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Infection processes of xylem-colonizing pathogenic bacteria: possible explanations for the scarcity of qualitative disease resistance genes against them in crops

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Disease resistance against xylem-colonizing pathogenic bacteria in crops.

Abstract

Plant pathogenic bacteria cause destructive diseases in many commercially important crops. Among these bacteria, eight pathogens, Ralstonia solanacearum, Xanthomonas oryzae pv. oryzae, X. campestris pv. campestris, Erwinia amylovora, Pantoea stewartii subsp. stewartii, Clavibacter michiganensis subsp. michiganensis, Pseudomonas syringae pv. actinidiae, and Xylella fastidiosa, infect their host plants through different infection sites and paths and eventually colonize the xylem tissues of their host plants, resulting in wilting symptoms by blocking water flow or necrosis of xylem tissues. Noticeably, only a relatively small number of resistant cultivars in major crops against these vascular bacterial pathogens except X. oryzae pv. oryzae have been found or generated so far, although these pathogens threaten productivity of major crops. In this review, we summarize the lifestyles of major xylem-colonizing bacterial pathogens and then discuss the progress of current research on disease resistance controlled by qualitative disease resistance genes or quantitative trait loci against them. Finally, we propose infection processes of xylem-colonizing bacterial pathogens as one of possible reasons for why so few qualitative disease resistance genes against these pathogens have been developed or identified so far in crops.

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References

  • Ben C et al (2013) MtQRRS1, an R-locus required for Medicago truncatula quantitative resistance to Ralstonia solanacearum. New Phytol 199:758–772. doi:10.1111/nph.12299

    Article  CAS  PubMed  Google Scholar 

  • Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744. doi:10.1126/science.1171647

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Buban T, Orosz-Kovacs Z, Farkas A (2003) The nectary as the primary site of infection by Erwinia amylovora (Burr.) Winslow et al.: a mini review. Plant Syst Evol 238:183–194. doi:10.1007/s00606-002-0266-1

    Google Scholar 

  • Camargo LEA, Williams PH, Osborn TC (1995) Mapping of quantitative trait loci controlling resistance of Brassica oleracea to Xanthomonas campestris pv. campestris in the field and greenhouse. Phytopathology 85:1296–1300

    Article  Google Scholar 

  • Carlos de Oliveira A, Bastianel M, Cristofani-Yaly M, Morais do Amaral A, Machado MA (2007) Development of genetic map of the citrus varieties ‘Murcott’ tangor and ‘Pera’ sweet orange by using fluorescent AFLP markers. J Appl Genet 48:219–231

    Article  PubMed  Google Scholar 

  • Chalupowicz L et al (2012) Colonization and movement of GFP-labeled Clavibacter michiganensis subsp. michiganensis during tomato infection. Phytopathology 102:23–31. doi:10.1094/PHYTO-05-11-0135

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee S, Almeida RP, Lindow S (2008) Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. Ann Rev phytopathol 46:243–271. doi:10.1146/annurev.phyto.45.062806.094342

    Article  CAS  Google Scholar 

  • Coaker GL, Francis DM (2004) Mapping, genetic effects, and epistatic interaction of two bacterial canker resistance QTLs from Lycopersicon hirsutum. Theor Appl Genet 108:1047–1055. doi:10.1007/s00122-003-1531-6

    Article  CAS  PubMed  Google Scholar 

  • Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lon B Biol Sci 363:557–572. doi:10.1098/rstb.2007.2170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Davis MJ, Gillaspie AG, Vidaver AK, Harris RW (1984) Clavibacter: a new genus containing some phytopathogenic Coryneform bacteria, including Clavibacter xyli subsp. xyli sp. nov., subsp. nov. and Clavibacter xyli subsp. cynodontis subsp. nov. pathogens that cause ratoon stunting disease of sugarcane and bermudagrass stunting disease. Int J Syst and Evol Microbio 34:107–117

    Google Scholar 

  • Deslandes L et al (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci USA 99:2404–2409. doi:10.1073/pnas.032485099

