra). J Plant Physiol. 2011;168:619–27.
Enoksson M, Salvesen G. Metacaspases are not caspases – always doubt. Cell Death Differ. 2010;17:1221.
Eriksson J. Über die Spezialisierung des Parasitsimus bei den Getreiderostpilzen. Ber Dtsch Getreiderostpilze Z Pflanzenkr. 1894;4:197–203.
Fadeel B, Zhivotovsky B, Orrenius S. All along the watch tower: on the regulation of apoptosis regulators. FASEB J. 1999;13:1647–57.
Fan J, Doerner P. Genetic and molecular basis of nonhost disease resistance: complex, yes; silver bullet, no. Curr Opin Plant Biol. 2012;15:400–6.
Farkas GL, Király Z. Amide metabolism in wheat leaves infected with stem rust. Physiol Plant. 1961;14:344–53.
Farrakh S, Wang MN, Chen XM. Expression profiling of pathogenesis-related protein genes in wheat resistance to the stripe rust pathogen (Puccinia striiformis f. sp. tritici). Phytopathology. 2016;S4:197
Feng H, Wang X, Sun Y, Wang X, Chen X, Guo J, Duan Y, Huang L, Kang Z. Cloning and characterization of a calcium binding EF-hand protein gene TaCab1 from wheat and its expression in response to Puccinia striiformis f. sp. tritici and abiotic stresses. Mol Biol Rep. 2011;38:3857–66.
Feng H, Zhang Q, Li HY, Wang XJ, Wang XD, Duan XY, Wang B, Kang ZS. vsiRNAs derived from the miRNA-generating sites of pri-taemiR159a based on the BSMV system play positive roles in the wheat response to Puccinia striiformis f. sp. tritici through the regulation of TaMyb3 expression. Plant Physiol Biochem. 2013a;68:90–5.
Feng H, Zhang Q, Wang QL, Wang XJ, Liu J, Li M, Huang LL, Kang ZS. Target of tae-miR408, a chemocyanin-like protein gene (TaCLP1), plays positive roles in wheat response to high-salinity, heavy cupric stress and stripe rust. Plant Mol Biol. 2013b;83:433–43.
Feng H, Duan XY, Zhang Q, Li XR, Wang B, Huang LL, Wang XJ, Kang ZS. The target gene of tae-miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust. Mol Plant Pathol. 2014a;15:284–96.
Feng H, Liu W, Zhang Q, Wang X, Wang X, Duan X, Li F, Huang L, Kang Z. TaMDHAR4, a monodehydroascorbate reductase gene participates in the interactions between wheat and Puccinia striiformis f. sp. tritici. Plant Physiol Biochem. 2014b;76:7–16.
Feng H, Wang XJ, Zhang Q, Fu YP, Feng CX, Wang B, Huang LL, Kang ZS. Monodehydroascorbate reductase gene, regulated by the wheat PN-2013 miRNA, contributes to adult wheat plant resistance to stripe rust through ROS metabolism. Biochim Biophys Acta (BBA)-Gene Regulat Mech. 2014c;1839:1–12
Feng H, Wang B, Zhang Q, Fu YP, Huang LL, Wang XJ, Kang ZS. Exploration of microRNAs and their targets engaging in the resistance interaction between wheat and stripe rust. Front Plant Sci. 2015;6:469.
Feng H, Wang T, Feng CX, Zhang Q, Zhang XM, Huang LL, Wang XJ, Kang ZS. Identification of microRNAs and their corresponding targets involved in the susceptibility interaction of wheat response to Puccinia striiformis f. sp. tritici. Physiol Plant. 2016;157:95–107.
Feuillet C, Schachermayr G, Keller B. Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. Plant J. 1997;11:45–52.
Feuillet C, Reuzeau C, Kjellbom P, Keller B. Molecular characterization of a new type of receptor-like kinase (wlrk) gene family in wheat. Plant Mol Biol. 1998;37:943–53.
Feuillet C, Penger A, Gellner K, Mast A, Keller B. Molecular evolution of receptor-like kinase genes in hexaploid wheat. Independent evolution of orthologs after polyploidization and mechanisms of local rearrangements at paralogous loci. Plant Physiol. 2001;125:1304–13.
Feuillet C, Travella S, Stein N, Albar L, Nublat A, Keller B. Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc Natl Acad Sci U S A. 2003;100:15253–8.
Fluhr R, Mattoo AK. Critical reviews in plant sciences. In: Conger BV (ed) Ethylene biosynthesis and perception, vol 15. Boca Raton: CRC Press; 1996. pp 479–523
Frandsen G, Müller-Uri F, Nielsen M, Mundy J, Skriver K. Novel plant Ca2+-binding protein expressed in response to abscisic acid and osmotic stress. J Biol Chem. 1996;271:343–8.
Fric F, Heitefuss R. Immunochemische und elektrophoretische Untersuchungen der Proteine von Weizenblättern nach Infektion mit Puccinia graminis tritici. Phytopathol Z. 1970;69:236–46.
Fu DL, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen XM, Sela H, Fahima T, Dubcovsky J. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009;323:1357–60.
Fu ZQ, Dong X. Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol. 2013;64:839–63.
Fu YP, Duan XY, Tang CL, Li XR, Voegele RT, Wang XJ, Wei GR, Kang ZS. TaADF7, an actin-depolymerizing factor, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. Plant J. 2014;78:16–30.
Fukuda R, McNew JA, Weber T, Parlati F, Engel T, Nickel W, Rothman JE, Söllner TH. Functional architecture of an intracellular membrane t-SNARE. Nature. 2000;407:198–202.
Fullington JG, Nityagopala A. Effect of rust infection on the protein components of wheat. Phytochemistry. 1986;25:1289–129.
Gale MD, Devos KM. Plant comparative genetics after 10 years. Science. 1998;282:656–9.
Gan PH, Dodds PN, Hardham AR. Plant infection by biotrophic fungal and oomycete pathogens. In: Silvia P, František B, editors. Signaling and communication in plant symbiosis. New York: Springer; 2012. p. 183–212.
Gassner G, Franke W. Untersuchungen über den Stickstoffhaushalt rostinfizierter Getreideblätter. Phytopathol Z. 1938;11:517–70.
Gay JL, Salzberg A, Woods AM. Dynamic experimental evidence for the plasma membrane ATPase domain hypothesis of haustorial transport and for ionic coupling of the haustorium of Erysiphe graminis to the host cell (Hordeum vulgare). New Phytol. 1987;107:541–8.
Goddard MV. Cytological studies of Puccinia striiformis (yellow rust of wheat). Trans Br Mycol Soc. 1976;66:433–7.
Gordon TR, Duniway JM. Effects of powdery mildew infection on the efficiency of CO2 fixation and light utilization by sugar beet leaves. Plant Physiol. 1982;69:139–42.
Gou JY, Li K, Wu KT, Wang XD, Lin HQ, Cantu D, Uauy C, Dobon-Alonso A, Midorikawa T, Inoue K, Sáncheza J, Fu DL, Blechl A, Wallington E, Fahima Z, Meeta M, Epstein L, Dubcovsky J. Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. Plant Cell. 2015;27:1755–70.
Grant JJ, Yun BW, Loake GJ. Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J. 2000;24:569–82.
Gray J, Close PS, Briggs SP, Johal GS. A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell. 1997;89:25–31.
Gray J, Janick-Buckner D, Buckner B, Close PS, Johal GS. Light-dependent death of maize lls1 cells is mediated by mature chloroplasts. Plant Physiol. 2002;130:1894–907.
Guo HS, Xie Q, Fei JF, Chua NH. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell. 2005;17:1376–86.
Guo J, Bai P, Yang Q, Liu F, Wang X, Huang L, Kang Z. Wheat zinc finger protein TaLSD1, a negative regulator of programmed cell death, is involved in wheat resistance against stripe rust fungus. Plant Physiol Biochem. 2013;71:164–72.
Hahn M. The rust fungi: cytology, physiology and molecular biology of infection. In: Kronstadt J, editor. Fungal pathology. Dordrecht: Kluwer Academic Publisher; 2000. p. 267–306.
Hahn M, Mendgen K. Characterization of in planta induced rust genes isolated from a haustorium-specific cDNA library. Mol Plant-Microbe Interact. 1997;10:427–37.
Hahn M, Mendgen K. Signal and nutrient exchange at biotrophic plant-fungus interfaces. Curr Opin Plant Biol. 2001;4:322–7.
Hahn M, Neef U, Struck C, Göttfert M, Mendgen K. A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. Mol Plant Microbe Interact. 1997b;10:438–45.
Hahn M, Deising H, Struck C, Mendgen K. Fungal morphogenesis and enzyme secretion during pathogenesis. In: Hartleb H, Heitefuss R, Hoppe H-H, editors. Resistance of crop plants against fungi. Jena: Gustav Fischer; 1997a. p. 33–57.
Hakoyama T, Oi R, Hazuma K, Suga E, Adachi Y, Kobayashi M, Akai R, Sato S, Fukai E, Tabata S, Shibata S, Wu G.-J., Hase Y, Tanaka A, Kawaguchi M, Kouchi H, Umehara Y, Suganuma N. The SNARE protein SYP71 expressed in vascular tissues is involved in symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Physiol. 2012; 160:897–905
Halfter U, Ishitani M, Zhu JK. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci U S A. 2000;97:3735–40.
Hao YB, Wang T, Wang K, Wang XJ, Fu YP, Huang LL, Kang ZS. Transcriptome analysis provides insights into the mechanisms underlying wheat plant resistance to stripe rust at the adult plant stage. PLoS One. 2016a;11:e0150717.
Hao YB, Wang XJ, Wang K, Li HY, Duan XY, Tang CL, Kang ZS. TaMCA1, a regulator of cell death, is important for the interaction between wheat and Puccinia striiformis. Sci Rep. 2016b;6:26946.
Harder DE, Mendgen K. Filipin-sterol complexes in bean rust- and oat crown rust-fungal/plant interactions: freeze-etch electron microscopy Uromyces appendiculatus. Protoplasma. 1982;112:46–54.
Harder D, Chong J. Structure and physiology of haustoria. In: Bushnell WR, Roslfs AP, editors. The Cereal Rusts. New York: Academic Press; 1984. p. 431–76.
Harder DE, Chong J. Rust haustoria. In: Mendgen K, Lesemann D-E, editors. Electron microscopy of plant pathogens. Berlin: Springer; 1991. p. 235–50.
Hardham AR, Jones DA, Takemoto D. Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol. 2007;10:342–8.
Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol. 2003;23:6494–506.
Hart H, Becker H. Beitrage zur Frage des Zwischenwirtes für Puccinia glumarum. Z Pflanzenkr (Pflanzenpathol) Pflanzenschutz. 1939;49:559–66.
