Identification of Tomato Ve1 Homologous Proteins in Flax and Assessment for Race-Specific Resistance in Two Fiber FlaxCultivars against Verticillium dahliae Race 1.
Verticillium dahliae; fiber flax; race specific resistance; Ecology, Evolution, Behavior and Systematics; Ecology; Plant Science
Abstract :
[en] In the last decade, the soil borne fungal pathogen Verticillium dahliae has had an increasingly strong effect on fiber flax (Linum usitatissimum L.), thus causing important yield losses in Normandy, France. Race-specific resistance against V. dahliae race 1 is determined by tomato Ve1, a leucine-rich repeat (LRR) receptor-like protein (RLP). Furthermore, homologous proteins have been found in various plant families. Herein, four homologs of tomato Ve1 were identified in the flax proteome database. The selected proteins were named LuVe11, LuVe12, LuVe13 and LuVe14 and were compared to other Ve1. Sequence alignments and phylogenic analysis were conducted and detected a high similarity in the content of amino acids and that of the Verticillium spp. race 1 resistance protein cluster. Annotations on the primary structure of these homologs reveal several features of tomato Ve1, including numerous copies of a 28 amino acids consensus motif [XXIXNLXXLXXLXLSXNXLSGXIP] in the LRR domain. An in vivo assay was performed using V. dahliae race 1 on susceptible and tolerant fiber flax cultivars. Despite the presence of homologous genes and the stronger expression of LuVe11 compared to controls, both cultivars exhibited symptoms and the pathogen was observed within the stem. Amino acid substitutions within the segments of the LRR domain could likely affect the ligand binding and thus the race-specific resistance. The results of this study indicate that complex approaches including pathogenicity tests, microscopic observations and gene expression should be implemented for assessing race-specific resistance mediated by Ve1 within the large collection of flax genotypes.
Blum, Adrien ; Université de Liège - ULiège > Département GxABT > Plant Sciences ; UNILASALLE-Campus Rouen, Aghyle Unit, SFR Normandie Végétal FED 4277, 3 rue du Tronquet, 76134 Mont-Saint-Aignan Cedex, France ; Glycobiologie et Matrice Extracellulaire Végétale EA 4358, SFR Normandie Végétal FED 4277, Université de Rouen, 76821 Mont-Saint-Aignan, France
Castel, Lisa; UNILASALLE-Campus Rouen, Aghyle Unit, SFR Normandie Végétal FED 4277, 3 rue du Tronquet, 76134 Mont-Saint-Aignan Cedex, France
Trinsoutrot-Gattin, Isabelle ; UNILASALLE-Campus Rouen, Aghyle Unit, SFR Normandie Végétal FED 4277, 3 rue du Tronquet, 76134 Mont-Saint-Aignan Cedex, France
Driouich, Azeddine; Glycobiologie et Matrice Extracellulaire Végétale EA 4358, SFR Normandie Végétal FED 4277, Université de Rouen, 76821 Mont-Saint-Aignan, France
Laval, Karine; UNILASALLE-Campus Rouen, Aghyle Unit, SFR Normandie Végétal FED 4277, 3 rue du Tronquet, 76134 Mont-Saint-Aignan Cedex, France
Language :
English
Title :
Identification of Tomato Ve1 Homologous Proteins in Flax and Assessment for Race-Specific Resistance in Two Fiber FlaxCultivars against Verticillium dahliae Race 1.
Agrios, G.N. Plant Pathology; Academic Press: San Diego, CA, USA, 1997; 635p.
Belfanti, E.; Silfverberg-Dilworth, E.; Tartarini, S.; Patocchi, A.; Barbieri, M.; Zhu, J.; Vinatzer, B.A.; Gianfranceschi, L.; Gessler, C.; Sansavini, S. The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc. Natl. Acad. Sci. USA 2004, 101, 886–890.
Blum, A.; Bressan, M.; Zahid, A.; Trinsoutrot-Gattin, I.; Driouich, A.; Laval, K. Verticillium Wilt on fiber flax: Symptoms and pathogen development in planta. Plant Dis. 2018, 102, 2421–2429.
Chai, Y.; Zhao, L.; Liao ZSun, X.; Zuo, K.; Zhang, L.; Wang, S.; Tang, K. Molecular cloning of a potential Verticillium dahliae resistance gene SlVe1 with multi-site polyadenylation from Solanum lycopersicoides. DNA Seq. 2003, 14, 375–384.
Chinchilla, D.; Zipfel, C.; Robatzek, S.; Kemmerling, B.; Nürnberger, T.; Jones, J.D.G.; Felix, G.; Boller, T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 2007, 448, 497–500.
de Jonge, R.; van Esse, H.P.; Maruthachalam, K.; Bolton, M.D.; Santhanam, P.; Saber, M.K.; Zhang, Z.; Usami, T.; Lievens, B.; Subbarao, K.V. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. USA 2012, 109, 5110–5115.
