Skip to main content
SpringerLink
Log in

Molecular Mechanisms for Resistance to Biotic Stresses

  • Chapter
  • First Online:
The Citrus Genome

Part of the book series: Compendium of Plant Genomes ((CPG))

Abstract

Diverse pathogens including viruses, viroids, fungi, and bacteria are responsible of diseases on Citrus. Some of them in addition represent a treath to Citrus industry in some specific areas, others are either worldwide spread or have a restricted distribution. Breeding program searching for resistance to a given pathogen must take into consideration the nature of the interaction being studied. In addition a large number of data generated by sequencing projects will contribute to the identification of individual genes or groups of genes potentially associated with resistance to biotic and abiotic factors. This chapter introduce the molecular basis of plant resistance to innate immune response elicited by non-specific elicitors and how successful pathogens have evolved to evade them or trigger them later in the infection so that they become infective. The other paragraphs are dedicated to illustrating three important disease model studies caused by a fungus (Alternaria brown rot), an oomycete (Phythophthora root rot) and a virus (Citrus Tristeza).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Andolfo G, Jupe F, Witek K, Etherington GJ, Ercolano MR, Jones JDG (2014) Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biol 14:1–12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barrett HC, Rhodes AM (1976) A numerical taxonomic study of affinity relationships in cultivated citrus and its close relatives. Syst Bot 1:105–136

    Article  Google Scholar 

  • Bernet GP, Breto MP, Asins MJ (2004) Expressed sequence enrichment for candidate gene analysis of Citrus Tristeza Virus resistance. Theor Appl Genet 108:592–602

    Article  CAS  PubMed  Google Scholar 

  • Bernet GP, Gorris MT, Carbonell EA, Cambra M, Asins MJ (2008) Citrus tristeza virus resistance in a core collection of sour orange based on a diversity study of three germplasm collections using QTL-linked markers. Plant Breed 127:398–406

    Article  Google Scholar 

  • Birker DHK, Takahara H, Narusaka M, Deslandes L, Narusaka Y, Reymond M, Parker JE, O’Connell R (2009, Nov) A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J 60(4):602–613

    Google Scholar 

  • Boava LP, Cristofani-Yaly M, Mafra VS et al (2011a) Global gene expression of Poncirus trifoliata, Citrus sunki and their hybrids under infection of Phytophthora parasitica. BMC Genom 12:39

    Article  CAS  Google Scholar 

  • Boava LP, Cristofani-Yaly M, Stuart RM, Machado MA (2011b) Expression of defense-related genes in response to mechanical wounding and Phytophthora parasitica infection in Poncirus trifoliata and Citrus sunki. Physiol Mol Plant Pathol 76:119–125

    Article  CAS  Google Scholar 

  • Bowman KD, Rouse RE (2006) US-812 citrus rootstock. HortScience 41:832–836

    Article  Google Scholar 

  • Broadbent, P, Bevington, KB, Coote BG (1991) Control of stem pitting of grapefruit in Australia by mild strain protection. In: Proceedings of the 11th conference of the international organization of citrus virologists, pp 64–70

    Google Scholar 

  • Castle WS, Tucker DPA (1998) Florida citrus rootstocks selection guide. In University of Florida Corporation Extension. University of Florida, Gainesville, FL

    Google Scholar 

  • Castle WS, Tucker DPH, Krezdorn AH, Youtsey CO (1993) Rootstocks for Florida citrus. University of Florida, IFAS, Gainesville, FL

    Google Scholar 

  • Catanzariti AM, Dodds PN, Ve T, Kobe B, Ellis JG, Staskawicz BJ (2010) The AvrM effector from flax rust has a structured C-terminal domain and interacts directly with the M resistance protein. Mol Plant Microbe Interact 23:49–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y et al (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–1481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi HW, Klessig DF (2016) DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biol 16:232

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Costa AS, Muller GW (1980) Tristeza control by cross protection. Plant Dis 64:538–541

