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Tomato Ve-resistance locus: resilience in the face of adversity?

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Abstract

Main conclusion

The Ve-resistance locus in tomato acts as a resilience gene by affecting both the stress/defense cascade and growth, constituting a signaling intercept with a competitive regulatory mechanism.

Abstract

For decades, the tomato Ve-gene has been recognized as a classical resistance R-gene, inherited as a dominant Mendelian trait and encoding a receptor protein that binds with a fungal effector to provide defense against Verticillium dahliae and V. albo-atrum. However, recent molecular studies suggest that the function and role(s) of the Ve-locus and the two proteins that it encodes are more complex than previously understood. This review summarizes both the background and recent molecular evidence and provides a reinterpretation of the function and role(s) of the Ve1- and Ve2-genes and proteins that better accommodates existing data. It is proposed that these two plasma membrane proteins interact to form a signaling intercept that directly links defense and growth. The induction of Ve1 by infection or wounding promotes growth but also downregulates Ve2 signaling, resulting in a decreased biosynthesis of PR proteins. In this context, the Ve1 R-gene acts as a Resilience gene rather than a Resistance gene, promoting taller more robust tomato plants with reduced symptoms (biotic and abiotic) and Verticillium concentration.

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Data sharing is not applicable to this article as no datasets were generated or analyzed.

References

  • Bar M, Sharfman M, Avni A (2011) LeEix1 functions as a decoy receptor to attenuate LeEix2 signaling. Plant Signal Behav 6:455–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol 121:96–102

    Article  Google Scholar 

  • Berne S, Javornik B (2016) Signalling crosstalk of plant defence responses to xylem-invading pathogens. In: Shanker A, Shanker C (eds) Abiotic and biotic stress in plants: recent advances and future perspectives. Intech Open, London, pp 1416–1435

    Google Scholar 

  • Bishop CD, Cooper RM (1983) An ultrastructure study of root invasion in three vascular wilt diseases. Physiol Plant Pathol 22:15–27

    Article  Google Scholar 

  • Castroverde CDM (2016) Molecular biology of the tomato Ve gene family. Molecular and cellular biology. University of Guelph, Guelph, pp 1–205

    Google Scholar 

  • Castroverde CDM, Nazar RN, Robb EJ (2016a) Verticillium Ave1 effector induces tomato defense gene expression independent of Ve1 prot. Plant Signal Behav 11:e1245254

    Article  PubMed  PubMed Central  Google Scholar 

  • Castroverde CDM, Nazar RN, Robb J (2016b) Verticillium Ave1 effector induces tomato defense gene expression independent of Ve1 protein. Plant Signal Behav 11:1–3

    Article  Google Scholar 

  • Castroverde CDM, Xu X, Nazar RN, Robb J (2017) Biotic factors that induce the tomato Ve1 R-gene. Plant Sci 265:61–69

    Article  CAS  PubMed  Google Scholar 

  • Castroverde CDM, Morais de Avila LG, Romero VA, Blaya-Fernandez J, Nazar RN, Robb J (2019) Differential repression of the Ve R-genes in tomato. Plant Gene 18:100174

    Article  CAS  Google Scholar 

  • Chen P, Lee B, Robb J (2004) Tolerance to a non-host isolate of Verticillium dahliae in tomato. Physiol Mol Plant Pathol 64:283–291

    Article  CAS  Google Scholar 

  • Cheung AY, Qu L-J, Russinova E, Zhao Y, Zipfel C (2020) Update on receptors and signaling. Plant Physiol 182:1527–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi HW, Klessig DF (2016) DAMPs, Pamps and NAMPs inplant immunity. BMC Plant Biology 16:232–241

    Article  PubMed  PubMed Central  Google Scholar 

  • de Jonge R, van Esse HP, Maruthachalam K, Bolton MD, Santhanam P, Saber MK, Zhang Z, Usami T, Lievens B, Subbarao KV, Thomma BPHJ (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc Natl Acad Sci USA 109:5110–5115