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Digonnet C et al (2012) Deciphering the route of Ralstonia solanacearum colonization in Arabidopsis thaliana roots during a compatible interaction: focus at the plant cell wall. Planta 236:1419–1431. doi:10.1007/s00425-012-1694-y

    Article  CAS  PubMed  Google Scholar 

  • Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ (2013) TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol 23:390–398. doi:10.1016/j.tcb.2013.04.003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eichenlaub R, Gartemann KH (2011) The Clavibacter michiganensis subspecies: molecular investigation of gram-positive bacterial plant pathogens. Ann Rev Phytopathol 49:445–464. doi:10.1146/annurev-phyto-072910-095258

    Article  CAS  Google Scholar 

  • Everett KR, Taylor RK, Romberg MK, Rees-George J, Fullerton RA, Vanneste JL, Manning MA (2011) First report of Pseudomonas syringae pv. actinidiae causing kiwifruit bacterial canker in New Zealand. Australas Plant Dis Notes 6:67–71

    Article  Google Scholar 

  • Foolad MR, Panthee DR (2012) Marker-assisted selection in tomato breeding. Crit Rev Plant Sci 31:93–123. doi:10.1080/07352689.2011.616057

    Article  Google Scholar 

  • Gartemann KH, Kirchner O, Engemann J, Grafen I, Eichenlaub R, Burger A (2003) Clavibacter michiganensis subsp. michiganensis: first steps in the understanding of virulence of a Gram-positive phytopathogenic bacterium. J Biotechnol 106:179–191

    Article  CAS  PubMed  Google Scholar 

  • Gartemann KH et al (2008) The genome sequence of the tomato-pathogenic actinomycete Clavibacter michiganensis subsp. michiganensis NCPPB382 reveals a large island involved in pathogenicity. J Bacteriol 190:2138–2149. doi:10.1128/JB.01595-07

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Godiard L, Sauviac L, Torri KU, Grenon O, Mangin B, Grimsley NH, Marco Y (2003) ERECTA, an LRR receptor-like kinase protein controlling development pleiotrophically affects resistance to bacterial wilt. Plant J 36:353–365

    Article  CAS  PubMed  Google Scholar 

  • Hai TTH, Esch E, Wang JF (2008) Resistance to Taiwanese race 1 strains of Ralstonia solanacearum in wild tomato germplasm. Eur J Plant Pathol 122:471–479

    Article  Google Scholar 

  • Hu KM, Qiu DY, Shen XL, Li XH, Wang SP (2008) Isolation and manipulation of quantitative trait loci for disease resistance in rice using a candidate gene approach. Mol Plant 1:786–793. doi:10.1093/mp/ssn039

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329. doi:10.1038/nature05286

    Article  CAS  PubMed  Google Scholar 

  • Khan MA, Zhao YF, Korban SS (2013) Identification of genetic loci associated with fire blight resistance in Malus through combined use of QTL and association mapping. Physiol Plant 148:344–353. doi:10.1111/ppl.12068

    Article  CAS  PubMed  Google Scholar 

  • Kifuji Y, Hanzawa H, Terasawa Y, Ashutosh Nishio T (2013) QTL analysis of black rot resistance in cabbage using newly developed EST-SNP markers. Euphytica 190:289–295. doi:10.1007/s10681-012-0847-1

    Article  CAS  Google Scholar 

  • Koh YJ, Kim GH, Koh HS, Lee YS, Kim SC, Jung JS (2012) Occurrence of a new type of Pseudomonas syringae pv. actinidiae strain of bacterial canker on kiwifruit in Korea. Plant Pathol J 28:423–427. doi:10.5423/Ppj.Nt.05.2012.0061

    Article  CAS  Google Scholar 

  • Konarska A, Masierowska M, Weryszko-Chmielewska E (2005) The structure of nectaries and nectar secretion in common pear (Pyrus communis L.). J Apic Sci 49:85–92