Dereeper, A.; Audic, S.; Claverie, J.M.; Blanc, G. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol. Biol. 2010, 12, 8–10.
Dereeper, A.; Guignon, V.; Blanc, G.; Audic, S.; Buffet, S.; Chevenet, F.; Dufayard, J.F.; Guindon, S.; Lefort, V.; Lescot, M.; et al. Phylogeny fr: Robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36, W465–W469.
Diederichsen, A. Ex situ collections of cultivated flax (Linum usitatissimum L.) and other species of the genus Linum L. Genet. Resour. Crop. Evol. 2007, 54, 661–678.
Diwan, N.; Fluhr, R.; Eshed, Y.; Zamir, D.; Tanksley, S.D. Mapping of Ve in tomato: A gene conferring resistance to the broad-spectrum pathogen, Verticillium dahliae race 1. Theor. Appl. Genet. 1999, 98, 315–319.
Fei, J.; Chai, Y.R.; Wang, J.; Lin, J.; Sun, X.F.; Sun, C.; Zuo, K.J.; Tang, K.X. cDNA cloning and characterization of the Ve homo-logue gene StVe from Solanum torvum Swartz. DNA Seq. 2004, 15, 88–95.
Fradin, E.F.; Abd-El-Haliem, A.; Masini, L.; van den Berg, G.C.; Joosten, M.H.; Thomma, B.P. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 2011, 156, 2255–2265.
Fradin, E.F.; Thomma, B.P.H.J. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. al-boatrum. Mol. Plant Pathol. 2006, 7, 71–86.
Fradin, E.F.; Zhang, Z.; Rovenich, H.; Song, Y.; Liebrand, T.W.H.; Masini, L.; van den Berg, G.C.M.; Joosten, M.H.A.J.; Thomma, B.P.H.J. Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2. PLoS ONE 2014, 9, e88208.
Grogan, R.; Ioannou, N.; Schneider, R.; Sall, M.; Kimble, K. Verticillium wilt on resistant tomato cultivars in California: Virulence of isolates from plants and soil and relationship of inoculum density to disease incidence. Phytopathology 1979, 69, 1176–1180.
Hayes, R.J.; McHale, L.K.; Vallad, G.E.; Truco, M.J.; Michelmore, R.W.; Klosterman, S.J.; Maruthachalam, K.; Subbarao, K.V. The inheritance of resistance to Verticillium wilt caused by race 1 isolates of Verticillium dahliae in the lettuce cultivar La Brillante. Theor Appl. Genet. 2011, 123, 509–517.
Huis, R.; Hawkins, S.; Neutelings, G. Selection of reference genes for quantitative gene expression normalization in flax (Linum usitatissimum L.). BMC Plant Boil. 2010, 10, 71.
Inderbitzin PSubbarao, K.V. Verticillium Systematics and Evolution: How confusion impedes Verticillium Wilt management and how to resolve it. Phytopathology 2014, 104, 564–574.
Jeong, S.; Trotochaud, A.E.; Clark, S.E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 1999, 11, 1925–1933.
Jones, D.A.; Thomas, C.M.; Hammond-Kosack, K.E.; Balint-Kurti, P.J.; Jones, J.D.G. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 1994, 266, 789–793.
Käll, L.; Krogh, A.; Sonnhammer, E.L. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 2004, 338, 1027–1036.
Kawchuk, L.M.; Hachey, J.; Lynch, D.R.; Kulcsar, F.; van Rooijen, G.; Waterer, D.R.; Robertson, A.; Kokko, E.; Byers, R.; Howard, B.J.; et al. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. USA 2001, 98, 6511–6515.
Malnoy, M.; Xu, M.; Borejsza-Wysocka, E.; Korban, S.S.; Aldwinckle, H.S. Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol. Plant Microbe Interact. 2008, 21, 448–458.
Nürnberger, T.; Kemmerling, B. Receptor protein kinases: Pattern recognition receptors in plant immunity. Trends Plant Sci. 2006, 11, 519–522.
Ogawa, M.; Shinohara, H.; Sakagami, Y.; Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 2008, 319, 294.
Schaible, L.; Cannon, O.S.; Waddoups, V. Inheritance of resistance to Verticillium wilt in a tomato cross. Phytopathology 1951, 41, 986–990.
Schulze, B.; Mentzel, T.; Jehle, A.K.; Mueller, K.; Beeler, S.; Boller, T.; Felix, G.; Chinchilla, D. Rapid heteromerization and phos-phorylation of ligand-activated plant transmembrane receptors and their associated kinaseBAK1. J. Biol. Chem. 2010, 285, 9444– 9451.