Harter C, Pavel J, Coccia F, Draken E, Wegehingel S, Tschochner H, Wieland F. Nonclathrin coat protein gamma, a subunit of coatomer, binds to the cytoplasmic dilysine motif of membrane proteins of the early secretory pathway. Proc Natl Acad Sci U S A. 1996;93:1902–6.
He R, Drury GE, Rotari VI, Gordon A, Willer M, Farzaneh T, Woltering EJ, Gallois P. Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis. J Biol Chem. 2008;283:774–83.
Heath MC. Ultrastructural and functional similarity of the haustorial neckband of rust fungi and the Casparian strip of vascular plants. Can J Bot. 1976;54:2484–9.
Heath MC. Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann Bot. 1997;80:713–20.
Heath MC. Hypersensitive response-related death. Plant MolBiol. 2000;44:321–34.
Heath MC, Skalamera D. Cellular interactions between plants and biotrophic fungal parasites. Adv Bot Res. 1997;24:195–225.
Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jürgens G. Functional characterization of the KNOLLE-interactingt-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol. 2001;155:239–49.
Heisterüber D, Schulte P, Moerschbacher B. Soluble carbohydrates and invertase activity in stem rust-infected, resistant and susceptible near-isogenic wheat leaves. Physiol Mol Plant Pathol. 1994;45:111–23.
Heitefuss R. Untersuchungen zur Physiologie des temperaturgesteuerten Verträglichkeitsgrades von Weizen undPuccinia graminis tritici. I. Veränderungen von Sauerstoffaufnahme und Phosphatstoffwechsel. Phytopathol Z. 1965;54:379–400.
Heitefuss R. Nucleic acid metabolism in obligate parasitism. Annu Rev Phytopathol. 1966a;4:221–42.
Heitefuss R. Untersuchungen zur Physiologie des temperaturgesteuerten Verträglichkeitsgrades von Weizen und Puccinia graminis tritici. II. Veränderungen des Nukleinsäurestoffwechsels. Phytopathol Z. 1966b;55:67–85.
Heitefuss R. Der Einfluss von Actinomycin auf Puccinia graminis tritici auf Weizen und den Einbau von Orotsäure-C14 und Uridin-H3 in Wirtspflanze und Parasit. Phytopathol Z. 1970;69:107–14.
Heitefuss R, Wolf G. Nucleic acids in host–parasite interactions. Encycl Plant Physiol, New Ser. 1976;4:480–508.
Hengartner M, Horvitz HR. C. elegans cell survival gene ced-9 encodes a functional homologue of the mammalian proto-onco gene bcl-2. Cell. 1994;76:665–76.
Henty-Ridilla JL, Shimono M, Li J, Chang JH, Day B, Staiger CJ. The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog. 2013;9:e1003290.
Henty-Ridilla JL, Li J, Day B, Staiger CJ. ACTIN DEPOLYMERIZING FACTOR4 regulates actin dynamics during innate immune signaling in Arabidopsis. Plant Cell. 2014;26:340–52.
Hetherington AM, Brownlee C. The generation of Ca2+ signals in plants. Annu Rev Plant Biol. 2004;55:401–27.
Hilu HM. Host-pathogen relationships of Puccinia sorghi in nearly isogenic resistant and susceptible seedling corn. Phytopathology. 1965;55:563–9.
Hovmøller MS, Sorensen CK, Walter S, Justesen AF. Diversity of Puccinia striiformis on cereals and grasses. Annu Rev Phytopathol. 2011;49:197–217.
Hu GG, Rijkenberg FHJ. Ultrastructural localization of cytokinins in Puccinia recondite f. sp. tritici-infected wheat leaves. Physiol Mol Plant Pathol. 1998;52:79–94.
Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics. 2003;164:655–64.
Huang J, Wang J, Zhang H. Rice ZFP15 gene encoding fora novel C2H2-type zinc finger protein lacking DLN box, is regulated by spike development but not by abiotic stresses. Mol Biol Rep. 2005;32:177–83.
Huang X, Ma J, Chen X, Wang X, Ding K, Han D, Qu Z, Hang L, Kang Z. Genes involved in adult plant resistance to stripe rust in wheat cultivar Xingzi 9104. Physiol Mol Plant Pathol. 2013;81:26–32.
Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, Shirasu K, Dangl JL. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 2003;22:5679–89.
Hückelhoven R, Dechert C, Kogel KH. Overexpressionof barley BAX inhibitor 1 induces breakdown of mlo-mediatedpenetration resistance to Blumeria graminis. Proc Natl Acad Sci U S A. 2003;100:5555–60.
Hurni S, Brunner S, Buchmann G, Herren G, Jordan T, Krukowski P, Wicker T, Yahiaoui N, Mago R, Keller B. Rye Pm8 and wheat Pm3 are orthologous genes and show evolutionary conservation of resistance function against powdery mildew. Plant J. 2013;76:957–69.
Imaseki H. The biochemistry of ethylene biosynthesis. In: Mattoo AK, Suttle JC, editors. The plant hormone ethylene. Boca Raton: CRC Press; 1991. p. 1–20.
Inada N, Ueda T. Membrane trafficking pathways and their roles in plant-microbe interactions. Plant Cell Physiol. 2014;55:672–86.
Ishikawa T, Shigeoka S. Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem. 2008;72:1143–54.
Izawa T, Foster R, Chua NH. Plant bZIP protein DNA binding specificity. J Mol Biol. 1993;230:1131–44.
Jagger LJ, Newell C, Berry ST, MacCormack R, Boyd LA. Histopathology provides a phenotype by which to characterize stripe rust resistance genes in wheat. Plant Pathol. 2011;60:640–8.
Jameson PE. Cytokinins and auxins in plant-pathogen interactions–An overview. Plant Growth Regul. 2000;32:369–80.
Jayasekaran K, Kim KN, Vivekanandan M, Shin JS, Ok SH. Novel calcium-binding GTPase (AtCBG) involved in ABA-mediated salt stress signaling in Arabidopsis. Plant Cell Rep. 2006;25:1255–62.
Jiang Z, Ge S, Xing L, Han D, Kang Z, Zhang G, Wang X, Wang X, Chen P, Cao A. RLP1.1, a novel wheat receptor-like protein gene, is involved in the defence response against Puccinia striiformis f. sp. tritici. J Exp Bot. 2013;64:3735–46.
Jin H. Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett. 2008;582:2679–84.
Jin Y. Role of Berberis spp. as alternate hosts in generating new races of Puccinia graminis and P. striiformis. Euphytica. 2011;179:105–8.
Jin Y, Szabo LJ, Carson M. Century-old mystery of Puccinia striiformis life history solved with the identification of Berberis as an alternate host. Phytopathology. 2010;100:432–5.
Johnson R. Durable resistance to yellow (stripe) rust in wheat and its implications in plant breeding. In: Simmonds NW, Rajaram S, editors. Breeding strategies for resistance to the rusts of wheat. Mexico City: CYMMIT; 1988. p. 63–75.
Johnson LB, Brannaman BL, Zscheile FP. Protein and enzyme changes in wheat leaves following infection with Puccinia recondita. Phytopathology. 1968;58:578–83.
Jones JD, Dangl JL. The plant immune system. Nature. 2006;444:323–9.
Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994;266:789–93.
Jung HW, Hwang BK. The leucine-rich repeat (LRR) protein, CaLRR1, interacts with the hypersensitive induced reaction (HIR) protein, CaHIR1, and suppresses cell death induced by the CaHIR1 protein. Mol Plant Pathol. 2007;8:503–14.
Jung HW, Lim CW, Lee SC, Choi HW, Hwang CH, Hwang BK. Distinct roles of the pepper hypersensitive inducedreaction protein gene CaHIR1 in disease and osmotic stress, as determined by comparative transcriptome and proteome analyses. Planta. 2008;227:409–25.
Kalde M, Nühse TS, Findlay K, Peck SC. The syntaxinSYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Natl Acad Sci U S A. 2007;104:11850–5.
Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Che FS. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO J. 2009;28:926–36.
Kang ZS. Ultrastructure of plant pathogenic fungi. Beijing: China Science &Technology Press; 1996.
Kang ZS, Huang LL, Li ZQ. Ultrastructure of wheat cell responses to invasion of wheat stripe rust. Acta Agric Beoreali-occidentalis Sin. 1993;2:25–8.
Kang ZS, Li ZQ, Shang HS. Nuclear condition of uredinial stage of wheat stripe rust. Acta Phys Sin. 1994;24:26–31.
Kang ZS, Huang LL, Li JY. Morphology of plant pathogenic fungi under scanning electron microscope. Beijing: China Agriculture Press; 1997.
Kang ZS, Huang LL, Buchenauer H. Ultrastructural changes and localization of lignin and callose in compatible and incompatible interactions between wheat and Puccinia striiformis. J Plant Dis Prot. 2002;109:25–37.
Kang L, Li J, Zhao T, Xiao F, Tang X, et al. Interplay of the Arabidopsis nonhost resistance gene NHO1 with bacterial virulence. Proc Natl Acad Sci U S A. 2003a;100:3519–24.
Kang ZS, Huang LL, Buchenauer H. Subcellular localization of chitinase and β-1,3–glucanase in compatible and incompatible interaction between wheat and Puccinia striiformis f. sp. tritici. J Plant Dis Protect. 2003b;110:170–83.
Kang ZS, Wang Y, Huang LL, Wei GR, Zhao J. Histology and ultrastructure of incompatible combination between Puccinia striifromis and wheat cultivars with resistance of low reaction type. Sci Agric Sin. 2003c;36:1026–31.
Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, Katou S, Yoshioka H, Terauchi R. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol Plant Pathol. 2003;4:383–91.
Karrer EE, Beachy RN, Holt CA. Cloning of tobacco genes that elicit the hypersensitive response. Plant Mol Biol. 1998;36:681–90.
Katiyar-Agarwal S, Jin H. Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol. 2010;48:225–46.
Kawai M, Pan L, Reed JC, Uchimiya H. Evolutionallyconserved plant homologue of the Bax inhibitor-1 (BI-1) gene capableof suppressing Bax-induced cell death in yeast. FEBS Lett. 1999;464:143–7.
Kawai-Yamada M, Jin U, Yoshinaga K, Hirata A, Uchimiya H. Mammalian Bax-induced plant cell death can be downregulatedby overexpression of Arabidopsis Bax inhibitor-1 (AtBI-1). Proc Natl Acad Sci U S A. 2001;98:12295–300.
Kawai-Yamada M, Ohmori Y, Uchimiya H. Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell. 2004;16:21–32.
Kawchuk LM, Hachey J, Lynch DR, Kulcsar F, Gv R, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prüfer D. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci U S A. 2001;98:6511–5.
Kazan K, Manners JM. Linking development to defense: auxin in plant–pathogen interactions. Trends Plant Sci. 2009;14:373–82.
