[en] Fiber flax (Linum usitatissimum L.), an important crop in Normandy (France), is increasingly affected by Verticillium wilt caused by the soilborne fungus Verticillium dahliae. This disease leads to nonnegligible yield losses and depreciated fibers that are consequently difficult to upgrade. Verticillium wilt is a major threat to a broad range of agriculture. In this study, susceptible fiber flax cultivar Adélie was infected by VdLu01 (isolated from fiber flax, this study) or green fluorescent protein-tagged VdLs17 (transformed and provided by the department of Plant Pathology, University of California, Davis). Between 3 and 4 weeks postinoculation, wilting symptoms on leaves were first observed, with acropetal growth during the following weeks. Pathogen development was tracked by confocal laser-scanning microscopy during the asymptomatic and symptomatic stages. First, conidia germination led to the development of hyphae on root epidermis; more particularly, on the zone of cell differentiation and around emerging lateral roots, while the zone of cell division and the root tip were free of the pathogen. At 3 days postinoculation, the zone of cell differentiation and lateral roots were embedded into a fungal mass. Swelling structures such as appressoria were observed at 1 week postinoculation. At 2 weeks postinoculation and onward, the pathogen had colonized xylem vessels in roots, followed by the stem and, finally, leaves during the symptomatic stage. Additionally, observations of infected plants after retting in the field revealed microsclerotia embedded inside the bast fiber bundle, thus potentially contributing to weakening of fiber. All of these results provide a global account of V. dahliae development when infecting fiber flax.
Zahid, Abderrakib; Glycobiologie et Matrice Extracellulaire végétale EA 4358, SFR Végétal-Agronomie, Université de Rouen, and Département de Production, Protection et Biotechnologie végétale (Unité de Génétique, Biotechnologies et Amélioration des Plantes) Institut Agronomique et Vétérinaire Hassan II B.P. 6202 Rabat-Instituts, Madinat Al Irfan C.P. 10101, Morocco
Agrios, G. N. 1997. Plant Pathology. Academic Press, San Diego, CA.
Agrios, G. N. 2005. Plant Pathology. Elsevier Academic Press, Burlington, MA.
Atallah, Z. K., Bae, J., Jansky, S. H., Rouse, D. I., and Stevenson, W. R. 2007. Multiplex real-time quantitative PCR to detect and quantify Verticillium dahliae colonization in potato lines that differ in response to Verticillium wilt. Phytopathology 97:865-872.
Baley, C. 2002. Analysis of flax fibres tensile behaviour and analysis of the tensile stiffness increase. Composites Part A. 33:939-948.
Banno, S., Saito, H., Sakai, H., Urushibara, T., Ikeda, K., Kabe, T., Kemmochi, I., and Fujimura, M. 2011. Quantitative nested real-time PCR detection of Verticillium longisporum and V. dahliae in the soil of cabbage fields. J. Gen. Plant Pathol. 77:282-291.
Bejarano-Alcázar, J., Termorshuizen, A. J., and Jiménez-Díaz, R. M. 1999. Singlesite root inoculations on eggplant with microsclerotia of Verticillium dahliae. Phytoparasitica 27:279-289.
Bhat, R. G., and Subbarao, K. V. 1999. Host range specificity in Verticillium dahliae. Phytopathology 89:1218-1225.
Bilodeau, G. J., Koike, S. T., Uribe, P., and Martin, F. N. 2012. Development of an assay for rapid detection and quantification of Verticillium dahliae in soil. Phytopathology 102:331-343.
Bressan, M., Blum, A., Castel, L., Trinsoutrot-Gattin, I., Laval, K., and Gangneux, C. 2016. Assessment of Verticillium flax inoculum in agroecosystem soils using real-time PCR assay. Appl. Soil Ecol. 108:176-186.
de Jonge, R., van Esse, H. P., Maruthachalam, K., Bolton, M. D., Santhanam, P., Saber, M. K., Zhang, Z., Usami, T., Lievens, B., and Subbarao, K. V. 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.
DeVay, J. E., Forreste, L. L., Garber, R. H., and Butterfield, E. J. 1974. Characteristics and concentration of propagules of Verticillium dahliae in airdried field soils in relation to prevalence of Verticillium wilt in cotton. Phytopathology 64:22-29.