    Article  PubMed  PubMed Central  Google Scholar 

  • Deance N, Sanchez V, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155

    Google Scholar 

  • Deng Y, Zhai K, Xie Z, Yang D, Zhu X, Liu J, Wang X, Qin P, Yang Y, Zhang G, Li Q, Zhang J, Wu S, Milazzo J, Mao B, Wang E, Xie H, Tharreau D, He Z (2017) Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 335:963–965

    Google Scholar 

  • Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J (2008) Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant 3:423–445

    Article  Google Scholar 

  • Dinkel H, Van Roey K, Michael S, Kumar M, Uyar B, Altenberg B, Milchevskaya V, Schneider M, Kühn H, Behrendt A, Dahl SL, Damerell V, Diebel S, Kalman S, Klein S, Knudsen AC, Mäder C, Merrill S, Staudt A, Thiel V, Welti L, Davey NE, Diella F, Gibson T (2016) ELM 2016–data update and new functionality of the eukaryotic linear motif resource. Nucleic Acids Res 44:D294-300

    Article  CAS  PubMed  Google Scholar 

  • Diwan N, Fluhr R, Eshed Y, Zamir D, Tanksley SD (1999) Mapping of Ve in tomato: a gene conferring resistance to the broad-spectrum pathogen, Verticillium dahliae Kleb. race 1. Theor Appl Genet 98:315–319

    Article  CAS  Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209

    Article  CAS  PubMed  Google Scholar 

  • Flor HH (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–669

    Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Fradin EF, Thomma BPHJ (2006) Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7:71–86

    Article  CAS  PubMed  Google Scholar 

  • Fradin EF, Zhang Z, Juarez-Ayala JC, Castroverde CDM, Nazar RN, Robb J, Liu C-M, Thomma BPHJ (2009) Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol 150:320–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fradin EF, Abd-El-Haliem A, Masini L, van den Berg GC, Joosten MH, Thomma BPHJ (2011) Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol 156:2255–2265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fradin EF, Zhang Z, Rovenich H, Song Y, Liebrand TW, Masini L, van den Berg GC, Joosten MH, Thomma BPHJ (2014) Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homologue Ve2. PLoS ONE 9:e88208

    Article  PubMed  PubMed Central  Google Scholar 

  • Franci LJ, Wheeler TA (1993) Interaction of plant-parasitic nematodes with wilt-inducing fungi. In: Khan W (ed) Nematode interactions. Springer, New York, pp 79–103

    Chapter  Google Scholar 

  • Freeman BC, Beattie GA (2008) An overview of plant defenses against pathogens and herbivores. In: The plant health instructor. Iowa State University, Ames

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Genoud T, Métraux J-P (1999) Crosstalk in plant cell signaling: structure and function of the genetic network. Trends Plant Sci 4:503–507

    Article  CAS  PubMed  Google Scholar 

  • Gold J, Robb J (1995) The role of the coating response in Craigella tomatoes infected with Verticillium dahliae, races 1 and 2. Physiol Mol Plant Pathol 47:141–157

    Article  Google Scholar 

  • He M, He C-Q, Ding NZ (2018a) Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front Plant Sci 9:1771

    Article  PubMed  PubMed Central  Google Scholar 

  • He Y, Zhou J, Shan L, Meng X (2018b) Plant cell surface receptor-mediated signaling—a common theme amid diversity. J Cell Sci 131:jcs209353

    Article  PubMed  PubMed Central  Google Scholar 

  • Heath M (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334

    Article  CAS  PubMed  Google Scholar 

  • Heinz R, Lee SW, Saparno A, Nazar RN, Robb J (1998) Cyclical systemic colonization in Verticillium-infected tomato. Physiol Mol Plant Pathol 52:385–396

    Article  Google Scholar 

  • Imran QM, Yun B-W (2020) Pathogen-induced defense strategies in plants. J Crop Sci Biotech 23:97–105

    Article  Google Scholar 

  • Ingvardsen C, Veierskov B (2001) Ubiquitin- and proteasome-dependent proteolysis in plants. Physiol Plant 112:451–459

    Article  CAS  PubMed  Google Scholar 

  • Irani NG, Russinova E (2009) Receptor endocytosis and signaling in plants. Curr Opin Plant Biol 12:653–659