Keller B, Bieri S, Bossolini E, Yahiaoui N. Cloning genes and QTLs for disease resistance in cereals. In: Varshney RK, Tuberosa R, editors. Genomic-assisted crop improvement. Dordrecht: Springer; 2007. p. 103–27.
Kim WK, Rohringer R. Metabolism of aromatic compounds in healthy and rust-infected primary leaves of wheat. III. Studies on the metabolism of tryptophan. Can J Bot. 1969;47:1425–33.
Kim SY, Thomas TL. A family of basic leucine zipper proteins bind to seed specification elements in the carrot Dc3 gene promoter. J Plant Physiol. 1998;152:607–13.
Kim CY, Lee SH, Park HC, Bae CG, Cheong YH, Choi YJ, Han C, Lee SY, Lim CO, Cho MJ. Identification of rice blast fungal elicitor-responsive genes by differential display analysis. Mol Plant-Microbe Interact. 2000;13:470–4.
Kim CY, Koo YD, Jin JB, Moon BC, Kang CH, Kim ST, Park BO, Lee SY, Kim ML, Huang I, Kang KY, Bahk JD, Lee SY, Cho MJ. Rice C2-domain proteins are induced and translocated to the plasma membrane in response to a fungal elicitor. Biochemistry. 2003a;42:11625–31.
Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S. CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell. 2003b;15:411–23.
Kim YJ, Kim JE, Lee JH, Lee MH, Jun HW, Bahk YY, Hwang BK, Hwang I, Kim WT. The Vr-PLC3 gene encodes a putative plasma membrane-localized phos-phoinositide-specific phospholipase C whose expression is induced by abiotic stress in mung bean (Vigna radiata L.). FEBS Lett. 2004;556:127–36.
Kim JH, Kim HS, Lee YH, Kim YS, Oh HW, Joung H, Chae SK, Suh KH, Jeon JH. Polyamine biosynthesis regulated by StARD expression plays an important role in potato wound periderm formation. Plant Cell Physiol. 2008a;49:1627–32.
Kim YC, Kim SY, Choi D, Ryu CM, Park JM. Molecular characterization of a pepper C2 domain- containing SRC2 protein implicated in resistance against host and non-host pathogens and abiotic stresses. Planta. 2008b;227:1169–79.
Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Hwang D, Nam HG. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science. 2009a;323:1053–7.
Kim MC, Chung WS, Yun DJ, Cho MJ. Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant. 2009b;2:13–21.
Király Z, Elhammad ME, Pozsar BI. Increased cytokinin activity of rust-infected bean and broad bean leaves. Phytopathology. 1967;57:93.
Kitanaka C, Kuchino Y. Caspase-independent programmed cell death with necrotic morphology. Cell Death Differ. 1999;6:508.
Knight H. Calcium signaling during abiotic stress in plants. Int Rev Cytol. 2000;195:269–324.
Koh S, Andre A, Edwards H, Ehrhardt D, Somerville S. Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 2005;44:516–29.
Kolmer JA. Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol. 1996;34:435–55.
Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J. Calcium sensors and their interacting protein kinases: genomics of the Arabidopsis and rice CBL-CIPK signaling networks. Plant Physiol. 2004;134:43–58.
Kopitz J, André S, von Reitzenstein C, Versluis K, Kaltner H, Pieters RJ, Wasano K, Kuwabara I, Liu FT, Cantz M, Heck AJR, Gabius HJ. Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene. 2003;22:6277–88.
Kosugi S, Ohashi Y. Cloning and DNA-binding properties of a tobacco Ethylene-Insensitive3 (EIN3) homolog. Nucleic Acids Res. 2000;28:960–7.
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360–3.
Krattinger SG, Lagudah ES, Wicker T, Risk JM, Ashton AR, Selter LL, Matsumoto T, Keller B. Lr34 multi-pathogen resistance ABC transporter: molecular analysis of homoeologous and orthologous genes in hexaploid wheat and other grass species. Plant J. 2011;65:392–403.
Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med. 1997;3:614–20.
Kroemer G, Martin SJ. Caspase-independent cell death. Nat Med. 2005;11:725–30.
Kruijt M, DE Kock MJ, de Wit PJ. Receptor-like proteins involved in plant disease resistance. Mol Plant Pathol. 2005;6:85–97.
Kwon SI, Cho HJ, Bae K, Jung JH, Jin HC, Park OK. Role of an Arabidopsis Rab GTPase RabG3b in pathogen response and leaf senescence. J Plant Biol. 2009;52:79–87.
Lalanne E, Michaelidis C, Moore JM, Gagliano W, Johnson A, Patel R, et al. Analysis of transposon insertion mutants highlights the diversity of mechanisms underlying male progamic development in Arabidopsis. Genetics. 2004;167:1975–86.
Lambrecht M, Okon Y, Broek A. V, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol 8:298–300
Landschulz WH, Johnson PF, McKnight SL. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1998;240:1759–64.
Laura M, Consonni R, Locatelli F, Fumagalli E, Allavena A, Coraggio I, Mattana M. Metabolic response to cold and freezing of Osteospermum ecklonis overexpressing OsMyb4. Plant Physiol Biochem. 2010;48:764–71.
Lee JH, Kim WT. Molecular and biochemical characterization of VR-EILs encoding mung bean ETHYLENE INSENSITIVE3-LIKE proteins. Plant Physiol. 2003;132:1475–88.
Lee TF, McNellis TW. Evidence that the BONZAI1/COPINE1 protein is a calcium and pathogen-responsive defense suppressor. Plant Mol Biol. 2009;69:155–66.
Li MR. Water relation and photosynthesis in stripe rusted wheat leaves. Dissertation, Department of Plant Protection, Northwest A&F University., Shaanxi, China; 1998
Li A, Heath MC. Effect of plant growth regulators on the interactions between bean plants and rust fungi non-pathogenic on beans. Physiol Mol Plant Pathol. 1990;37:245–54.
Li ZQ, Zeng SM. Wheat stripe rust in China. Beijing: China Agriculture Press; 2002.
Li L, Yu XF, Thompson MG, Yoshida S, Asami T, Chory J, Yin YH. Arabidopsis MYB30 is a direst target of BES1 and cooperates with BED1 to regulate brassinosteroid-induced gene expression. Plant J. 2009;58:275–86.
Li HB, Wei GR, Xu JR, Huang LL, Kang ZS. Identification of wheat proteins with altered expression levels in leaves infected by the stripe rust pathogen. Acta Physiol Plant. 2011;33:2423–35.
Li H, Ren B, Kang ZS, Huang LL. Comparison of cell death and accumulation of reactive oxygen species in wheat lines with or without Yr36 responding to Puccinia striiformis f. sp. tritici under low and high temperatures at seedling and adult-plant stages. Protoplasma. 2016a;253:787–802.
Li Q, Qin JF, Zhao YY, Zhao J, Huang LL, Kang ZS. Virulence analysis of sexual progeny of the wheat stripe rust pathogen recovered from wild barberry in Shaanxi and Gansu. Acta Phys Sin. 2016b;46:809–20.
Line RF, Chen XM. Successes in breeding for and managing durable resistance to wheat rusts. Plant Dis. 1995;79:1254–5.
Line RF, Qayoum A. Virulence, aggressiveness, evolution and distribution of races of Puccinia striiformis (the cause of stripe rust of wheat) in North America, 1968–1987. United States Department of Agriculture, Agricultural Research Service, Technical Bulletin Number 1788; 1992, 44 pp
Lipka U, Fuchs R, Kuhns C, Petutschnig E, Lipka V. Live and let die- Arabidopsis nonhost resistance to powdery mildews. Eur J Cell Biol. 2010;89:194–9.
Littlefield LJ, Health MC. Ultrastructure of rust fungi. New York: Academic Press; 1979.
Liu J, Zhu JK. A calcium sensor homolog required for plant salt tolerance. Science. 1998;280:1943–5.
Liu HM, Liu TG, Xu SC, Liu DQ, Chen WQ. Inheritance of yellow rust resistance in an elite wheat germplasm Xingzi 9104. Acta Agron Sin. 2006;32:1742–5.
Liu B, Xue XD, Cui S, Zhang XY, Han QM, Zhu L, Liang XF, Wang XJ, Huang LL, Chen XM, Kang ZS. Cloning and characterization of a wheat β-1,3-glucanase gene induced by the stripe rust pathogen Puccinia striiformis f. sp. tritici. Mol Biol Rep. 2010;37:1045–52.
Liu FR, Guo J, Bai PF, Duan YH, Wang XD, Cheng YL, Feng H, Huang LL, Kang ZS. Wheat TaRab7 GTPase is part of the signaling pathway in responses to stripe rust and abiotic stimuli. PLoS One. 2012a;7:e37146.
Liu J, Zhang Q, Chang Q, Zhuang H, Huang LL, Kang ZS. Cloning and characterization of the actin gene from Puccinia striiformis f. sp. tritici. Microbiol. Biotechnol. 2012b;28:2331.
Liu W, Frick M, Huel R, Nykiforuk CL, Wang X, Gaudet DA, Eudes F, Conner RL, Kuzyk A, Chen Q, Kang Z, Laroche A. The stripe rust resistance gene Yr10 encodes an evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Mol Plant. 2014;7:1740–55.
Liu J, Han LN, Huai BY, Zheng PJ, Chang Q, Guan T, Li D, Huang LL, Kang ZS. Down-regulation of a wheat alkaline/neutral invertase correlates with reduced host susceptibility to wheat sripe rust caused by Puccinia striiformis. J Exp Bot. 2015;66:7325–38.
Liu MJ, Peng Y, Li HY, Deng L, Wang XJ, Kang ZS. TaSYP71, a Qc-SNARE, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. Front Plant Sci. 2016a;7:544.
Liu P, Myo T, Ma W, Lan DY, Qi T, Guo J, Song P, Guo J, Kang ZS. TaTypA, a ribosome-binding GTPase protein, positively regulates wheat resistance to the stripe rust fungus. Front Plant Sci. 2016b.; https://doi.org/10.3389/fpls.2016.00873.
Llave C, Kasschau KD, Rector MA, Carrington JC. Endogenous and silencing-associated small RNAs in plants. Plant Cell. 2002;14:1605–19.
Loehrer M, Langenbach C, Goellner K. Characterization of nonhost resistance of Arabidopsis to the Asian soybean rust. Mol Plant-Microbe Interact. 2008;21:1421–30.
Loon LCV, Geraats BPJ, Linthorst HJM. Ethylene as a modulator of disease resistance in plants. Trends Plant Sci. 2006;11:184–91.
Lorrain S, Vailleau F, Balagué C, Roby D. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 2003;8:263–71.
Lowe I, Cantu D, Dubcovsky J. Durable resistance to the wheat rusts: integrating systems biology and traditional phenotype-based research methods to guide the deployment of resistance genes. Euphytica. 2011;179:69–79.