    Article  Google Scholar 

  • Cuenca J, Aleza P, Vicent A, Brunel D, Ollitrault P, and Navarro L (2013) Genetically based location from triploid populations and gene ontology of a 3.3-Mb genome region linked to Alternaria brown spot resistance in citrus reveal clusters of resistance genes. PLoS ONE 8:e76755. https://doi.org/10.1371/journal.pone.0076755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cuenca J, Aleza P, Garcia-Lor A, Ollitrault P, Navarro L (2016) Fine mapping for identification of citrus alternaria brown spot candidate resistance genes and development of new SNP markers for marker-assisted selection. Front Plant Sci 7:1948. https://doi.org/10.3389/fpls.2016.01948

    Article  PubMed  PubMed Central  Google Scholar 

  • Dalio RJD, Magalhães DM, Rodrigues CM, Arena GD, Oliveira TS, Souza-Neto RR et al (2017) PAMPs, PRRs, effectors and R-genes associated with citrus–pathogen interactions. Ann Bot 119:749–774. PMID: 28065920

    Google Scholar 

  • Dalio RJD, Máximo HJ, Oliveira TS, Azevedo TM, Felizatti HL, Campos MA, Machado MA (2018) Molecular basis of Citrus sunki susceptibility and Poncirus trifoliata resistance upon Phytophthora parasitica attack. Mol Plant Microbe Interact 31:386–398

    Article  CAS  PubMed  Google Scholar 

  • Dawson TE, Mooney PA (2000) Evidence for trifoliate resistance breaking isolates of citrus tristeza virus in New Zealand. In: Fourteenth IOCV conference, pp 69–76

    Google Scholar 

  • Dawson WO, Garnsey SM, Tatineni S, Folimonova SY, Harper SJ, Gowda S (2013, May 14) Citrus tristeza virus-host interactions. Front Microbiol. 4:88. https://doi.org/10.3389/fmicb.2013.00088. PMID: 23717303; PMCID: PMC3653117

  • de Ronde D, Butterbach P, Kormelink R (2014) Dominant resistance against plant viruses. Front Plant Sci 5:30. https://doi.org/10.3389/fpls.2014.00307

    Article  Google Scholar 

  • Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C et al (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci USA 100:8024–8029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dinesh-Kumar SP, Whitham S, Choi D, Hehl R, Corr C, Baker B (1995) Transposon tagging of tobacco mosaic virus resistance gene N: its possible role in the TMV-N-mediated signal transduction pathway. Proc Natl Acad Sci USA 92(10):4175–4180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang C-I, Ayliffe MA et al (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103:8888–8893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dominguez A, Hermoso de Mendoza A, Guerri J, Cambra M, Navarro L, Moreno P, Pena L (2002) Pathogen derived resistance to citrus tristeza virus (CTV) in transgenic Mexican lime (Citrus aurantifolia (Christ. Swing.) plants expressing its p25 coat protein gene. Mol Breeding 10:1–10

    Article  CAS  Google Scholar 

  • Duxbury Z, Ma Y, Furzer OJ, Huh SU, Cevik V, Jones JD, Sarris PF (2016) Pathogen perception by NLRs in plants and animals: parallel worlds. BioEssays 38(8):769–781

    Article  PubMed  Google Scholar 

  • EFSA PLH (EFSA Panel on Plant Health), Jeger M, Bragard C, Caffier D, Dehnen-Schmutz K, Gilioli G, Gregoire J-C, Ja ques Miret JA, MacLeod A, Navajas Navarro M, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Chatzivassiliou E, Winter S, Catara A, Duran-Vila N, Hollo G, Candresse T (2017) Scientific opinion on the pest categorisation of Citrus tristeza virus (non-European isolates). EFSA J 15(10):5031, 29. https://doi.org/10.2903/j.efsa.2017.5031

  • Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13(4):472–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10(4):366–371

    Article  CAS  PubMed  Google Scholar 

  • Fagoaga C, Lopez C, de Mendoza AH, Moreno P, Navarro L, Flores R, Pena L (2006) Post-transcriptional gene silencing of the p23 silencing suppressor of Citrus tristeza virus confers resistance to the virus in transgenic Mexican lime. Plant Mol Biol 60:153–165

