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Temporal Transcriptional Changes in SAR and Sugar Transport-Related Genes During Wheat and Leaf Rust Pathogen Interactions

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Abstract

Leaf rust (Puccinia triticina Erikss.) is one of the most damaging pathogens of wheat (Triticum aestivum L.). With the rapid evolution of new races, worldwide distribution, and high genetic diversity, P. triticina has the ability to cause severe epidemics in wheat growing areas. In plants, salicylic acid (SA) and sugar-mediated defense pathways are expected to provide durable and broad-spectrum resistance. To understand the role of SA and sugar-mediated resistance mechanisms in wheat during early leaf rust infection, expression profiles of the key regulators of SA (TaEDS1, TaPAD4, TaNDR1, TaRAR1, TaSGT1, TaHSP90, TaEDS5, TaPAL, and TaNPR1) and sugar (TaHTP, TaSTP13A) pathways were analyzed in time-course experiments between two wheat near-isogenic lines (NILs) differing in the leaf rust resistance gene, Lr24. The quantification of candidate gene expression using reverse transcription quantitative real-time PCR at different time points post inoculation showed stage-specific transcriptional reprogramming between compatible and incompatible interactions. Interestingly, two distinct expression patterns were observed between two types of interactions. The genes acting upstream of SA in the SA pathway (TaEDS1, TaPAD4, TaNDR1, TaRAR1, TaSGT1, TaHSP90, TaEDS5) showed strong expressions at a later stage [48 h post inoculation (hpi)] of leaf rust infection in the compatible interaction compared to unchanged or slightly changed expressions in the incompatible interaction. Further, these genes showed similar expression patterns in either of the interactions, suggesting their cooperative or coordinated functions. On the other hand, the genes involved in SA biosynthesis (TaPAL), SA downstream signaling (TaNPR1), and sugar transportation (TaHTP, TaSTP13A) showed a strong expression at mid phase of infection between 6 and 24 hpi in the incompatible interaction compared to the compatible interaction. These expression patterns suggest that TaPAL and TaNPR1 play a positive regulatory role in the SA-mediated resistance pathway whereas TaHTP (Lr67) plays an important role in the sugar-mediated resistance pathway activated by the leaf rust resistance gene, Lr24.

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References

  • Aliferis KA, Faubert D, Jabaji S (2014) A metabolic profiling strategy for the dissection of plant defense against fungal pathogens. PLoS ONE 9:e111930

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integrat Plant Biol 53:412–428

    Article  CAS  Google Scholar 

  • Andersen CL, Ledet-Jensen J, Orntoft T (2004) Normalization of real-time quantitative RT-PCR data: a model based variance estimation approach to identify genes suited for normalization-applied to bladder- and colon-cancer data-sets. Cancer Res 64:5245–5250

    Article  PubMed  CAS  Google Scholar 

  • Bancal MO, Hansart A, Sache I, Bancal P (2012) Modeling fungal sink competitiveness with grains for assimilates in wheat infected by a biotrophic pathogen. Ann Bot 110:113–123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bao F, Huang X, Zhu C, Zhang X, Li X, Yang S (2014) Arabidopsis HSP90 protein modulates RPP4-mediated temperature-dependent cell death and defense responses. New Phytol 202:1320–1334

    Article  PubMed  CAS  Google Scholar 

  • Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. J Exp Bot 58:4019–4026

    Article  PubMed  CAS  Google Scholar 

  • Bhardwaj SC, Prashar M, Kumar S, Gangwar OP, Gupta N, Prasad P, Khan H (2016) Patterns of physiologic diversity of Puccinia triticina on wheat in Indian subcontinent during 2008–2013. Indian J Agric Sci 86:55–64

    CAS  Google Scholar 

  • Birch ANE, Shep herd T, Hancock R, Goszcz K (2009) Understanding sugar sensing in induced plant defences and stress tolerance. In: Proceedings of the 25th meeting of the international society of chemical ecology, 23–27 August 2009, Neuchatel, Switzerland, p 230

  • Bolouri Moghaddam MR, Van den Ende W (2012) Sugars and plant innate immunity. J Exp Bot 63:3989–3998