Lu M, Tang X, Zhou JM. Arabidopsis NHO1 is required for general resistance against Pseudomonas bacteria. Plant Cell. 2001;13:437–47.
Lu Y, Wang MN, Chen XM, See D, Chao SM, Jing JX. Mapping of Yr62 and a small effect QTL for high-temperature adult-plant resistance to stripe rust in spring wheat PI 192252. Theor Appl Genet. 2014;127:1449–59.
Luan S. The CBL–CIPK network in plant calcium signaling. Cell. 2008;14:37–42.
Lunderstädt J. Effect of rust infection on hexokinase activity and carbohydrate dissimilation in primary leaves of wheat. Can J Bot. 1966;44:1345–64.
Lupton FGH, Macer RCF. Inheritance of resistance to yellow rust (Puccinia glumarum Erikss. & Henn.) in seven varieties of wheat. Trans Br Mycol Soc. 1962;45:21–45.
Ma Q, Shang HS. Ultrastructural analysis of the interaction between Puccinia striiformis f. sp. tritici and wheat after thermal induction of resistance. J Plant Pathol. 2004;86:19–26.
Ma JB, Huang XL, Wang XJ, Chen XM, Qu ZP, Huang LL, Kang ZS. Identification of expressed genes during compatible interaction between stripe rust (Puccinia striiformis) and wheat using a cDNA library. BMC Genomics. 2009;10:586.
Maccaferri M, Zhang J, Bulli P, Abate Z, Chao S, Cantu D, Bossolini E, Chen X, Pumphrey M, Dubcovsky J. A genome-wide association study of resistance to stripe rust (Puccinia striiformis f. sp. tritici) in a worldwide collection of hexa-ploid spring wheat (Triticum aestivum L.). G3: Genes Genom Genet. 2015;5:449–65.
MacDonald PW, Strobel GA. Adenosine diphosphate-glucose pyrophosphorylase control of starch accumulation in rust-infected wheat leaves. Plant Physiol. 1970;46:126–35.
Mackrill JJ. Protein-protein interactions in intracellular Ca2+ -release channel function. Biochem J. 1999;337:345–61.
Magyarosy AC, Malkin R. Effect of powdery mildew infection of sugar beet on the content of electron carriers in chloroplasts. Physiol Plant Pathol. 1978;13:183–8.
Magyarosy AC, Schurmann P, Buchanan BB. Effect of powdery mildew infection on photosynthesis by leaves and chloroplasts of sugar beets. Plant Physiol. 1976;57:486–9.
Mains EB. Studies concerning heteroecious rusts. Mycologica. 1933;25:407–17.
Malca I, Murray HC, Zscheile FB. Organic conistituents in conidia of Eripsiplie gramninis tritici. Phytopathology. 1962;52:891–3.
Mallard S, Nègre S, Pouya S, Gaudet D, Lu ZX, Dedryver F. Adult plant resistance-related gene expression in ‘Camp Remy’ wheat inoculated with Puccinia striiformis. Mol Plant Pathol. 2008;9:213–25.
Manners JM. The host–haustorium interface in powdery mildews. Aust J Plant Physiol. 1989;16:45–52.
Mao C, Xu R, Szulc ZM, Bielawska A, Galadari SH, Obeid LM. Cloning and characterization of a novel human alkaline ceramidase. J Biol Chem. 2001;276:26577–88.
Marasas CN, Smale M, Singh RP. The economic impact of productivity maintenance research: breeding for leaf rust resistance in modern wheat. Agric Econ. 2003;29:253.
Mares DJ. A light and electron microscope study of the interaction of yellow rust (Puccinia striiformis) with a susceptible wheat cultivar. Ann Bot. 1979;43:183–9.
Mares DJ, Cousen S. The interaction of yellow rust (Puccinia striiformis) with winter wheat cultivars showing adult plant resistance: macroscopic and microscopic events associated with the resistant reaction. Physiol Plant Pathol. 1977;10:257–74.
Martinez-Garcia JF, Moyano E, Alcocer MJ, Martin C. Two bZIP proteins from Antirrhinum flowers preferentially bind a hybrid C-box/G-box motif and help to define a new sub-family of bZIP transcription factors. Plant J. 1998;13:489–505.
Maruta T, Noshi M, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S. H2O2-triggered retrograde signaling from chloroplasts to nucleus plays specific role in response to stress. J Biol Chem. 2012;287:11717–29.
Mashaal SF, Bama B, Király Z. Effect of photosynthesis inhibitors on wheat stem rust development. Acta Physiol Acad Sci Hung. 1981;16:45–8.
Matsumura H, Nirasawa S, Kiba A, Urasaki N, Saitoh H, Ito M, Kawai-Yamada M, Uchimiya H, Terauchi R. Overexpressionof Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. Plant J. 2003;33:425–34.
McIntosh RA, Wellings CR, Park RF. Wheat rusts: an atlas of resistance genes. Melbourne: CSIRO Publications; 1995.
McIntosh RA, Yamazaki Y, Dubcovsky J, Rogers WJ, Morris CF, Appels R, Xia XC. Catalogue of gene symbols for wheat. 2013. http://wheat.pw.usda.gov/GG2/Triticum/wgc/2013/GeneCatalogueIntroduction.pdf. Accessed 23 Dec 2016.
Melichar JPE, Berry S, Newell C, MacCormack R, Boyd LA. QTL identification and microphenotype characterization of the developmentally regulated yellow rust resistance. Theor Appl Genet. 2008;117:391–9.
Mellersh DG, Heath MC. An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Mol Plant-Microbe Interact. 2003;16:398–404.
Mendgen K. Microautoradiographic studies on hostparasite interactions. II. The exchange of 3H-lysine between Uromyces phaseoli and Phaseolus vulgaris. Arch Microbiol. 1979;123:129–35.
Mendgen K. Nutrient uptake in rust fungi. Phytopathology. 1981;71:983–9.
Mendgen K, Hahn M. Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 2002;7:352–6.
Mendgen K, Nass P. The activity of powdery-mildew haustoria after feeding the host cell with different sugars, as measured with a potentiometric cyanine dye. Planta. 1988;174:283–8.
Metzger RJ, Silbaugh BA. Inheritance of resistance to stripe rust and its association with brown glume color in Triticum aestivum L., “P.I. 178383”. Crop Sci. 1970;10:567–8.
Michelmore RW, Christopoulou M, Caldwell KS. Impacts of resistance gene genetics, function, and evolution on a durable future. Annu Rev Phytopathol. 2013;51:291–319.
Miklis M, Consonni C, Bhat RA, Lipka V, Schulze-Lefert P, Panstruga R. Barley MLO modulates actin-dependent and actin- Independent antifungal defense pathways at the cell periphery. Plant Physiol. 2007;144:1132–43.
Mirocha CJ, Zaki AI. Fluctuation in amount of starch in host plants invaded by rust and mildew fungi. Phytopathology. 1966;56:1220–2.
Mitchell DT. Carbon dioxide exchange by infected first leaf tissues susceptible to wheat stem rust. Trans Br Mycol Soc. 1979;72:63–8.
Mitchell DT, Fung AK, Lewis DH. Changes in the ethanol-soluble carbohydrate composition and acid invertase in infected first leaf tissues susceptible to crown rust of oat and wheat stem rust. New Phytol. 1978;80:381–92.
Mittapalli O, Shukle RH. Molecular characterization and responsive expression of a defender against apoptotic cell death homologue from the Hessian fly, Mayetiola destructor. Comp Biochem Physiol B: Biochem Mol Biol. 2008;149:517–23.
Moldenhauer J, Moerschbacher BM, Van der Westhuizen AJ. Histological investigation of stripe rust (Puccinia striiformis f. sp tritici) development in resistant and susceptible wheat cultivars. Plant Pathol. 2006;55:469–74.
Moldenhauer J, Pretorius ZA, Moerschbacher BM, Prins R, van der Westhuizen AJ. Histopathology and PR-protein markers provide insight into adult plant resistance to stripe rust of wheat. Mol Plant Pathol. 2008;9:137–45.
Moncrief ND, Kretsinger RH, Goodman M. Evolution of EF-hand calcium-modulated proteins I. Relationships based on amino acid sequences. J Mol Evol. 1990;30:522–62.
Montalbini P, Buchanan BB. Effect of a rust infection on photophosphorylation by isolated chloroplasts. Physiol Plant Pathol. 1974;4:191–6.
Montalbini P, Elstner EF. Ethylene evolution by rust-infected, detached bean (Phaseolus vulgaris L.) leaves susceptible and hypersensitive to Uromyces phaseoli (Pers.) Wint. Planta. 1977;135:301–6.
Morel JB, Dangl JL. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 1997;4:671–83.
Mueth NA, Ramachandran SR, Hulbert SH. Small RNAs from the wheat stripe rust fungus (Puccinia striiformis f. sp. tritici). BMC Genomics. 2015;16:718.
Mysore KS, Ryu CM. Nonhost resistance: how much do we know? Trends Plant Sci. 2004;9:97–104.
Nagarajan S, Nayar SK, Bahadur P. Race 13 (67S8) of Puccinia striiformis virulent on Triticum spelta var. album in India. Plant Dis. 1986;70:173.
Nahm MY, Kim SW, Yun D, Lee SY, Cho MJ, et al. Molecular and biochemical analyses of OsRab7, a rice Rab7 homolog. Plant Cell Physiol. 2003;44:1341–9.
Nakashima K, Yamaguchi-Shinozaki K. Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiol Plant. 2006;126:62–71.
Nalefski EA, Falke JJ. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci. 1996;5:2375–90.
Nandi A, Welti R, Shah J. The Arabidopsis thaliana dihydrox-yacetone phosphate reductase gene suppressor of fatty acid desaturase deficiency1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell. 2004;16:465–77.
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science. 2006;312:436–9.
Navazio L, Sponga L, Dainese P, Fitchette-Laine AC, Faye L, Baldan B, Mariani P. The calcium binding protein calreticulin in pollen of Liriodendron tulipifera L. Plant Sci. 1998;131:35–42.
Ng CK, Carr K, McAinsh MR, Powell B, Hetherington AM. Drought-induced guard cell signal transduction involves sphingosine-1-phosphate. Nature. 2001;410:596–9.
Niks RE. How specific is non-hypersensitive host and nonhost resistance of barley to rust and mildew fungi? J Integr Agric. 2014;13:244–54.
Niu XP, Renshaw-Gegg L, Miller L, Guiltinan MJ. Bipartite determinants of DNA-binding specificity of plant basic leucine zipper proteins. Plant Mol Biol. 1999;41:1–13.
Nühse TS, Bottrill AR, Jones AME, Peck SC. Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J. 2007;51:931–40.
O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435:839–43.