    Article  CAS  PubMed  Google Scholar 

  • Fagoaga C, Pensabene-Bellavia G, Moreno P, Navarro L, Flores R, and Peña L (2011) Ectopic expression of the p23 protein of Citrus tristeza virus differentially modifies viral accumulation and tropism in two transgenic woody hosts. Mol Plant Pathol 12:898–910

    Google Scholar 

  • Folimonova SY (2013) Developing an understanding of cross-protection by Citrus tristeza virus. Front Microbiol. https://doi.org/10.3389/fmicb.2013.00076

  • Folimonova SY, Folomonov AS, Satyanarayana T, Dawson T (2008) Citrus tristeza virus: survival at the edge of the movement continuum. J Virol 82:6546–6556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang DQ, Federici CT, Roose ML (1998) A high-resolution linkage map of the citrus tristeza virus resistance gene region in Poncirus trifoliata (L.) Raf. Genetics 150:883–890

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garnsey SM, Barrett HC, Hutchison DJ (1987) Identification of citrus tristeza virus resistance in citrus relatives and potential applications. Phytophylactica 19:187–191

    Google Scholar 

  • Garnsey SM, Su H, Tsai M (1997) Differential susceptibility of pummelo and Swingle citrumelo to isolates of citrus tristeza virus. In: Da Graca J, Moreno P, Yokomi R (eds) Proceedings of the 3rd conference of the international organization of citrus virologists (IOCV), Riverside, CA, pp 38–146

    Google Scholar 

  • Ghosh A, Das A, Meena R, Baranwal VK (2014) Evidence for resistance to Citrus tristeza virus in pomelo (Citrus maxima Merr.) grown in Darjeeling and Sikkim hillsof India. Phytoparasitica 42:503–508

    Article  Google Scholar 

  • Gmitter FG Jr, Chen C, Machado MA, Alves de Souza A, Ollitrault P, Froehlicher Y, Shimizu T (2012) Citrus genomics. Tree Genet Genomes 8:611–626

    Article  Google Scholar 

  • Gmitter FG, Xiao SY, Huang S, Hu XL, Garnsey SM, Deng Z (1996) A localized linkage map of the citrus tristeza virus resistance gene region. Theor Appl Genet 92:688–695

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Munoz N, Velazquez K, Vives MC, Guerri J (2017) The resistance of sour orange to Citrus tristeza virus is mediated by both the salycilic acid and the RNA silencing defense pathways. Mol Plant Pathol 18:1253–1266

    Article  CAS  PubMed  Google Scholar 

  • Graham JH, Menge JA (2000) Phytophthora-induced diseases. In: Compendium of Citrus diseases, (eds. Timmer, L.W., Garnsey, S.M. and Graham, J.H.) American Phytopathlogical Society, St. Paul, MN, pp 12–15

    Google Scholar 

  • Guidetti-Gonzalez S, Carrer H (2007) Putative resistance genes in the CITEST database. Genet Mol Biol 30:931–942

    Article  CAS  Google Scholar 

  • Harper SJ (2013, April 23) Citrus tristeza virus: evolution of complex and varied genotypic groups. Front Microbiol 4:93. https://doi.org/10.3389/fmicb.2013.00093

  • Heidrich K, Tsuda K, Blanvillain-Baufume S, Wirthmueller L, Bautor J, Parker JE (2013) Arabidopsis TNL-WRKY domain receptor RRS1 contributes to temperature-conditioned RPS4 auto-immunity. Front Plant Sci 4:403

    Article  PubMed  PubMed Central  Google Scholar 

  • Hogenhout SA, Van der Hoorn RL, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Mol Plant Microbe Interact 22:115–122

    Article  CAS  PubMed  Google Scholar 

  • Isshiki A, Akimitsu K, Yamamoto M, Yamamoto H (2001) Endopolygalacturonase is essential for citrus black rot caused by Alternaria citri but not brown spot caused by Alternaria alternata. Mol Plant Microbe Interact 14:749–757