    Article  PubMed  CAS  Google Scholar 

  • Bolton MD (2009) Primary metabolism and plant defense-fuel for the fire. Mol Plant Microbe Interact 22:487–497

    Article  PubMed  CAS  Google Scholar 

  • Bolton MD, Kolmer JA, Garvin DF (2008) Wheat leaf rust caused by Puccinia triticina. Mol Plant Pathol 9:563–575

    Article  PubMed  Google Scholar 

  • Cabello S, Lorenz C, Crespo S, Cabrera J, Ludwig R, Escobar C, Hofmann J (2014) Altered sucrose synthase and invertase expression affects the local and systemic sugar metabolism of nematode-infected Arabidopsis thaliana plants. J Exp Bot 65:201–212

    Article  PubMed  CAS  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63

    Article  PubMed  CAS  Google Scholar 

  • Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Clarke JD, Aarts N, Feys BJ, Dong X, Parker JE (2001) Constitutive disease resistance requires EDS1 in the Arabidopsis mutants cpr1 and cpr6 and is partially EDS1-dependent in cpr5. Plant J 26:409–420

    Article  PubMed  CAS  Google Scholar 

  • Conrath U (2006) Systemic acquired resistance. Plant Signal Behav 1(4):179–184

    Article  PubMed  PubMed Central  Google Scholar 

  • Curtis TY, Halford NG (2014) Food security: the challenge of increasing wheat yield and the importance of not compromising food safety. Ann Appl Biol 164:354–372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dempsey DMA, Vlot AC, Wildermuth MC, Klessig DF (2011) Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156

    Article  PubMed  PubMed Central  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  PubMed  CAS  Google Scholar 

  • Duan C, Yu J, Bai J, Zhu Z, Wang X (2014) Induced defense responses in rice plants against small brown plant hopper infestation. Crop J 2:55–62

    Article  Google Scholar 

  • Dubin H, Brennan JP (2009) Combating stem and leaf rust of wheat: historical perspective, impacts, and lessons learned. International Food Policy Research Institute. IFPRI Discussion Paper No. 00910. 2020 Vision Initiative. http://www.ifpri.org/millionsfed

  • Eom JS, Chen LQ, Sosso D, Julius BT, Lin IW, Qu XQ, Frommer WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opin Plant Biol 25:53–62

    Article  PubMed  CAS  Google Scholar 

  • Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863

    Article  PubMed  CAS  Google Scholar 

  • Gao QM, Zhu S, Kachroo P, Kachroo A (2015) Signal regulators of systemic acquired resistance. Front Plant Sci 6:228

    PubMed  PubMed Central  Google Scholar 

  • Gupta SK, Charpe A, Koul S, Haque QMR, Prabhu KV (2006) Development and validation of SCAR markers co-segregating with an Agropyron elongatum derived leaf rust resistance gene Lr24 in wheat. Euphytica 150:233–240

    Article  CAS  Google Scholar 

  • Herbers K, Meuwly P, Frommer WB, Metraux JP, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hofmann J, El Ashry A, Anwar S, Erban A, Kopka J, Grundler F (2010) Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant J 62:1058–1071

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, Shirasu K, Dangl JL (2003) Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 22:5679–5689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huerta-Espino J, Singh R, German S, McCallum B, Park R, Chen W, Bhardwaj S, Goyeau H (2011) Global status of wheat leaf rust caused by Puccinia triticina. Euphytica 179:143–160

    Article  Google Scholar 

  • Ishihara T, Sekine KT, Hase S, Kanayama Y, Seo S, Ohashi Y, Kusano T, Shibata D, Shah J, Takahashi H (2008) Overexpression of the Arabidopsis thaliana EDS5 gene enhances resistance to viruses. Plant Biol 10:451–461

    Article  PubMed  CAS  Google Scholar 

  • Jasinski M, Duco E, Martinoia E, Boutry M (2003) The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol 131:1169–1177

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kano A, Hosotani K, Gomi K et al (2011) D-Psicose induces upregulation of defence-related genes and resistance in rice against bacterial blight. J Plant Physiol 168:1852–1857