Ohme-Takagi M, Suzuk K, Shinshi H. Regulation of ethylene-induced transcription of defense genes. Plant Cell Physiol. 2000;41:1187–92.
Olsen AN, Ernst HA, Leggio LL, Skriver K. NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 2005;10:79–87.
Ouelhadj A, Kuschk P, Humbeck K. Heavy metal stress and leaf senescence induce the barley gene HvC2d1 encoding a calcium-dependent novel C2 domain-like protein. New Phytol. 2005;170:261–73.
Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767–801.
Owera SAP, Farrar JF, Whitbread R. Growth and photosynthesis in barley infected with brown rust. Physiol Plant Pathol. 1981;18:79–90.
Padmanabhan C, Zhang X, Jin H. Host small RNAs are big contributors to plant innate immunity. Curr Opin Plant Biol. 2009;12:465–72.
Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D. Control of leaf morphogenesis by microRNAs. Nature. 2003;425:257–63.
Panthee DR, Yuan JS, Wright DL, Marois JJ, Mailhot D, Stewart Jr CN. Gene expression analysis in soybean in response to the causal agent of Asian soybean rust (Phakopsora pachyrhizi Sydow) in an early growth stage. Funct Integr Genomics. 2007;7:291–301.
Paz-Ares J, Ghosal D, Wienand U, Peterson PA, Saedler H. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J. 1987;6:3553–8.
Pegg GF. Endogenous auxins in healthy and diseased plants. Encycl Plant Physiol, New Ser. 1976;4:560–81.
Perfect SE, Green JR. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol. 2001;2:101–8.
Periyannan S, Moore J, Ayliffe M, Bansal U, Wang X, Huang L, Deal K, Luo M, Kong X, Bariana H, et al. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science. 2013;341:786–8.
Pfeiffer E, Jäger K, Reisener HJ. Untersuchungen über Stoffwechselbeziehungen zwischen Parasit und Wirt am Beispiel von Puccinia graminis var. tritici auf Weizcn. II. Aufnahme von Hexosen aus dem Wirtsgewebe. Planta. 1969;85:194–201.
Porter K, Shimono M, Tian M, Day B. Arabidopsis actin- depolymerizing factor-4 links pathogen perception, defense activation and transcription to cytoskeletal dynamics. PLoS Pathog. 2012;8:e1003006.
Pozo-Guisado E, Merino JM, Mulero-Navarro S, Lorenzo-Benayas MJ, Centeno F, Alvarez-Barrientos A, Fernandez-Salguero PM. Resveratrol-induced apoptosis in MCF-7 human breast cancer cells involves a caspase-independent mechanism with downregulationof Bcl-2 and NF-kB. Int J Cancer. 2005;115:74–84.
Preeni T, Ayres PG. Transpiration and the water relations of faba bean (Vicia faba) infected by rust (Uromyces viciae-fabae). New Phytol. 1986;102:385–95.
Prins R, Ramburan VP, Pretorius ZA, Boyd LA, Boshoff WHP, Smith PH, Louw JH. Development of a doubled haploid mapping population and linkage map for the bread wheat cross Kariega × Avocet S. South Afr J Plant Soil. 2005;22:1–8.
Qi Y, Tsuda K, Nguyen LV, Wang X, Lin J, Murphy AS, Glazebrook J, Thordal-Christensen H, Katagiri F. Physical association of Arabidopsis hypersensitive induced reaction proteins (HIRs) with the immune receptor RPS2. J Biol Chem. 2011;286:31297–307.
Quick WA, Shaw M. The physiology of host-parasite relations. XIV. The effect of rust infection on the nucleic acid content of wheat leaves. Can J Bot. 1964;42:1531–40.
Raeder JM, Bever WM. Spore germination of Puccinia glumarum with notes on related species. Phytopathology. 1931;21:76–789.
Raffaele S, Rivas S, Roby D. An essential role for salicylic acid in AtMYB30-mediated control of the hypersensitive cell death program in Arabidopsis. FEBS Lett. 2006;580:3498–504.
Raffaele S, Vailleau F, Leger A, Joubes J, Mierch O, Huard C, Blee E, Mongrand S, Domergue F, Roby B. A MYB transcription factor regulates very long chain fatty acid biosynthesis for acti- vation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008;20:752–67.
Rahman M. Biochemical analysis of type II Metacaspase (mcII-Pa). Masters thesis. Swedish University of Agricultural Sciences, Uppsala, Sweden. 2010
Ramburan VP, Pretorius ZA, Louw JH, Boyd LA, Smith PH, Boshoff WHP, Prins R. A genetic analysis of adult plant resistance to stripe rust in the wheat cultivar Kariega. Theor Appl Genet. 2004;108:1426–33.
Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D. Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J. 2011;68:100–13.
Ravane S, Gakiere B, Job D, Douce R. The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci U S A. 1998;95:7805–12.
Reddy VS, Reddy AS. Proteomics of calcium-signaling components in plants. Phytochemistry. 2004;65:1745–76.
Reiter BG, Yudkin LY, Yudnika NB. Submicroscopic structure of Puccinia recondite f. sp. tritici and leaf cells of Triticum aestivum. Mikol Fitopatol. 1976;10:257–60.
Ren T, Qu F, Morris TJ. HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell. 2000;12:1917–26.
Ren RS, Wang MN, Chen XM, Zhang ZJ. Characterization and molecular mapping of Yr52 for high-temperature adult-plant resistance to stripe rust in spring wheat germplasm PI 183527. Theor Appl Genet. 2012;125:847–57.
Risk JM, Selter LL, Krattinger SG, Viccars LA, Richardson TM, Buesing G, Herren G, Lagudah ES, Keller B. Functional variability of the Lr34 durable resistance gene in transgenic wheat. Plant Biotechnol J. 2012;10:477–87.
Robert C, Bancal MO, Ney B, Lannou C. Wheat leaf photosynthesis loss due to leaf rust, with respect to lesion development and leaf nitrogen status. New Phytol. 2005;165:227–41.
Roberts EA, Chua J, Kyei GB, Deretic V. Higher order Rab programming in phagolysosome biogenesis. J Cell Biol. 2006;174:923–9.
Roelfs AP. Wheat and rye stem rust. In: Roelfs AP, Bushnell W, editors. The cereal rusts, vol. II. Orlando: Academic Press; 1985. p. 3–27.
Rohringer R. Untersuchungen zur Biochemie von Weizenkeimpflanzen nach Infektion mit Puccinia graminis tritici, Erikss und Henn, phR 126 A. Phytopathol Z. 1957;29:45–64.
Ron M, Avni A. The receptor for the fungal elicitor ethylene inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell. 2004;16:1604–15.
Rubiales D, Niks RE. Characterization of Lr34, a major gene conferring nonhypersensitive resistance to wheat leaf rust. Plant Dis. 1995;79:1208–12.
Rubio-Somoza I, Weigel D. MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 2011;16:258–64.
Ruf IK, Rhyne PW, Yang H, Borza C, Hutt-Fletcher LM, Cleveland JL, Sample JT. Epstein-Barr virus regulates c-MYC, apoptosis and tumorigenicity in Burkitt lymphoma. Mol Cell Biol. 1999;19:1651–60.
Rushton PJ, Somssich IE. Transcriptional control of plant genes responsive to pathogens. Curr Opin Plant Biol. 1998;1:311–5.
Ryerson E, Li A, Young JP, Heath MC. Changes in abscisic acid levels in bean leaves during the initial stages of host and nonhost reactions to rust fungi. Physiol Mol Plant Pathol. 1993;43:265–73.
Rzewuski G, Cornell KA, Rooney L, Burstenbinder K, Wirtz M, Hell R, Sauter M. OsMTN encodes a 50-methylthioadenosine nucleosidase that is up-regulated during submergence-induced ethylene synthesis in rice (Oryza sativa L.). J Exp Bot. 2007;58:1505–14.
Saintenac C, Zhang W, Salcedo A, Rouse MN, Trick HN, Akhunov E, Dubcovsky J. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science. 2013;341:783–6.
Samborski DJ, Rohringer R, Person C. Effect of rust-inhibiting compounds on the metabolism of wheat leaves. Can J Bot. 1961;39:1019–27.
Sanders D, Brownlee C, Harper JF. Communicating with calcium. Plant Cell. 1999;11:691–706.
Sauter M, Lorbiecke R, Ouyang B, Pochapsky TC, Rzewuski G. The immediate-early ethylene response gene OsARD1 encodes an acireductone dioxygenase involved in recycling of the ethylene precursor S-adenosylmethionine. Plant J. 2005;44:718–29.
Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R, Menzel D, Salinas J, Mancuso S, Valpuesta V, Baluska F, Botella MA. Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell. 2008;20:3374–88.
Scianimanico S, Desrosiers M, Dermine JF, Méresse S, Descoteaux A, et al. Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes. Cell Microbiol. 1999;1:19–32.
Shafiei R, Hang C, Kang J-G, Loake GJ. Identification of loci controlling nonhost disease resistance in Arabidopsis against the leaf rust pathogen Puccinia triticina. Mol Plant Pathol. 2007;8:773–84.
Shang HS, Zhang H, Li ZQ. RNA synthesis in primary leaves of stripe rusted wheat. Plant Physiol Commun. 1994;30:266–8.
Sharma YK, Davis KR. The effects of ozone on antioxidant responses in plants. Free Radic Biol Med. 1997;23:480–8.
Sharma P, Dubey RS. Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul. 2005;46:209–21.
Sharma-Poudyal D, Chen XM, Wan AM, Zhan GM, Kang ZS, Cao SQ, Jin SL, Morgounov A, Akin B, Mert Z, Shah SJA, Bux H, Ashraf M, Sharma RC, Madariaga R, Puri KD, Wellings C, Xi KQ, Wanyera R, Manninger K, Ganzález MI, Koyda M, Sanin S, Patzek LJ. Virulence characterization of international collections of the wheat stripe rust pathogen, Puccinia striiformis f. sp. tritici. Plant Dis. 2013;97:379–86.
Shaw M. The physiology and host–parasite relations of the rusts. Annu Rev Phytopathol. 1963;1:259–94.
Shaw M, Colotelo N. The physiology of host–parasite relations. VII. The effect of stem rust on the nitrogen and amino acids in wheat leaves. Can J Bot. 1961;39:1351–72.
Shaw M, Hawkins AR. The physiology of host–parasite relations. V. A preliminary examination of the level of free endogenous indoleacetic acid in rusted and mildewed cereal leaves and their ability to decarboxylate exogenously supplied radioactive indoleacetic acid. Can J Bot. 1958;36:1–16.
Shaw M, Manocha MS. Fine structure in detached, senescing wheat leaves. Can J Bot. 1965a;43:747–55.