    Google Scholar 

  • Lavie M, Shillington E, Eguiluz C, Grimsley N, Boucher C (2002) PopP1, a new member of the YopJ/AvrRxv family of type III effector proteins, acts as a host-specificity factor and modulates aggressiveness of Ralstonia solanacearum. Mol Plant Microbe Interact 15:1058–1068. doi:10.1094/MPMI.2002.15.10.1058

    Article  CAS  PubMed  Google Scholar 

  • Lebeau A et al (2013) Genetic mapping of a major dominant gene for resistance to Ralstonia solanacearum in eggplant. Theor Appl Genet 126:143–158. doi:10.1007/s00122-012-1969-5

    Article  CAS  PubMed  Google Scholar 

  • Leigh JA, Coplin DL (1992) Exopolysaccharides in plant-bacterial interactions. Ann Rev Microbiol 46:307–346. doi:10.1146/annurev.mi.46.100192.001515

    Article  CAS  Google Scholar 

  • Li ZK et al (1999) A “defeated” rice resistance gene acts as a QTL against a virulent strain of Xanthomonas oryzae pv. oryzae. Mol Gen Genet 261:58–63

    Article  CAS  PubMed  Google Scholar 

  • Malnoy M, Martens S, Norelli JL, Barny MA, Sundin GW, Smits TH, Duffy B (2012) Fire blight: applied genomic insights of the pathogen and host. Ann Rev Phytopathol 50:475–494. doi:10.1146/annurev-phyto-081211-172931

    Article  CAS  Google Scholar 

  • Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, Leung H, Leach JE (2009) A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol 149:286–296. doi:10.1104/pp.108.128348

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mansfield J et al (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629. doi:10.1111/j.1364-3703.2012.00804.x

    Article  PubMed  Google Scholar 

  • Mukaihara T, Tamura N, Iwabuchi M (2010) Genome-wide identification of a large repertoire of Ralstonia solanacearum type III effector proteins by a new functional screen. Mol Plant Microbe Interact 23:251–262. doi:10.1094/MPMI-23-3-0251

    Article  CAS  PubMed  Google Scholar 

  • Newman KL, Almeida RPP, Purcell AH, Lindow SE (2003) Use of a green fluorescent strain for analysis of Xylella fastidiosa colonization of Vitis vinifera. Appl Environ Microbiol 69:7319–7327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139. doi:10.3389/fpls.2013.00139

    Article  PubMed Central  PubMed  Google Scholar 

  • Nino-Liu DO, Ronald PC, Bogdanove AJ (2006) Xanthomonas oryzae pathovars: model pathogens of a model crop. Mol Plant Pathol 7:303–324. doi:10.1111/j.1364-3703.2006.00344.x

    Article  CAS  PubMed  Google Scholar 

  • Oh CS, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16:132–140. doi:10.1016/j.tplants.2010.11.001

    Article  CAS  PubMed  Google Scholar 

  • Pataky JK, Bohn MO, Lutz JD, Richter PM (2008) Selection for quantitative trait loci associated with resistance to Stewart’s wilt in sweet corn. Phytopathology 98:469–474. doi:10.1094/PHYTO-98-4-0469

    Article  CAS  PubMed  Google Scholar 

  • Peeters N, Carrere S, Anisimova M, Plener L, Cazale AC, Genin S (2013a) Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex. BMC Genom 14:859. doi:10.1186/1471-2164-14-859

    Article  Google Scholar 

  • Peeters N, Guidot A, Vailleau F, Valls M (2013b) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic area. Mol Plant Pathology 14:651–662

    Article  CAS  Google Scholar 

  • Peeters N, Guidot A, Vailleau F, Valls M (2013c) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic area. Mol Plant Pathol 14:651–662