    Article  PubMed  CAS  Google Scholar 

  • Kawamura Y, Takenaka S, Hase S, Kubota M, Ichinose Y, Kanayama Y et al (2009) Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1. Plant Cell Physiol 50:924–934

    Article  PubMed  CAS  Google Scholar 

  • Khan M, Bukhari A, Dar Z, Rizvi S (2013) Status and strategies in breeding for rust resistance in wheat. Agric Sci 4:292–301

    Google Scholar 

  • Koch JR, Creelman RA, Eshita SM, Seskar M, Mullet JE, Davis KR (2000) Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid. The role of programmed cell death in lesion formation. Plant Physiol 123:487–496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kogel KH, Langen G (2005) Induced disease resistance and gene expression in cereals. Cell Microbiol 7:1555–1564

    Article  PubMed  CAS  Google Scholar 

  • Kolmer JA (2005) Tracking wheat rust on a continental scale. Curr Opin Plant Biol 8:441–449

    Article  PubMed  Google Scholar 

  • Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H et al (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323:1360–1363

    Article  PubMed  CAS  Google Scholar 

  • Kumari C, Dutta TK, Banakar P, Rao U (2016) Comparing the defence-related gene expression changes upon root-knot nematode attack in susceptible versus resistant cultivars of rice. Sci Rep 6:22846

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    Article  PubMed  CAS  Google Scholar 

  • Lemonnier P, Gaillard C, Veillet F, Verbeke J, Lemoine R, Coutos-Thévenot P et al (2014) Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant Mol Biol 85:473–484

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Wang Y, Zhang H, Zhang Q, Zhai H, Liu Q, He S (2017) The plasma membrane-localized sucrose transporter IbSWEET10 contributes to the resistance of sweet potato to Fusarium oxysporum. Front Plant Sci 8:197

    PubMed  PubMed Central  Google Scholar 

  • Lin WC, Lu CF, Wu JW, Cheng ML, Lin YM, Yang NS, Black L, Green SK, Wang JF, Cheng CP (2004) Transgenic tomato plants expressing the Arabidopsis NPR1gene display enhanced resistance to a spectrum of fungal and bacterial diseases. Transgenic Res 13:567–581

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) Molecular chaperone hsp90 associates with resistance protein n and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 279:2101–2108

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Yuan M, Zhou Y, Li X, Xiao J, Wang S (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ. https://doi.org/10.1111/j.1365-3040.2011.02391.x

    Article  PubMed  Google Scholar 

  • Long DL, Roelfs AP, Leonard KJ (1994) Virulence and diversity of Puccinia recondite f. sp. tritici in United States in 1992. Plant Dis 78:901–906

    Article  Google Scholar 

  • Lu H, Greenberg JT, Holuigue L (2016) Editorial: salicylic acid signaling networks. Front Plant Sci 7:238

    PubMed  PubMed Central  Google Scholar 

  • Makandar R, Nalam VJ, Chowdhury Z, Sarowar S, Klossner G, Lee H, Burdan D, Trick HN, Gobbato E, Parker JE et al (2015) The combined action of ENHANCED DISEASE SUSCEPTIBILITY1, PHYTOALEXIN DEFICIENT4, and SENESCENCE-ASSOCIATED101 promotes salicylic acid-mediated defenses to limit Fusarium graminearum infection in Arabidopsis thaliana. Mol Plant Microbe Interact 28:943–953

    Article  PubMed  CAS  Google Scholar 

  • McCallum BD, Hiebert CW, Cloutier S, Bakkeren G, Rosa SB, Humphreys DG, Saville BJ (2016) A review of wheat leaf rust research and the development of resistant cultivars in Canada. Can J Plant Pathol 38:1–18

    Article  CAS  Google Scholar 

  • Mishra AN, Prakasha TL, Kaushal K, Dubey VG (2014) Validation of Lr24 in some released bread wheat varieties and its implications in leaf rust resistance breeding and deployment in central India. Indian Phytopathol 67:102–103