Shaw M, Manocha MS. The physiology of host–parasite relations. XV. Fine structure in rust-infected wheat leaves. Can J Bot. 1965b;43:1285–92.
Shaw M, Bhattacharya PK, Quick WA. Chloroph, protein and nucleicacid levels in detached, senescing wheat leaves. Can J Bot. 1958;43:739–46.
Shen X, Li HY, Jia QZ, Feng HQ, Li MQ, Liang HG. Influence of wheat stripe rust infection on photosynthetic function and expression protein D1 of wheat leaves. Acta Ecol Sin. 2008;28:669–76.
Shimada C, Lipka V, O’Connell R, Okuno T, Schulze-Lefert P, Takano Y. Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant-Microbe Interact. 2006;19:270–9.
Siberil Y, Doireau P, Gantet P. Plant bZIP G-box binding factors: modular structure and activation mechanisms. FEBS J. 2001;268:5655–66.
Siebert R. Biochemische Untersuchungen zum Wirt-Parasit-Verhältnis am Beispiel von Puccinia graminis tritici. Phytopathol Z. 1961;40:221–44.
Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development. 2007;134:1051–60.
Silverman W. The development of stem rust on wheat leaves treated with some sugars and sugar alcohols. Phytopathology. 1960;50:114–9.
Singh RP. Association between gene Lr34 for leaf rust resistance and leaf tip necrosis in wheat. Crop Sci. 1992a;32:874.
Singh RP. Genetic association of leaf rust resistance gene Lr34 with adult plant resistance to stripe rust in bread wheat. Phytopathology. 1992b;82:835–8.
Singh K, Foley RC, Oñate-Sánchez L. Transcription factors in plant defense and stress responses. Curr Opin Plant Biol. 2002;5:430–6.
Smith RCG, Heritage AD, Stapper M, Barrs MD. Effect of stripe rust (Puccinia striiformis West.) and irrigation on the yield and foliage temperature of wheat. Field Crop Res. 1986;14:39–51.
Sohn J, Voegele RT, Mendgen K, Hahn M. High level activation of vitamin B1 biosynthesis genes in haustoria of the rust fungus Uromyces fabae. Mol Plant-Microbe Interact. 2000;13:629–36.
Sorensen CK, Justesen AF, Hovmoller MS. 3-D imaging of temporal and spatial development of Puccinia striiformis haustoria in wheat. Mycologia. 2012;104:1381–9.
Spanu PD. The genomics of obligate (and nonobligate) biotrophs. Annu Rev Phytopathol. 2012;50:91–109.
Spoel SH, Dong X. How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol. 2012;12:89–100.
Staiger CJ, Gibbon BC, Kovar DR, Zonia LE. Profilin and actin-depolymerizing factor: modulators of actin organization in plants. Trends Plant Sci. 1997;2:275–81.
Stein N, Feuillet C, Wicker T, Schlagenhauf E, Keller B. Subgenome chromosome walking in wheat: a 450-kb physical contig in Triticum monococcum L. spans the Lr10 locus in hexaploid wheat (Triticum aestivum L.). Proc Natl Acad Sci U S A. 2000;97:13436–41.
Stoddart JL. Leaf senescence. In: Jeffcoat B (ed) Aspects and prospects of plant growth regulators. Wantage: British Plant Growth Regulatory Group, ARC Letcombe Laboratory; 1981. pp 51–63
Straib W. Untersuchungen über das vorkommen physiologischer rassen des gelbrostes (Puccinia glumarum) in den Jahren 1935–1936 und über die Agressivität einiger neuer Formen auf Getreide und Gräsern. Arb. Biol. Reichsanst. Land= Forstwirtsch. Berlin-Dahlem. 1937;22:91–119.
Struck C, Ernst M, Hahn M. Characterization of a developmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol Plant Pathol. 2002;3:23–30.
Struck C, Müller E, Martin H, Lohaus G. The Uromyces fabae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol Plant Pathol. 2004;5:183–9.
Stubbs RW. Stripe rust. In: Roelfs AP, Bushnell W, editors. The cereal rusts, vol. II. Orlando: Academic Press; 1985. p. 61–101.
Stulemeijer IJ, Stratmann JW, Joosten MH. Tomato mitogen activated protein kinases LeMPK1, LeMPK2, and LeMPK3are activated during the Cf-4/Avr4-induced hypersensitive response and have distinct phosphorylation specificities. Plant Physiol. 2007;144:1481–94.
Su H, Conner RL, Graf RJ, Kuzyk AD. Virulence of Puccinia striiformis f. sp. tritici, cause of stripe rust on wheat, in western Canada from 1984 to 2002. Can J Plant Pathol. 2003;25:312–9.
Sunkar R, Zhu J-K. Novel and stress-regulated microRNAs andother small RNAs from Arabidopsis. Plant Cell. 2004;16:2001–19.
Sutton PN, Henry MJ, Hall JL. Glucose, and not sucrose, is transported from wheat to wheat powdery mildew. Planta. 1999;208:426–30.
Syamananda R, Staples RC. The carbohydrate content of rusted corn leaves. Contrib Boyce Thompson Inst. 1963;22:1–8.
Szabo L. Hidden robbers: the role of fungal haustoria in parasitism of plants. Proc Natl Acad Sci. 2001;98:7654–5.
Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol. 2010;11:515–28.
Takezawa D. A rapid induction by elicitors of the mRNA encoding CCD-1, a 14 kDa Ca2+ -binding protein in wheat cultured cells. Plant Mol Biol. 2000;42:807–17.
Tanaka Y, Makishima T, Sasabe M, Ichinose Y, Shiraishi T, Nishimoto T, Yamada T. dad-1, a putative programmed cell death suppressor gene in rice. Plant Cell Physiol. 1997;38:379–83.
Tang CL, Wang XJ, Duan XY, Wang XD, Huang LL, Kang ZS. Functions of the lethal leaf-spot 1 gene in wheat cell death and disease tolerance to Puccinia striiformis. J Exp Bot. 2013;64:2955–69.
Tang CL, Deng L, Chang D, Chen ST, Wang XJ, Kang ZS. TaADF3, an actin-depolymerizing factor, negatively modulates wheat resistance against Puccinia striiformis. Front Plant Sci. 2016;6:1214.
Tani T, Yamamoto H. RNA and protein synthesis and enzyme changes during infection. In: Daly JM, Uritani I, editors. Recognition and specificity in plant host–parasite interaction. Baltimore: University Park Press; 1979. p. 273–87.
Tani T, Yoshikawa M, Naito N. Effect of rust infection of oat leaves on cytoplasmic and chloroplast ribosomal ribonucleic acids. Phytopathology. 1973;63:491–4.
Thomma BP, Eggermont K, Tierens KF, Broekaert WF. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiol. 1999;121:1093–102.
Tian M, Chaudhry F, Ruzicka DR, Meagher RB, Staiger CJ, Day B. Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol. 2009;150:815–24.
Tian CM, Kang ZS, Li ZQ, Zhap YX. Researches on the histology and cytology of poplar leaf rust. J Northwest Forestry Univ. 2001;16:43–9.
Tieman DM, Ciardi JA, Taylor MG, Klee HJ. Members of the tomato LeEIL (EIN3-like) gene family are functionally redundant and regulate ethylene responses throughout plant development. Plant J. 2001;26:47–58.
Tissera P, Ayres PG. Endogenous ethylene affects the behavior of stomata in epidermis isolated from rust infected faba bean (Vicia faba L.). New Phytol. 1986;104:53–61.
Tranzschel W. Promežutočnye chozjaeva rzavčiny chlebov i ich der UdSSR. (The alternate hosts of cereal rust fungi and their distribution in the UdSSR). Bull Plant Prot Ser. 1934;2:4–40.
Uauy C, Brevis JC, Chen XM, Khan IA, Jackson LF, Chicaiza O, Distelfeld A, Fahima T, Dubcovsky J. High-temperature adult plant (HTAP) stripe rust resistance gene Yr36 from Triticum turgidum ssp. dicoccoides is closely linked to the grain protein content locus Gpc-B1. Theor Appl Genet. 2005;112:97–105.
Umezawa T, Fujita M, Fujita Y, Yamaquchi-Shinozaki K, Shinozaki K. Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol. 2006;17:113–22.
Umnov AM, Artemenko EN, Chkanikov DI. The presence of indolyl-3-acetic acid in uredospores of wheat stem rust. Mikol Fitopatol. 1978;12:222–7.
Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylides C. A R2R3-MYB gene, AtMYB30, acts as appositive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci U S A. 2002;99:10179–84.
Van Loon L. Pathogenesis-related proteins. Plant Mol Biol. 1985;4:111–6.
Van Troys M, Huyck L, Leyman S, Dhaese S, Vandekerkhove J, Ampe C. Ins and outs of ADF/cofilin activity and regulation. Eur J Cell Biol. 2008;87:649–67.
Vannini C, Iriti M, Bracale M, Locatelli F, Faoro F, Croce P, Pirona R, Di Maro A, Coraggio I, Genga A. The ectopic expression of the rice OsMyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol. 2006;69:26–42.
Vannini C, Campa M, Iriti M, Genga A, Faoro F, Carravieri S, Rotino GL, Rossoni M, Spinardi A, Bracale M. Evaluation of transgenic tomato plants ectopically expressing the rice OsMyb4 gene. Plant Sci. 2007;173:231–9.
Ventelon-Debout M, Delalande F, Brizard JP, Diemer H, Van Dorsselaer A, Brugidou C. Proteome analysis of cultivar specific deregulations of Oryza sativa indica and O. sativa japonica cellular suspensions undergoing rice yellow mottle virus infection. Proteomics. 2004;4:216–25.
Venugopal SC, Chanda B, Vaillancourt L, Kachroo A, Kachroo P. The common metabolite glycerol-3-phosphate is a novel regulator of plant defense signaling. Plant Signal Behav. 2009;4:746–9.
Vercammen D, Belenghi B, Van De Cotte B, Beunens T, Gavigan JA, De Rycke R, Brackenier A, Inzé D, Harris JL, Van Breusegem F. Serpin1 of Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J Mol Biol. 2006;364:625–36.
Vieira OV, Bucci C, Harrison RE, Trimble WS, Lanzetti L, et al. Modulation of Rab5 and Rab7 recruitment to phagosomes by phosphatidylinositol 3-kinase. Mol Cell Biol. 2003;23:2501–14.
Voegele RT, Mendgen K. Rust haustoria: nutrient uptake and beyond. New Phytol. 2003;159:93–100.
Voegele RT, Mendgen KW. Nutrient uptake in rust fungi: how sweet is parasitic life? Euphytica. 2011;179:41–55.
Voegele RT, Struck C, Hahn M, Mendgen K. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci U S A. 2001;98:8133–8.