    Article  CAS  PubMed  Google Scholar 

  • Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Front Immunol 4:297

    Google Scholar 

  • Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Vance RE, Dangl JL (2016) Intracellular innate immune surveillance devices in plants and animals. Science 354(6316)

    Article  PubMed  CAS  Google Scholar 

  • Kohmoto K, Itoh Y, Shimomura N, Kondoh Y, Otani H, Kodama M, Nishimura S, Nakatsuka S (1993) Isolation and biological activities of two host-specific toxins from the tangerine pathotype of Alternaria alternata. Phytopathology 83:495–502

    Article  CAS  Google Scholar 

  • Kamoun S (2009) The secretome of plant-associated fungi and oomycetes. In: Deising HB (ed) The Mycota. Springer, Berlin, pp 173–180

    Chapter  Google Scholar 

  • Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463

    Article  CAS  PubMed  Google Scholar 

  • Krasileva KV, Dahlbeck D, Staskawicz BJ (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:2444–2458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D, Kraut A et al (2015) A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell 161(5):1074–1088

    Article  PubMed  CAS  Google Scholar 

  • Leipe DD, Koonin EV, Aravind L (2004) STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J Mol Biol 343(1):1–28

    Article  CAS  PubMed  Google Scholar 

  • Lopez C, Cervera M, Fagoaga C, Moreno P, Navarro L, Flores R, Pena L (2010) Accumulation of transgene-derived siRNAs is not sufficient for RNAi-mediated protection against Citrus tristeza virus in transgenic Mexican lime. Mol Plant Pathol 11:33–41

    Article  CAS  PubMed  Google Scholar 

  • Lu R, Folimonov A, Shintaku M, Li WX, Falk BW, Dawson WO et al (2004) Three distinct suppressors of RNA silencing encoded by a 20-kb viral RNA genome. Proc Natl Acad Sci USA 101:15742–15747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Machado MA, Cristofani-Yaly M, Bastianel M (2011) Breeding, genetic and genomic of citrus for disease resistance. Revista Brasileira de Fruticultura 33(spe1):158–172

    Article  Google Scholar 

  • Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54(2):263–272

    Article  CAS  PubMed  Google Scholar 

  • Maekawa T, Kracher B, Vernaldi S, Loren Ver, van Themaat E, Schulze-Lefert P (2012) Conservation of NLR-triggered immunity across plant lineages. Proc Natl Acad Sci USA 109(49):20119–20123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore R (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7:212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mermigka G, Sarris PF (2019) The rise of plant resistosomes. Trends Immunol 40(8):670–673

    Article  CAS  PubMed  Google Scholar 

  • Mermigka G, Amprazi M, Mentzelopoulou A, Amartolou A, Sarris PF (2020) Plant and animal innate immunity complexes: fighting different enemies with similar weapons. Trends Plant Sci 25(1):80–91

    Article  CAS  PubMed  Google Scholar 

  • Mestre PF, Asins MJ, Pina JA, Navarro L (1997) Efficient search for new resistant genotypes to the citrus tristeza closterovirus in the orange subfamily Aurantioideae. Theor Appl Genet 95:1282–1288

    Article  Google Scholar 

  • Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15(4):809–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyamoto Y, Masunaka A, Tsuge T, Yamamoto M, Ohtani K, Fukumoto T et al (2010) ACTTS3 encoding a polyketide synthase is essential for the biosynthesis of act-toxin and pathogenicity in the tangerine pathotype of Alternaria alternata. Mol Plant Microbe Interact 23:406–414. https://doi.org/10.1094/MPMI-23-4-0406

    Article  CAS  PubMed  Google Scholar 

  • Moreno P, Ambrós S, Albiach-Martí MR, Guerri J, Peña L (2008) Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Mol Plant Pathol 9:251–268

    Article  CAS  PubMed  Google Scholar 

  • Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M et al (2009) RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 60:218–226

    Article  CAS  PubMed  Google Scholar 

  • Nishimura MT, Dangl JL (2014) Paired plant immune receptors. Science 344:267–268