    Google Scholar 

  • Moore JW, Herrera-Foessel S, Lan C, Schnippenkoetter W, Ayliffe M, Huerta-Espino J, Kong X (2015) A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat. Nat Genet 47:1494–1498

    Article  PubMed  CAS  Google Scholar 

  • Morkunas I, Kozłowska M, Ratajczak L, Marczak M (2007) Role of sucrose in the development of Fusarium wilt in lupine embryo axes. Physiol Mol Plant Pathol 70:25–37

    Article  CAS  Google Scholar 

  • National Center for Biotechnology Information (NCBI) (2017) [Internet] Bethesda (MD): National Library of Medicine (US) National Center for Biotechnology Information, 1988. https://www.ncbi.nlm.nih.gov/. Accessed 04 Oct 2017

  • Nawrath C, Heck S, Parinthawong N, Métraux J (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26:509–515

    Article  PubMed  CAS  Google Scholar 

  • Pieterse CMJ, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

    Article  PubMed  CAS  Google Scholar 

  • Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20:492–499

    Article  PubMed  CAS  Google Scholar 

  • Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    Article  PubMed  CAS  Google Scholar 

  • Rio DC (2015) Denaturation and electrophoresis of RNA with formaldehyde. Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.prot080994

    Article  PubMed  Google Scholar 

  • Roelfs AP (1984) Race specificity and methods of study. In: Bushnell WR, Roelfs AP (eds) The cereal rusts vol. I. Origins, specificity, structure, and physiology. Acadamic Press, Orlando, pp 132–164

    Google Scholar 

  • Rojas CM, Senthil-Kumar M, Tzin V, Mysore K (2014) Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front Plant Sci 5:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruuhola T, Julkunen-Tiitto R (2003) Trade-off between synthesis of salicylates and growth of micropropagated Salix pentandra. J Chem Ecol 29:1565–1588

    Article  PubMed  CAS  Google Scholar 

  • Sade D, Brotman Y, Eybishtz A, Cuadros-Inostroza A, Fernie AR, Willmitzer L, Czosnek H (2013) Involvement of the hexose transporter gene LeHT1 and of sugars in resistance of tomato to Tomato yellow leaf curl virus. Mol Plant 6:1707–1710

    Article  PubMed  CAS  Google Scholar 

  • Schellenberg B, Ramel C, Dudler R (2010) Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Mol Plant Microbe Interact 23:1287–1293

    Article  PubMed  CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative Ct method. Nat Protoc 3:1101–1108

    Article  PubMed  CAS  Google Scholar 

  • Schnippenkoetter W, Lo C, Liu G, Dibley K, Chan WL, White J, Godwin I (2017) The wheat Lr34 multipathogen resistance gene confers resistance to anthracnose and rust in sorghum. Plant Biotechnol J. https://doi.org/10.1111/pbi.12723

    Article  PubMed  PubMed Central  Google Scholar 

  • Schornack S, Ballvora A, Gurlebeck D, Peart J, Baulcombe D, Ganal M, Baker B, Bonas U, Lahaye T (2004) The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 37:46–60

    Article  PubMed  CAS  Google Scholar 

  • Serfling A, Templer SE, Winter P, Ordon F (2016) Microscopic and molecular characterization of the prehaustorial resistance against wheat leaf rust (Puccinia triticina) in Einkorn (Triticum monococcum). Front Plant Sci 7:1668

    Article  PubMed  PubMed Central  Google Scholar 

  • Shah J (2003) The salicylic acid loop in plant defence. Curr Opin Plant Biol 6:365–371

    Article  PubMed  CAS  Google Scholar 

  • Sharma AK, Singh DP, Singh AK, Saharan MS, Jat MC, Babu KS, Singh SS (2010) Progress report of all India coordinated wheat and barley improvement project 2009–10, vol. III, crop protection. Directorate of Wheat Research, Karnal, p 247

    Google Scholar 

  • Silverman P, Seskar M, Kanter D, Schweizer P, Métraux JP, Raskin I (1995) Salicylic acid in rice: biosynthesis, conjugation and possible role. Plant Physiol 108:633–639