Voegele RT, Wirsel S, Ulla Möll U, Lechner M, Mendgen K. Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol Plant-Microbe Interact. 2006;19:625–34.
von Broembsen SL, Hadwiger LA. Characterization of disease resistance responses in certain gene-for-gene interactions between flax and Melampsora lini. Physiol Plant Pathol. 1972;2:207–15.
Wahl R, Wippel K, Goos S, Kämper J, Sauer N. A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 2010;8:e1000303.
Walters DR, McRoberts N, Fitt BDL. Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biol Rev Camb Philos Soc. 2008;83:79–102.
Wan AM, Chen XM. Variation of telial formation in the Puccinia striiformis f. sp. tritici population. Phytopathology. 2016;S4:206–7.
Wan AM, Muleta KT, Zegeye H, Hundie B, Pumphrey MO, Chen XM. Virulence characterization of wheat stripe rust fungus Puccinia striiformis f. sp. tritici in Ethiopia and evaluation of Ethiopian wheat germplasm for resistance to races of the pathogen from Ethiopia and the United States. Plant Dis. 2017;101:73–80.
Wang BT, Shang HS. The relation between the high-temperature resistance of wheat to stripe rust and lignin synthesis. Acta Phys Sin. 1996;23:229–34.
Wang MN, Chen XM. First Report of Oregon grape (Mahonia aquifolium) as an alternate host for the wheat stripe rust pathogen (Puccinia striiformis f. sp. tritici) under artificial inoculation. Plant Dis. 2013;97:839.
Wang MN, Chen XM. Barberry does not function as an alternate host for Puccinia striiformis f. sp. tritici in the U. S. Pacific Northwest due to teliospore degradation and barberry phenology. Plant Dis. 2015;99:1500–6.
Wang Y, Kang ZS, Li ZQ. Study on heterokaryon distribution of Puccinia striiformis f. sp. tritici West. in the different mountain areas of Tianshui. J Triticeae Crops. 2004;24:110–3.
Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS. Histochemical studies on the accumulation of reactive oxygen species (O2 − and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol. 2007;71:230–9.
Wang F, Zhong NQ, Gao P, Wang GL, Wang HY, Xia GX. SsTypA1, a chloroplast-specific TypA/BipA-type GTPase from the halophytic plant Suaeda salsa, plays a role in oxidative stress tolerance. Plant Cell Environ. 2008a;31:982–94.
Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu CM, Woods-Tör A, Zipfel C, de Wit PJ, Jones JD, Tör M, Thomma BP. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol. 2008b;147:503–17.
Wang MN, Coram TE, Ling P, Boyd L, Chen XM. High-resolution genetic and physical mapping of the Yr5 gene for resistance to stripe rust of wheat. Phytopathology. 2008c;98:S166.
Wang XJ, Tang CL, Zhang G, Li YC, Wang CF, Liu B, Qu ZP, Zhao J, Han QM, Huang LL, Chen XM, Kang ZS. cDNA-AFLP analysis reveals differential gene expression in compatible interaction of wheat challenged with Puccinia striiformis f. sp. tritici. BMC Genomics. 2009a;10:289.
Wang XY, Li Q, Niu XW, Chen HY, Xu LL, Qi CK. Characterization of a canola C2 domain gene that interacts with PG, an effector of the necrotrophic fungus Sclerotinia sclerotiorum. J Exp Bot. 2009b;60:2613–20.
Wang XJ, Liu W, Chen XM, Tang CL, Dong YL, Ma JB, Huang XL, Wei GR, Han QM, Huang LL, Kang ZS. Differential gene expression in incompatible interaction between wheat and stripe rust fungus revealed by cDNA-AFLP and comparison to compatible interaction. BMC Plant Biol. 2010a;10:9.
Wang XJ, Tang CL, Deng L, Cai GL, Liu XY, Liu B, Han QM, Buchenauer H, Wei GR, Han DJ, Huang LL, Kang ZS. Characterization of a pathogenesis-related thaumatin-like protein gene TaPR5 from wheat induced by stripe rust fungus. Physiol Plant. 2010b;139:27–38.
Wang GF, Wei X, Fan R, Zhou H, Wang X, Yu C, Dong L, Dong Z, Wang X, Kang Z, Ling H, Shen QH, Wang D, Zhang X. Molecular analysis of common wheat genes encoding three types of cytosolic heat shock protein 90 (Hsp90): functional involvement of cytosolic Hsp90s in the control of wheat seedling growth and disease resistance. New Phytol. 2011a;191:418–31.
Wang MN, Wan AM, Chen XM, Evans CK. Barberry is more important as an alternate host for stem rust than for stripe rust in the U.S. Pacific Northwest. In: Oral presentations, poster abstracts, participants and program of BGRI technical workshop, June 13–16, 2011, St. Paul, MN, USA. 2011b, pp 166
Wang XJ, Tang CL, Zhang H, Xu JR, Liu B, Lv J, Han DJ, Huang LL, Kang ZS. TaDAD2, a negative regulator of programmed cell death, is important for the interaction between wheat and the stripe rust fungus. Mol Plant-Microbe Interact. 2011c;24:79–90.
Wang XD, Wang XJ, Feng H, Tang CL, Bai PF, Wei GR, Huang LL, Kang ZS. TaMCA4, a novel wheat metacaspase gene functions in programmed cell death induced by the fungal pathogen Puccinia striiformis f. sp. tritici. Mol Plant-Microbe Interact. 2012a;25:755–64.
Wang XJ, Tang CL, Huang XL, Li FF, Chen XM, Zhang G, Sun YF, Han DJ, Kang ZS. Wheat BAX inhibitor-1 contributes to wheat resistance to Puccinia striiformis. J Exp Bot. 2012b;63:4571–84.
Wang X, Richards J, Gross T, Druka A, Kleinhofs A, Steffenson B, Acevedo M, Brueggeman R. The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol Plant-Microbe Interact. 2013;26:407–18.
Wang XD, Wang XJ, Deng L, Chang HT, Dubcovsky J, Feng H, Han QM, Huang LL, Kang ZS. Wheat TaNPSN SNARE homologues are involved in vesicle-mediated resistance to stripe rust (Puccinia striiformis f. sp. tritici). J Exp Bot. 2014a;65:4807–20.
Wang B, Sun YF, Song N, Wei JP, Wang XJ, Feng H, Yin ZY, Kang ZS. MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiol Biochem. 2014b;80:90–6.
Wang MN, Wan AM, Chen XM. Barberry as alternate host is important for Puccinia graminis f. sp. tritici but not for Puccinia striiformis f. sp. tritici in the U.S. Pacific Northwest. Plant Dis. 2015;99:1507–16.
Wang XD, Yang BJ, Li K, Kang ZS, Cantu D, Dubcovski J. A conserved Puccinia striiformis protein interacts with wheat NPR1 and reduces induction of pathogenesis-related genes in response to pathogens. Mol Plant-Microbe Interact Online: http://dx.doi.org/10.1094/MPMI-10-16-0207-R. 2016a.
Wang ZY, Zhao J, Chen XM, Peng YL, Ji JJ, Zhao SL, Lv YJ, Huang LL, Kang ZS. Virulence variation of Puccinia striiformis f. sp. tritici isolates collected from Berberis spp. in China. Plant Dis. 2016b;100:131–8.
Watanabe N, Lam E. Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem. 2005;280:14691–9.
Watanabe N, Lam E. Calcium-dependent activation and autolysis of Arabidopsis metacaspase 2d. J Biol Chem. 2011;286:10027.
Watanabe S, Shimada TL, Hiruma K, Takano Y. Pathogen infection trial increases the secretion of proteins localized in the endoplasmic reticulum body of Arabidopsis. Plant Physiol. 2013;163:659–64.
Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH. Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics. 2002;162:381–94.
Wegele H, Muller L, Buchner J. Hsp70 and Hsp90 – a relay team for protein folding. Rev Physiol Bioch P. 2004;151:1–44.
Wei T, Zhang C, Hou X, Sanfaçon H, Wang A. The SNARE protein Syp71 is essential for turnip mosaic virus infection by mediating fusion of virus-induced vesicles with chloroplasts. PLoS Pathog. 2013;9:e1003378.
Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, Huang HD, Jin H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science. 2013;342:118–23.
Whetstone RD, Atkinson TA, Spaulding DD. Berberidaceae. In: Flora of North America, Vol. 3. Website: www.eFloras.org. 1989. Accessed 23 Dec 2016.
Whitney HS, Shaw M, Naylor JM. The physiology of host–parasite relations. XII. A cytophotometric study of the distribution of DNA and RNA in rust-infected leaves. Can J Bot. 1962;40:1533–44.
Wildermuth MC, Dewdney J, Wu G, Ausubel FM. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. 2001;414:562–5.
William HM, Singh RP, Huerta-Espino J, Ortiz-Islas S, Hoisington D. Molecular marker mapping of leaf rust resistance gene Lr46 and its association with stripe rust resistance gene Yr29 in wheat. Phytopathology. 2003;93:153–9.
Williamson CE. Ethylene, a metabolic product of diseased or injured plants. Phytopathology. 1950;40:205–8.
Woltering EJ. Death proteases come alive. Trends Plant Sci. 2004;9:469–72.
Woods AM, Gay JL. The interface between haustoria of Puccinia poarum (monokaryon) and Tussilago farfara. Physiol Mol Plant Pathol. 1987;30:167–85.
Wright RG, Lennard JH. Mitosis in Puccinia striiformis. Light Microsc Trans Br Mycol Soc. 1978;70:91–8.
Wrigley CW, Webster HL. The effect of stem rust infection on the soluble proteins of wheat leaves. Aust J Biol Sci. 1966;19:895–901.
Wynn WK. Photosynthetic phosphorylation by chloroplasts isolated from rust-infected oats. Phytopathology. 1963;53:1376–7.
Xia N, Zhang G, Liu XY, Deng L, Cai GL, Zhang Y, Wang XJ, Zhao J, Huang LL, Kang ZS. Characterization of a novel wheat NAC transcription factor gene involved in defense response against stripe rust pathogen infection and abiotic stresses. Mol Biol Rep. 2010a;37:3703–12.
Xia N, Zhang G, Sun YF, Zhu L, Xu LS, Chen XM, Liu B, Yu YT, Wang XJ, Huang LL, Kang ZS. TaNAC8, a novel NAC transcription factor gene in wheat, responds to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol. 2010b;74:394–402.
Xie Q, Frugis G, Colgan D, Chua NH. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 2000;14:3024–36.
Xoconostle-Cazares B, Xiang Y, Ruiz-Medrano R, Wang HL, Monzer J, Yoo BC, McFarland KC, Franceschi VR, Lucas WJ. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science. 1999;283:94–8.
Xu H, Heath MC. Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell. 1998;10:585–98.