Shepard, K.A.; Purugganan, M.D. Molecular population genetics of the Arabidopsis CLAVATA2 region the genomic scale of variation and selection in a selfing species. Genetics 2003, 163, 1083–1095.
Simko, I.; Costanzo, S.; Haynes, K.G.; Ewing, E.E.; Costanzo, S.; Christ, B.J.; Jones, R.W. Linkage disequilibrium mapping of a Verticillium dahliae resistance quantitative trait locus in tetraploid potato (Solanum tuberosum) through a candidate gene ap-proach. Theor. Appl. Genet. 2004, 108, 217–224.
Song, Y.; Zhang, Z.; Seidl, M.F.; Majer, A.; Jakse, J.; Javornik, B.; Thomma, B.P. Broad taxonomic characterization of Verticillium wilt resistance genes reveals an ancient origin of the tomato Ve1 immune receptor. Mol. Plant Pathol. 2017, 18, 195–209, doi:10.1111/mpp.12390.
Thomma, B.P.H.J.; van Esse, H.P.; Crous, P.W.; de Wit, P.J.G.M. Cladosporium fulvum (syn Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae. Mol. Plant Pathol. 2005, 6, 379–393.
Trotochaud, A.E.; Hao, T.; Wu, G.; Yang, Z.; Clark, S.E. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its as-sembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 1999, 11, 393–406.
Untergasser, A.; Cutcutache, I.; Koressaar, T.; Ye, J.; Faircloth, B.C.; Remm, M.; Rozen, S.G. Primer3—new capabilities and in-terfaces. Nucleic Acids Res. 2012, 40, e115.
Vaisey-genser, M.; Morris, D.H. Introduction: History of the cultivation and uses of flaxseed. In Flax, the Genus Linum; Muir, A., Westcott, N., Eds.; Taylor & Francis: London, UK, 2003; pp. 102–133.
Valade, R.; Cast, D.; Bert, F. Verticilliose du lin fibre, la prévention comme seule arme. Perspect. Agric. 2015, 424, 30–32.
Vallad, G.E.; Qin, Q.M.; Grube, R.; Hayes, R.J.; Subbarao, K.V. Characterization of race-specific interactions among isolates of Verticillium dahliae pathogenic on lettuce. Phytopathology 2006, 96, 1380–1387.
Vallad, G.E.; Subbarao, K.V. Colonization of resistant and susceptible lettuce cultivars by a green fluorescent protein-tagged isolate of Verticillium dahliae. Phytopathology 2008, 98, 871–885.
van Sumere, C. Retting of flax with special reference to enzyme-retting. In The Biology and Processing of Flax; Sharma, H.C., Van Sumere, C., Eds.; M Publications: Belfast, Northern Ireland, 1992; pp. 157–198.
Vinatzer, B.A.; Patocchi, A.; Gianfranceschi, L.; Tartarini, S.; Zhang, H.B.; Gessler, C.; Sansavini, S. Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol. Plant Microbe Interact. 2001, 14, 508–515.
Wang, G.; Ellendorff, U.; Kemp, B.; Mansfield, J.W.; Forsyth, A.; Mitchel, K.; Bastas, K.; Liu, C.M.; Woods-Tör, A.; Zipfel, C.; et al. A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol. 2008, 147, 503– 517.
Wang, Z.; Hobson, N.; Galindo, L.; Zhu, S.; Shi, D.; McDill, J.; Yang, L.; Hawkins, S.; Neutelings, G.; Datla, R.; et al. The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J. 2012, 72, 461–473.
Yadeta, K.A.; Thomma, B.P.H.J. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 2013, 4, 97.
Zelko, I.; Lux, A.; Sterckeman, T.; Martinka, M.; Kollárová, K.; Lišková, D. An easy method for cutting and fluorescent staining of thin roots. Ann. Bot. 2012, 110, 475–478.
Zhang, W.; Jiang, T.; Cui, X.; Qi, F.; Jian, G. Colonization in cotton plants by a green fluorescent protein labelled strain of Verti-cillium dahliae. Eur. J. Plant Pathol. 2012, 135, 867–876.
Zhang, Y.; Wang, X.; Yang, S.; Chi, J.; Zhang, G.; Ma, Z. Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbadense and functional analysis in Arabidopsis thaliana. Plant Cell Rep. 2011, 30, 2085–2096.
Zhang, Z.; Song, Y.; Liu, C.M.; Thomma, B.P.H.J. Mutational analysis of the Ve1 immune receptor that mediates Verticillium resistance in tomato. PLoS ONE 2014, 9, e99511.
Zhao, P.; Zhao, Y.; Jin, Y.; Zhang, T.; Guo, H. Colonization process of Arabidopsis thaliana roots by a green fluorescent protein-tagged isolate of Verticillium dahliae. Protein Cell 2014, 5, 94–98.