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singh RP, Singh PK, Rutkoski J, Hodson DP, He X, Jørgensen LN, Huerta-Espino J (2016) Disease impact on wheat yield potential and prospects of genetic control. Annu Rev Phytopathol 54:303–322

    Article  PubMed  CAS  Google Scholar 

  • Sorahinobar M, Niknam V, Ebrahimzadeh H et al (2016) Central role of salicylic acid in resistance of wheat against Fusarium graminearum. J Plant Growth Regul 35:477

    Article  CAS  Google Scholar 

  • Stalman M, Koskamp AM, Luderer R, Vernooy JHJ, Wind JC, Wullems GJ, Croes AF (2003) Regulation of anthraquinone biosynthesis in cell cultures of Morinda citrifolia. J Plant Physiol 160:607–614

    Article  PubMed  CAS  Google Scholar 

  • Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819

    Article  PubMed  CAS  Google Scholar 

  • Sucher J, Boni R, Yang P, Rogowsky P, Buchner H, Kastner C, Kumlenh J, Krattinger SG, Keller B (2016) The durable wheat disease resistance gene Lr34 confers common rust and northern corn leaf blight resistance in maize. Plant Biotechnol J. https://doi.org/10.1111/pbi.12647

    Article  PubMed Central  PubMed  Google Scholar 

  • Sun L, Yang DL, Kong Y, Chen Y, Li XZ, Zeng LJ, He ZH (2014) Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice. Mol Plant Pathol 15:161–173

    Article  PubMed  CAS  Google Scholar 

  • Sutton PN, Gilbert MJ, Williams LE, Hall JL (2007) Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol Plant 129:787–795

    Article  CAS  Google Scholar 

  • Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29:1061–1076

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Han X, Kahmann R (2015) Microbial effectors target multiple steps in the salicylic acid production and signaling pathway. Front Plant Sci 6:349

    Article  PubMed  PubMed Central  Google Scholar 

  • Tauzin AS, Giardina T (2014) Sucrose and invertases: a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor S, Wakem M, Dijkman G, Alsarraj M, Nguyen M (2010) A practical approach to RT-qPCR—publishing data that conform to the MIQE guidelines. Methods 50:S1–S5

    Article  PubMed  CAS  Google Scholar 

  • Thao NP, Chen L, Nakashima A, Hara S, Umemura K, Takahashi A, Shirasu K, Kawasaki T, Shimamo K (2007) RAR1 and HSP90 form a complex with Rac/RopGTPase and function in innate-immune responses in rice. Plant Cell 19:4035–4045

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • The Arabidopsis Information Resource (TAIR) (2017) http://www.Arabidopsis.org/about Arabidopsis.html on http://www.Arabidopsis.org Oct 04

  • Tomar SMS, Menon MK (1998) Introgression of alien genes for leaf rust (Puccinia recondita) resistance in to bread wheat (Triticum aestivum L.) cultivars. Indian J Agric Sci 68:675–681

    Google Scholar 

  • Tsuda K, Glazebrook J, Katagiri F (2008) The interplay between MAMP and SA signaling. Plant Signal Behav 3:359–361

    Article  PubMed  PubMed Central  Google Scholar 

  • Udvardi MK, Czechowski T, Scheible WR (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20:1736–1737

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ustun S, Bartetzko V, Bornke F (2013) The Xanthomonas campestris type III effector XopJ targets the host cell proteasome to suppress salicylic-acid mediated plant defence. PLoS Pathog 9:e1003427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vargas WA, Martin JM, Rech GE, Rivera LP, Benito EP, Diaz-Minguez JM et al (2012) Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol 158:1342–1358

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang X, McCallum BD, Fetch T, Bakkeren G, Marais GF, Saville BJ (2013) Comparative microscopic and molecular analysis of Thatcher near-isogenic lines with wheat leaf rust resistance genes Lr2a, Lr3, LrB, or Lr9 upon challenge with different Puccinia triticina races. Plant Pathol 62:698–707