Xu LS, Jia JG, Lv J, Liang XF, Han DJ, Huang LL, Kang ZS. Characterization of the expression profile of a wheat aci-reductone-dioxygenase-like gene in response to stripe rust pathogen infection and abiotic stresses. Plant Physiol Biochem. 2010;48:461–8.
Yahiaoui N, Srichumpa P, Dudler R, Keller B. Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J. 2004;37:528–38.
Yamaguchi-Shinozaki K, Shinozaki K. Organization of cis-acting regulatory elements in osmotic- and cold-stress responsive promoters. Trends Plant Sci. 2005;10:88–94.
Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 2006;57:781–803.
Yamazaki T, Takat N, Uemura M, Kawamura Y. Arabidopsis synaptotagmin SYT1, a type I signal-anchor protein, requires tandem C2 domains for delivery to the plasma membrane. J Biol Chem. 2010;285:23165–76.
Yang CY, Shang HS, Li ZQ. Change of nitrogen in wheat leaves infected by stripe rust fungi. Acta Agric Beoreali-occidentalis Sin. 1991;S1:18–22.
Yang H, Li Y, Hua J. The C2 domain protein BAP1 negatively regulates defense responses in Arabidopsis. Plant J. 2006a;48:238–48.
Yang S, Yang H, Grisa WP, Sanchatjate S, Fink GR, Sun Q, Hua J. The BON/CPN gene family represses cell death and promotes cell growth in Arabidopsis. Plant J. 2006b;45:166–79.
Yang H, Yang S, Li Y, Hua J. The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death. Plant Physiol. 2007;145:135–46.
Yang WQ, Lai Y, Li MN, Xu WY, Xue YB. A novel C2-domain phospholipid-binding protein, OsPBP1, is required for pollen fertility in rice. Mol Plant. 2008;1:770–85.
Yang YH, Zhao J, Liu P, Xing HJ, Li CC, Wei GR, Kang ZS. Glycerol-3-phosphate metabolism in wheat contributes to systemic acquired resistance against Puccinia striiformis f. sp. tritici. PLoS One. 2013;8:e81756.
Yang YH, Zhao J, Xing HJ, Wang JY, Zhou K, Zhan GM, et al. Different non-host resistance responses of two rice subspecies, japonica and indica, to Puccinia striiformis f. sp tritici. Plant Cell Rep. 2014;33:423–33.
Yang YH, Yu Y, Bi CW, Kang ZS. Quantitative proteomics reveals the defense response of wheat against Puccinia striiformis f. sp. tritici. Sci Rep. 2016;6:34261.
Yao Y, Guo G, Ni Z, Sunkar R, Du J, Zhu JK, Sun Q. Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol. 2007;8:R96.
Yao JN, Zhang HC, Zhao J, Han QM, Cheng YL, Huang LL, Kang ZS. Histological and ultrastructural observation of teliospore formation in Puccinia striiformis f. sp. tritici. Mycosystema. 2012;31:560–6.
Yin CT, Chen XM, Wang XJ, Han QM, Kang ZS, Hulbert S. Generation and analysis of expression sequence tags from haustoria of the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. BMC Genomics. 2009;10:626.
Yin CT, Jurgenson JE, Hulbert SH. Development of a host-induced RNAi system in the wheat stripe rust fungus Puccinia striiformis f. sp. tritici. Mol Plant-Microbe Interact. 2011;24:554–61.
Yin CT, Park JJ, Gang DR, Hulbert SH. Characterization of traptophan 2-monooxygenase gene from Puccinia graminis f. sp. tritici involved in auxin biosynthesis and rust pathoenicity. Mol Plant-Microbe Interact. 2014;27:227–35.
Yin SN, Wang CF, Jiao M, Li F, Han QM, Huang LL, Zhang HC, Kang ZS. Subcellular localization of calcium in the incompatible and compatible interactions of wheat and Puccinia striiformis f. sp. tritici. Protoplasma. 2015;252:103–16.
Yin SN, Gao ZJ, Wang CF, Huang LL, Kang ZS, Zhang HC. Nitric oxide and reactive oxygen species coordinately regulate the germination of Puccinia striiformis f. sp. tritici urediniospores. Front Microbiol. 2016;7:178.
Ying JS. Berberidaceae. In: The Editorial Committee of Flora of China (ed) Flora of China, Vol. 29. Beijing: Science Press; 2001. pp 54–249.
Yu YH, Xia Xin Li, Yin WL, Zhang HC. Comparative genomics analysis of CIPK gene family in Arabidopsis and Populus. Plant Growth Regul. 2007;52:101–10.
Yu XM, Yu XD, Qu ZP, Huang XJ, Guo J, Han QM, Zhao J, Huang LL, Kang ZS. Cloning of a putative hypersensitive induced reaction gene from wheat infected by stripe rust fungus. Gene. 2008;407:193–8.
Yu X, Wang X, Wang C, Chen X, Qu Z, Yu X, Han Q, Zhao J, Guo J, Huang L, Kang Z. Wheat defense genes in fungal (Puccinia striiformis) infection. Funct Integr Genomics. 2010;10:227–39.
Yu XM, Wang XJ, Huang XJ, Buchenauer H, Han QM, Guo J, Zhao J, Qu ZP, Huang LL, Kang ZS. Cloning and characterization of a wheat neutral ceramidase gene Ta-CDase. Mol Biol Rep. 2011;38:3447–54.
Zenser N, Ellsmore A, Leasure C, Callis J. Auxin modulates the degradation rate of Aux/IAA proteins. Proc Natl Acad Sci U S A. 2001;98:11795–800.
Zhang H, Shang HS, Li ZQ. Changes in polyribosome and protein synthesis of wheat leaves in the early stage of stripe-rust infection. Acta Phys Sin. 1994;20:339–45.
Zhang HC, Han QM, Wang CF, Huang LL, Zhang QQ, Kang ZS. Histology and ultrastructure of resistant mechanism of a new wheat material Yilipu to Puccinia striiformis. Acta Phys Sin. 2008a;38:153–64.
Zhang Y, Qu Z, Zheng W, Liu B, Wang X, Xue X, et al. Stage-specific gene expression during urediniospore germination in Puccinia striiformis f. sp. tritici. BMC Genomics. 2008b;9:203.
Zhang Y, Zhang G, Xia N, Wang XJ, Huang LL, Kang ZS. Cloning and characterization of a bZIP transcription factor gene in wheat and its expression in response to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol. 2008c;73:88–94.
Zhang G, Dong YL, Zhang Y, Li YM, Wang XJ, Han QM, Guo J, Huang LL, Kang ZS. Cloning and characterization of a novel hypersensitive induced-reaction gene from wheat infected by stripe rust pathogen. J Phytopathol. 2009;157:722–8.
Zhang G, Li YM, Zhang Y, Dong YL, Wang XJ, Wei GR, Huang LL, Kang ZS. Cloning and characterization of a pathogenesis related protein gene TaPR10 from wheat induced by stripe rust pathogen. Agric Sci China. 2010;9:549–56. (in Chinese)
Zhang LX, Li ZF, Quan RD, Li GJ, Wang RG, Huang RF. An AP2 domain-containing gene, ESE1, targeted by the ethylene signaling component EIN3 is important for the salt response in Arabidopsis. Plant Physiol. 2011a;157:854–65.
Zhang W, Gao S, Zhou X, Chellappan P, Chen Z, Zhang X, Fromuth N, Coutino G, Coffey M, Jin H. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol. 2011b;75:93–105.
Zhang X, Zhao H, Gao S, Wang WC, Katiyar-Agarwal S, Huang HD, Raikhel N. Arabidopsis Argonaute 2 regulates innate immunity via miRNA393*-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol Cell. 2011c;42:356–66.
Zhang HC, Wang CF, Chen YL, Chen XM, Han QM, Huang LL, Wei GR, Kang ZS. Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Rep. 2012;31:2121–37.
Zhang G, Sun YF, Li YM, Dong YL, Huang XL, Yu YT, Wang JM, Wang XM, Wang XJ, Kang ZS. Characterization of a wheat C2 domain protein encoding gene regulated by stripe rust and abiotic stresses. Biol Plant. 2013;57:701–10.
Zhao J, Wang L, Wang ZY, Chen XM, Zhang HC, Yao JN, Zhan GM, Chen W, Huang LL, Kang ZS. Identification of eighteen Berberis species as alternate hosts of Puccinia striiformis f. sp. tritici and virulence variation in the pathogen isolates from natural infection of barberry plants in China. Phytopathology. 2013;103:927–34.
Zhao J, Yang YH, Kang ZS. Proteomic analysis of rice nonhost resistance to Puccinia striiformis f. sp. tritici using two-dimensional electrophoresis. Int J Mol Sci. 2014;15:21644–59.
Zhao J, Zhao SL, Peng YL, Qin JF, Huang LL, Kang ZS. Investigation on geographic distribution and identification of six Berberis spp. serving as alternate host for P. striiformis f. sp. tritici in Linzhi, Tibet. Acta Phys Sin. 2016;46:103–11.
Zheng W, Huang L, Huang J, Wang X, Chen X, Zhao J, Guo J, Zhuang H, Qiu C, Liu J, Liu H, Huang X, Pei G, Zhan G, Tang C, Cheng Y, Liu M, Zhang J, Zhao Z, Zhang S, Han Q, Han D, Zhang H, Zhao J, Gao X, Wang J, Ni P, Dong W, Yang L, Yang H, Xu JR, Zhang G, Kang Z. High genome heterozygosity and endemic genetic recombination in the wheat stripe rust fungus. Nat Commun. 2013;4:2673.
Zhou H, Li S, Deng Z, Wang X, Chen T, Zhang J, Chen S, Ling H, Zhang A, Wang D, Zhang X. Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in the wheat hypersensitive response to stripe rust fungus infection. Plant J. 2007;52:420–34.
Zhou L, Cheung MY, Li MW, Fu Y, Sun Z, Sun SSM, Lam HM. Rice Hypersensitive Induced Reaction Protein 1(OsHIR1) associates with plasma membrane and triggers hypersensitive cell death. BMC Plant Biol. 2010;10:290.
Zhou XL, Wang MN, Chen XM, Lu Y, Kang ZS, Jing JX. Identification of Yr59 conferring high-temperature adult-plant resistance to stripe rust in wheat germplasm PI 178759. Theor Appl Genet. 2014;127:935–45.
Zuo H, Wang J, Hao CZ, Zhang B, Ma Q. Histochemical response of nonhost resistance in pepper to the stripe rust fungus (Puccinia striiformis f. sp tritici). J Plant Pathol. 2013;95:275–83.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Kang, Z. et al. (2017). Wheat-Puccinia striiformis Interactions. In: Chen, X., Kang, Z. (eds) Stripe Rust. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-1111-9_3
Download citation
DOI: https://doi.org/10.1007/978-94-024-1111-9_3
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-024-1109-6
Online ISBN: 978-94-024-1111-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)