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Liang J, Noble PW (2007) Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol 23:435–461

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Karasov TL, Chae E, Herman JJ, Bergelson J (2017) Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29:666–680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawchuk LM, Lynch DR, Hachey J, Bains PS, Kulcsar F (1994) Identification of a codominant amplified polymorphic DNA marker linked to the verticillium wilt resistance gene in tomato. Theor Appl Genet 89:661–664

    Article  CAS  PubMed  Google Scholar 

  • Kawchuk L, Hachey J, Lynch DR, Klcsar F, van Rooijen G, Waterer DR, Robertson A, Kokko E, Byers R, Howard RJ, Fischer R, Prufer D (2001) Tomato Ve disease resistance genes encode cell surface-like receptors. Proc Natl Acad Sci USA 98:6511–6515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ku Y-S, Sintaha M, Cheung M-Y, Lam H-M (2018) Plant hormone signaling crosstalks between biotic and abiotic stress responses. Int J Mol Sci 19:3206

    Article  PubMed Central  Google Scholar 

  • Liang FS, Kong FN, Zhou CJ, Cao PX, Ye CJ, Wang B (2005) Cloning and characterization of a non-TIR-NBS-LRR type disease resistance gene analogue from peach. DNA Seq 16:103–110

    Article  CAS  PubMed  Google Scholar 

  • Mace ME, Bell AA, Beckman CH (1981) Fungal wilt diseases of plants. Academic Press, New York

    Google Scholar 

  • Mackey M, Kurosky A, Robb EJ, Nazar RN (2018) A graft mimic strategy for verticillium resistance in Tomato. Mol Biotechnol 60:665–669

    Article  CAS  PubMed  Google Scholar 

  • McAdam SAM, Brodribb TJ, Ross JJ (2016) Shoot-derived abscisic acid promotes root growth. Plant Cell Environ 39:652–659

    Article  CAS  PubMed  Google Scholar 

  • Mulligan RM, Chory J, Ecker JR (1997) Signaling in plants. Proc Natl Acad Sci USA 94:2793–2795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nazar RN, Robb J (2019) Signaling crosstalk in the Ve-resistance locus of tomato. Atlas of Science

  • Nazar RN, Castroverde CDM, Xu X, Kurosky A, Robb J (2018a) Wounding induces Tomato Ve1 R-gene expression, 2nd edon. In: Global conference on plant science and molecular biology

  • Nazar RN, Xu X, Kurosky A, Robb J (2018b) Antagonistic function of the Ve R-genes in tomato. Plant Mol Biol 98:67–79

    Article  CAS  PubMed  Google Scholar 

  • Nazar RN, Xu X, Shittu HO, Kurosky A, Robb EJ (2018c) Tomato Ve resistance locus; defense or growth. Planta 247:1339–1350

    Article  CAS  PubMed  Google Scholar 

  • Nazar RN, Xu X, Lee SW, Robb J (2020) The Ve-resistance locus, a plant signaling intercept. Planta 252:7–11

    Article  CAS  PubMed  Google Scholar 

  • Nishad R, Ahmed T, Rahman VJ, Kareem A (2020) Modulation of plant defense system in response to microbial interactions. Front Microbiol 11:1298

    Article  PubMed  PubMed Central  Google Scholar 

  • Pegg GF, Brady BL (2002) Verticillium wilts. CABI Publishing, Wallingford, Oxon

    Book  Google Scholar 

  • Powelson ML, Rowe RC (1993) Biology and management of early dying of potatoes. Annu Rev Phytopathol 31:111–126

    Article  CAS  PubMed  Google Scholar 

  • Preston GM (2000) Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol Plant Pathol 1:263–275

    Article  CAS  PubMed  Google Scholar 

  • Robb EJ, Powell DA, Street PFS (1989) Vascular coating: a barrier to colonization by the pathogen in Verticillium wilt of tomato. Can J Bot 67:600–607

    Article  Google Scholar 

  • Robb EJ, Shittu HO, Soman KV, Kurosky A, Nazar RN (2012) Elevated defense protein fails to protect tomato against Verticillium dahliae. Planta 236:623–633