    Article  CAS  PubMed  Google Scholar 

  • Ntoukakis V, Saur IM, Conlan B, Rathjen JP (2014) The changing of the guard: the Pto/Prf receptor complex of tomato and pathogen recognition. Curr Opin Plant Biol 20:69–74

    Article  CAS  PubMed  Google Scholar 

  • Oßwald W, Fleischmann F, Rigling D, Coelho AC, Cravador A, Diez R, Dalio RJ, Horta Jung M, Pfanz H, Robin C, Sipos G, Solla A, Cech T, Chambery A, Diamandis S, Hansen E, Jung T, Orlikowski LB, Parke J, Prospero S, Werres S (2014) Strategies of attack and defence in woody plant-Phytophthora interactions. Forest Pathol 44:169–190

    Article  Google Scholar 

  • Panabières F, Amselem J, Galiana E, Le Berre J-Y (2005) Gene identification in the oomycete pathogen Phytophthora parasitica during in vitro vegetative growth through expressed sequence tags. Fungal Genet Biol 42:611–623

    Article  PubMed  CAS  Google Scholar 

  • Panabieres F, Ali GS, Allagui MB et al (2016) Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathologia Mediterranea 55:20–40

    CAS  Google Scholar 

  • Powell CA, Pelosi RR, Cohen M (1992) Superinfection of orange trees containing mild isolates of citrus tristeza virus and severe Florida isolates of citrus tristeza virus. Plant Dis 76:141–144

    Article  Google Scholar 

  • Rai M (2006) Refinement of the Citrus tristeza virus resistance gene (Ctv) positional map in Poncirus trifoliata and generation of transgenic grapefruit (Citrus paradisi) plant lines with candidate resistance genes in this region. Plant Mol Biol 61:399–414

    Article  CAS  PubMed  Google Scholar 

  • Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall PH et al (2012) Intramolecular interaction influences binding of the flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathog 8:e1003004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosa DD, Campos MA, Targon MLPN, Souza AA (2007) Phytophthora parasitica transcriptome, a new concept in the understanding of the citrus gummosis. Genetics Mol Biol 30:997–1008

    Article  CAS  Google Scholar 

  • Ruiz-Ruiz S, Navarro B, Gisel A, Peña L, Navarro L, Moreno P, et al. (2011) Citrus tristeza virus infection induces the accumulation of viral small RNAs (21- 24-nt) mapping preferentially at the 3’-terminal region of the genomic RNA and affects the host small RNA profile. Plant Mol Biol 75:607–619

    Article  CAS  PubMed  Google Scholar 

  • Sahin-Cevik M, Cevik B, Karaca G (2014) Expression analysis of WRKY genes from Poncirus trifoliata in response to pathogen infection. J Plant Interact 9:182–193

    Article  CAS  Google Scholar 

  • Sarris PF, Cevik V, Dagdas G, Jones JD, Krasileva KV (2016) Comparative analysis of plant immune receptor architectures uncovers host proteins likely targeted by pathogens. BMC Biol 14:8

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J, Derbyshire P, Cevik V, Rallapalli G, Saucet SB et al (2015) A plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell 161:1089–1100

    Article  CAS  PubMed  Google Scholar 

  • Saucet SB, Ma Y, Sarris PF, Furzer OJ, Sohn KH, Jones JD (2015) Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4. Nat Commun 6:6338

    Article  CAS  PubMed  Google Scholar 

  • Scora RW (1975) On the history and origin of Citrus. Bull Torrey Bot Club 102(6):369–375

    Article  Google Scholar 

  • Scott KA, Hlela Q, Zablocki O, Read D, van Vuuren S, Pietersen G (2013) Genotype composition of populations of grapefruit cross protecting Citrus tristeza virus strain GFMS12 in different host plants and aphid-transmitted sub-isolates. Adv Virol 158:27–37

    CAS  Google Scholar 

  • Soler N, Plomer M, Fagoaga C, Moreno P, Navarro L, Flores R, Pena L (2012) Transformation of Mexican lime with an intron-hairpin construct expressing untranslatable versions of the genes coding for the three silencing suppressors of Citrus tristeza virus confers complete resistance to the virus. Plant Biotechnol J 10:597–608