    Article  CAS  PubMed  Google Scholar 

  • Perez-Donoso AG, Sun Q, Roper MC, Greve LC, Kirkpatrick B, Labavitch JM (2010) Cell wall-degrading enzymes enlarge the pore size of intervessel pit membranes in healthy and Xylella fastidiosa-infected grapevines. Plant Physiol 152:1748–1759. doi:10.1104/pp.109.148791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Purcell AH, Hopkins DL (1996) Fastidious xylem-limited bacterial plant pathogens. Ann Rev Phytopathol 34:131–151. doi:10.1146/annurev.phyto.34.1.131

    Article  CAS  Google Scholar 

  • Renzi M, Copini P, Taddei AR, Rossetti A, Gallipoli L, Mazzaglia A, Balestra GM (2012) Bacterial canker on kiwifruit in Italy: anatomical changes in the wood and in the primary infection sites. Phytopathology 102:827–840. doi:10.1094/PHYTO-02-12-0019-R

    Article  PubMed  Google Scholar 

  • Riaz S, Krivanek AF, Xu K, Walker MA (2006) Refined mapping of the Pierce’s disease resistance locus, PdR1, and Sex on an extended genetic map of Vitis rupestris × V. arizonica. Theor Appl Genet 113:1317–1329. doi:10.1007/s00122-006-0385-0

    Article  CAS  PubMed  Google Scholar 

  • Roper MC (2011) Pantoea stewartii subsp. stewartii: lessons learned from a xylem-dwelling pathogen of sweet corn. Mol Plant Pathol 12:628–637

    Article  CAS  PubMed  Google Scholar 

  • Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370–374. doi:10.1038/nature05966

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schornack S et al (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  CAS  PubMed  Google Scholar 

  • Schuetz M, Smith R, Ellis B (2013) Xylem tissue specification, patterning, and differentiation mechanisms. J Exp Bot 64:11–31. doi:10.1093/jxb/ers287

    Article  CAS  PubMed  Google Scholar 

  • Scortichini M, Marcelletti S, Ferrante P, Petriccione M, Firrao G (2012) Pseudomonas syringae pv. actinidiae: a re-emerging, multi-faceted, pandemic pathogen. Mol Plant Pathol 13:631–640. doi:10.1111/j.1364-3703.2012.00788.x

    Article  PubMed  Google Scholar 

  • Simpson AJ et al (2000) The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa consortium of the organization for nucleotide sequencing and analysis. Nature 406:151–159. doi:10.1038/35018003

    Article  CAS  PubMed  Google Scholar 

  • Sinha D, Gupta MK, Patel HK, Ranjan A, Sonti RV (2013) Cell wall degrading enzyme induced rice innate immune responses are suppressed by the type 3 secretion system effectors XopN, XopQ, XopX and XopZ of Xanthomonas oryzae pv. oryzae. PLoS ONE 8:e75867. doi:10.1371/journal.pone.0075867

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Soengas P, Hand P, Vicente JG, Pole JM, Pink DA (2007) Identification of quantitative trait loci for resistance to Xanthomonas campestris pv. campestris in Brassica rapa. Theor Appl Genet 114:637–645. doi:10.1007/s00122-006-0464-2

    Article  CAS  PubMed  Google Scholar 

  • Sole M, Popa C, Mith O, Sohn KH, Jones JD, Deslandes L, Valls M (2012) The awr gene family encodes a novel class of Ralstonia solanacearum type III effectors displaying virulence and avirulence activities. Mol Plant-Microbe Interact 25:941–953. doi:10.1094/MPMI-12-11-0321

    Article  CAS  PubMed  Google Scholar 

  • Sun QH, Hu J, Huang GX, Ge C, Fang RX, He CZ (2005) Type-II secretion pathway structural gene xpsE, xylanase- and cellulase secretion and virulence in Xanthomonas oryzae pv. oryzae. Plant Pathol 54:15–21. doi:10.1111/j.1365-3059.2004.01101.x

    Article  CAS  Google Scholar 

  • Sun Q, Sun Y, Walker MA, Labavitch JM (2013) Vascular occlusions in grapevines with Pierce’s disease make disease symptom development worse. Plant Physiol 161:1529–1541. doi:10.1104/pp.112.208157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tabei H, Mukoo H (1960) Anatomical studies of rice plant leaves affected with bacterial leaf blight, in particular reference to the structure of water exudation system. Bull Nat Inst Agric Sci Tokyo 11:37–43