    Article  CAS  PubMed  Google Scholar 

  • Ruthardt N, Fischer R, Emans N, Kawchuk LM (2007) Tomato protein of the resistance gene Ve2 to verticillium wilt [Verticillium spp.] is located in the endoplasmic reticulum. Can J Plant Pathol 29:3–8

    Article  CAS  Google Scholar 

  • Schaible L, Cannon OS, Waddoups V (1951) Inheritance of resistance to Verticillium wilt in a tomato cross. Phytopathology 41:986–990

    Google Scholar 

  • Sharfman M, Bar M, Ehrlich M, Schuster S, Melech-Bonfil S, Ezer R, Sessa S, Avni A (2011) Endosomal signaling of the tomato leucine-rich repeat receptor-like protein LeEix2. Plant J 68:418–423

    Article  Google Scholar 

  • Song Y, Zhang Z, Seidl MF, Majer A, Jakse JJ, Javornik B, Thomma BPHJ (2017) Broad taxonomic characterization of Verticillium wilt resistance genes reveals an ancient origin of the tomato Ve1 immune receptor. Mol. Plant Pathol. 18:195–201

    Article  CAS  PubMed  Google Scholar 

  • Street PFS, Robb J, Ellis BE (1986) Secretion of vascular coating components by xylem parenchyma cells of tomatoes infected with Verticillium albo-atrum. Protoplasma 132:1–11

    Article  Google Scholar 

  • Taylor JE, McAinsh MR (2004) Signalling crosstalk in plants: emerging issues. J Exptl Bot 55:147–149

    Article  CAS  Google Scholar 

  • Thomma BPHJ, Van Esse HP, Crous PW, De Wit PJGM (2005) Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Mol Plant Pathol 6:361–489

    Article  Google Scholar 

  • Thomma BPHJ, Nurnberger T, Joosten MH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Esse HP, Fradin EF, de Groot PJ, de Wit PJGM, Thomma BPHJ (2009) Tomato transcriptional responses to a foliar and a vascular fungal pathogen are distinct. Mol Plant Microbe Interact 22:245–258

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijin G, Van der Burg HA, Cornelissen BJC, Takken FLW (2007) Structure and function of resistance proteins in Solanaceous plants. Ann Rev Phytopathol 45:43–72

    Article  Google Scholar 

  • Vert G, Chory J (2011) Crosstalk in cellular signaling: background noise or the real thing? Dev. Cell 21:985–991

    CAS  Google Scholar 

  • Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu C-M, Woods-Tör A, Zipfel C, de Wit PJGM, Jones JDG, Tör M, Thomma BPHJ (2008) A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol 147:503–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10:1439–1462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Robb J, Nazar RN (2017) A “whole pot” strategy for root growth quantification or microbiota-root interaction studies. Soil Biol Biochem 111:154–156

    Article  CAS  Google Scholar 

  • Zhang Z, van Esse HP, van Damme M, Fradin EF, Liu C-M, Thomma BPHJ (2013) Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis. Mol Plant Pathol 14:719–727

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Song Y, Liu CM, Thomma B (2014) Mutational analysis of the Ve1 immune receptor that mediates Verticillium resistance in tomato. PLoS ONE 9:e99511

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Zhao F, Chen L, Pan Y, Sun L, Bao N, Zhang T, Cui C-X, Qiu Z, Zhang Y, Yang L, Xu L (2019) Jasmonate-mediated wound signalling promotes plant regeneration. Nat Plants 5:491–497

    Article  CAS  PubMed  Google Scholar 

  • Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Scheres B (2019) A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177:942–956

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    E. Jane Robb & Ross N. Nazar

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  1. E. Jane Robb
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  2. Ross N. Nazar
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Correspondence to E. Jane Robb.

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Communicated by Gerhard Leubner.

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Robb, E.J., Nazar, R.N. Tomato Ve-resistance locus: resilience in the face of adversity?. Planta 254, 126 (2021). https://doi.org/10.1007/s00425-021-03783-1

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