    Article  CAS  Google Scholar 

  • Wang J, Shine MB, Gao QM, Navarre D, Jiang W, Liu C et al (2014) Enhanced disease susceptibility1 mediates pathogen resistance and virulence function of a bacterial effector in soybean. Plant Physiol 165:1269–1284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • XLSTAT (2017) A user-friendly statistical software for Microsoft Excel. http://www.xlstat.com

  • Yang B, Sugio A, White FF (2006) Os8N3 is a host disease susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci USA 103:10503–10508

    Article  PubMed  CAS  Google Scholar 

  • Youssef RM, Kim KH, Haroon SA, Matthews BF (2013) Post-transcriptional gene silencing of the gene encoding aldolase from soybean cyst nematode by transformed soybean roots. Exp Parasitol 134:266–274

    Article  PubMed  CAS  Google Scholar 

  • Yuan JH, Liu TG, Chen WQ (2007a) Postulation of leaf rust resistance genes in 47 new wheat cultivars at seedling stage. Sci Agric Sin 40:1925–1935

    CAS  Google Scholar 

  • Yuan Y, Zhong S, Li Q, Zhu Z, Lou Y, Wang L, Wang J, Wang M, Yang D, He Z (2007b) Functional analysis of rice NPR1-like genes reveals that OsNPR1/NH1 is the rice orthologue conferring disease resistance with enhanced herbivore susceptibility. Plant Biotechnol J 5:313–324

    Article  PubMed  CAS  Google Scholar 

  • Zhao HB, Xu LF, Su T, Jiang Y, Hu LY, Ma FW (2015) Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis thaliana. J Pin Res 59:109–119

    Article  CAS  Google Scholar 

  • Zhu B, Chen TH, Li PH (1996) Analysis of late blight resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for osmotin-like protein. Planta 198:70–77

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are thankful to Dr. G.P. Singh, Director, ICAR-IIWBR, Karnal, India for liberal funding of research; to Dr. S.K. Chakrabarty, Director, ICAR-CPRI, Shimla, India for providing lab facilities; and to Dr. M. Sivasamy, Head, ICAR-IARI, Wellington, India, for providing the seed of Lr24 NIL.

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  1. ICAR-Indian Institute of Wheat and Barley Research, Regional station, Shimla, Himachal Pradesh, 171002, India

    Siddanna Savadi, Pramod Prasad, S. C. Bhardwaj, O. P. Gangwar, Hanif Khan & Subodh Kumar

  2. ICAR-Indian Institute of Wheat and Barley Research, Karnal, Haryana, 132001, India

    Prem Lal Kashyap

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  1. Siddanna Savadi
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Correspondence to S. C. Bhardwaj.

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344_2017_9777_MOESM1_ESM.jpg

Fig. S1 Leaf rust (P. triticina) infection types on the susceptible and the resistant wheat NILs. Supplementary material 1 (JPG 412 KB)

344_2017_9777_MOESM2_ESM.jpg

Fig. S2 Melt curve analysis of TaEDS1, TaPAD4, TaNDR1, TaSGT1, TaRAR1, TaHSP90, TaEDS5, TaHTP and TaSTP13A genes and reference gene (UBI) during the RT-qPCR produced single sharp peak. Supplementary material 2 (JPG 490 KB)

344_2017_9777_MOESM3_ESM.jpg

Fig. S3 Comparison of relative expression levels (A) among the SA pathway related genes (TaEDS1, TaPAD4, TaNDR1, TaSGT1, TaRAR1, TaHSP90 and TaEDS5) and (B) between the two sugar transporter genes (TaHTP and TaSTP13A) at each time point after inoculation during compatible and incompatible interactions of wheat and leaf rust pathogen. Expression values are log2 transformed and mean log2 values are represented as the stacked bar. R and S in brackets stand for resistant and susceptible NILs respectively. Supplementary material 3 (JPG 1447 KB)

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Savadi, S., Prasad, P., Bhardwaj, S.C. et al. Temporal Transcriptional Changes in SAR and Sugar Transport-Related Genes During Wheat and Leaf Rust Pathogen Interactions. J Plant Growth Regul 37, 826–839 (2018). https://doi.org/10.1007/s00344-017-9777-4

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  • DOI: https://doi.org/10.1007/s00344-017-9777-4

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