    Article  CAS  PubMed  Google Scholar 

  • Tatineni S, Dawson WO (2012) Enhancement or attenuation of disease by deletion of genes from Citrus tristeza virus. J Virol 86:7850–7857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timmer LW, Solel Z, Orozco-Santos M (2000) Alternaria brown spot of mandarins. In Timmer LW, Garnsey SM, Graham JH (eds) Compendium of citrus diseases. The American Phytopathological Society Press, St. Paul, MN, pp 19–21

    Google Scholar 

  • Timmer LW, Peever TL, Solel Z, Akimitsu K (2003) Alternaria diseases of citrus-novel Pathosystems. Phytopathol Mediterr 42:99–112

    Google Scholar 

  • Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y et al (2013) Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–66. https://doi.org/10.1111/j.1574-6976.2012.00350.x

    Article  CAS  PubMed  Google Scholar 

  • Van Vuuren SP, Collins RP, da Graca JV (1993) Growth and production of lime trees pre-immunized with mild Citrus tristeza virus isolates. Phytophylactica 25:39–42

    Google Scholar 

  • Wang Y, Zhou L, Li D, Dai L, Lawton-Rauh A, Srimani PK, Duan Y, Luo F (2015) Genome-wide comparative analysis reveals similar types of NBS genes in hybrid Citrus sinensis genome and original Citrus clementine genome and provides new insights into non-TIR NBS genes. PLoS ONE 10(3):e0121893

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF et al (2014) Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344(6181):299–303

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Schichijo T, Ueno I, Kihara T, Yamada T, Hirai M, Yamada S, Ieki H, Kuramoto T (1983) Survey for resistance of citrus cultivars and hybrid seedlings to Citrus tristeza virus (CTV). Bull Fruit Trees Res Stn Ser 10:51–68

    Google Scholar 

  • Zanutto CA, Corazza MJ, Carvalho Nunes WM (2013) Evaluation of the protective capacity of new mild Citrus tristeza virus (CTV) isolates selected for a preimmunization program. Scientia Agricola 70:116–124

    Article  CAS  Google Scholar 

  • Zhou CY, Hailstones D, Broadbent P, Connor R, Bowyer J (2002) Studies on mild strain cross protection against stem-pitting Citrus tristeza virus. In: Proceedings of the 15th conference of the international organization of citrus virologists, pp 125–157

    Google Scholar 

  • Zhou Y, Zhou CY, Li ZA, Wang XF, Liu KH (2008) Mild strains cross protection against stem-pitting tristeza of sweet orange. Scientia Agricultura Sinica 41:4085–4091

    CAS  Google Scholar 

  • Zhu Y, Qian W, Hua J (2010) Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog 6:e1000844

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Catania, Catania, Italy

    Vittoria Catara

  2. Hunan Agricultural University, Changsha, China

    Dai Suming

  3. Institute of Molecular Biology and Biotechnology, FORTH, Heraklion, Greece

    Panagiotis F. Sarris

  4. School of Biosciences, University of Exeter, Exeter, UK

    Panagiotis F. Sarris

  5. Department of Biology, University of Crete, 714 09, Crete, Greece

    Panagiotis F. Sarris

Authors
  1. Vittoria Catara
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dai Suming
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Panagiotis F. Sarris
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vittoria Catara .

Editor information

Editors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Catania, Catania, Italy

    Alessandra Gentile

  2. Department of Agriculture, Food and Environment, University of Catania, Catania, Italy

    Stefano La Malfa

  3. Horticulture and Landscape College, Hunan Agricultural University, Changsha, China

    Ziniu Deng

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Catara, V., Suming, D., Sarris, P.F. (2020). Molecular Mechanisms for Resistance to Biotic Stresses. In: Gentile, A., La Malfa, S., Deng, Z. (eds) The Citrus Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-15308-3_16

Download citation

Publish with us

Policies and ethics

Search

Navigation