    Google Scholar 

  • Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB (1996) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 274:2060–2063

    Article  CAS  PubMed  Google Scholar 

  • Tonu NN, Doullah MA, Shimizu M, Karim MM, Kawanabe T, Fujimoto R, Okazaki K (2013) Comparison of positions of QTLs conferring resistance to Xanthomonas campestris pv. campestris in Brassica oleracea. Am J Plant Sci 4:11–20

    Article  Google Scholar 

  • Um HY et al (2013) Altered gene expression and intracellular changes of the viable but nonculturable state in Ralstonia solanacearum by copper treatment. Plant Pathol J 29:374–385. doi:10.5423/PPJ.OA.07.2013.0067

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vasse J, Frey P, Trigalet A (1995) Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol Plant Microbe Interact 8:241–251

    Article  CAS  Google Scholar 

  • Vicente JG, Holub EB (2013) Xanthomonas campestris pv. campestris (cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops. Mol Plant Pathol 14:2–18. doi:10.1111/j.1364-3703.2012.00833.x

    Article  CAS  PubMed  Google Scholar 

  • Vicente JG, Taylor JD, Sharpe AG, Parkin IA, Lydiate DJ, King GJ (2002) Inheritance of Race-Specific Resistance to Xanthomonas campestris pv. campestris in Brassica Genomes. Phytopathology 92:1134–1141. doi:10.1094/PHYTO.2002.92.10.1134

    Article  CAS  PubMed  Google Scholar 

  • Vrancken K, Holtappels M, Schoofs H, Deckers T, Valcke R (2013) Pathogenicity and infection strategies of the fire blight pathogen Erwinia amylovora in Rosaceae: state of the art. Microbiology 159:823–832. doi:10.1099/mic.0.064881-0

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Rong W, He C (2008) Two Xanthomonas extracellular polygalacturonases, PghAxc and PghBxc, are regulated by type III secretion regulators HrpX and HrpG and are required for virulence. Mol Plant-Microbe Interact 21:555–563. doi:10.1094/MPMI-21-5-0555

    Article  PubMed  Google Scholar 

  • Wang JF, Ho FI, Truong HTH, Huang SM, Balatero CH, Dittapongpitch V, Hidayati N (2013) Identification of major QTLs associated with stable resistance of tomato cultivar ‘Hawaii 7996’ to Ralstonia solanacearum. Euphytica 190:241–252. doi:10.1007/s10681-012-0830-x

    Article  CAS  Google Scholar 

  • Yadeta KA, J Thomma BP (2013) The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci 4:97. doi:10.3389/fpls.2013.00097

    PubMed Central  PubMed  Google Scholar 

  • Zhang H, Wang S (2013) Rice versus Xanthomonas oryzae pv. oryzae: a unique pathosystem. Curr Opin Plant Biol 16:188–195

    Article  PubMed  Google Scholar 

  • Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35:345–351. doi:10.1016/j.it.2014.05.004

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Golden Seed Project (Center for Horticultural Seed Development, No. 213003-04-2-SBG20), Ministry of Agriculture, Food and Rural Affairs (MAFRA), Ministry of Oceans and Fisheries (MOF), Rural Development Administration (RDA), and Korea Forest Service (KFS) and also by “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ009762),” Rural Development Administration, Republic of Korea, to CSO.

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The authors declare that they have no conflict of interest.

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Correspondence to Chang-Sik Oh.

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Communicated by R. K. Varshney.

C. Bae and S. W. Han equally contributed to this work.

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Bae, C., Han, S.W., Song, YR. et al. Infection processes of xylem-colonizing pathogenic bacteria: possible explanations for the scarcity of qualitative disease resistance genes against them in crops. Theor Appl Genet 128, 1219–1229 (2015). https://doi.org/10.1007/s00122-015-2521-1

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