Diwan, N., Fluhr, R., Eshed, Y., Zamir, D., and Tanksley, S. D. 1999. Mapping of Ve in tomato: A gene conferring resistance to the broad-spectrum pathogen, Verticillium dahliae race 1. Theor. Appl. Genet. 98:315-319.
Eastburn, D. M., and Chang, R. J. 1994. Verticillium dahliae: A causal agent of root discoloration of horseradish in Illinois. Plant Dis. 78:496-498.
Fitt, D. D. L., Bauers, F., Burhenne, S., and Paul, V. H. 1992. Occurrence of Verticillium dahliae on linseed (Linum usitatissimum) in the UK and Germany. Plant Pathol. 41:86-90.
Fitzell, R., Evans, G., and Fahy, P. C. 1980. Studies on the colonization of plant roots by Verticillium dahliae Klebahn with use of immunofluorescent staining. Aust. J. Bot. 28:357-368.
Focher, B., Marzetti, A., and Sharma, H. S. S. 1992. Changes in the structure and properties of flax during processing. Pages 329-342 in: Biology and Processing of Flax. H. S. S. Sharma and C. F. van Sumere, eds. M. Publications, Belfast, Northern Ireland.
FAO. 2016. FAOSTAT Database. Food and Agriculture Organization of the United Nations, Rome, Italy. Retrieved November 07, 2017 from http://www.fao.org/faostat/en/.
Fradin, E. F., and Thomma, B. P. H. J. 2006. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 7:71-86.
Fradin, E. F., Zhang, Z., Ayala, J. C. J., Castroverde, C. D. M., Nazar, R. N., Robb, J., Liu, C. M., and Thomma, B. P. H. J. 2009. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 150:320-332.
Gerik, J. S., and Huisman, O. C. 1988. Study of field-grown cotton roots infected with Verticillium dahliae using an immunoenzymatic staining technique. Phytopathology 78:1174-1178.
Grogan, R., Ioannou, N., Schneider, R., Sall, M., and Kimble, K. 1979. Verticillium wilt on resistant tomato cultivars in California: Virulence of isolates from plants and soil and relationship of inoculum density to disease incidence. Phytopathology 69:1176-1180.
Gunawardena, U., and Hawes, M. C. 2002. Tissue specific localization of root infection by fungal pathogens: Role of root border cells. Mol. Plant-Microbe Interact. 15:1128-1136.
Gunawardena, U., Rodriguez, M., Straney, D., Romeo, J. T., VanEtten, H. D., and Hawes, M. C. 2005. Tissue-specific localization of pea root infection by Nectria haematococca. Mechanisms and consequences. Plant Physiol. 137:1363-1374.
Hawes, M. C., Gunawardena, U., Miyasaka, S., and Zhao, X. 2000. The role of root border cells in plant defense. Trends Plant Sci. 5:128-133.
Hoagland, D. R., and Arnon, D. I. 1950. The water-culture method for growing plants without soil. Calif. Agric. Exp. Stn. Circ. 347:1-32.
Hoffmann, G. M., and Rondomanski, W. 1959. Eine Verticilliose des Leins (Linum usitatissimum L.) in Deutschland. Nachrichtenbl. Dtsch. Pflanzenschutzdienst (Berlin) 13:91-92.
Inderbitzin, P., Bostock, R. M., Davis, R. M., Usami, T., Platt, H. W., and Subbarao, K. V. 2011. Phylogenetics and taxonomy of the fungal vascular wilt pathogen Verticillium, with the descriptions of five new species. PLoS One 6:e28341.
Inderbitzin, P., and Subbarao, K. V. 2014. Verticillium systematics and evolution: How confusion impedes verticillium wilt management and how to resolve it. Phytopathology 104:564-574.
Karajeh, M. R. 2006. Seed transmission of Verticillium dahliae in olive as detected by a highly sensitive nested PCR-based assay. Phytopathol. Mediterr. 45:15-23.
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., Fischer, R., and Prüfer, D. 2001. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. USA 98:6511-6515.
Klosterman, S. J., Atallah, Z. K., Vallad, G. E., and Subbarao, K. V. 2009. Diversity pathogenicity and management of Verticillium species. Annu. Rev. Phytopathol. 47:39-62.
Klosterman, S. J., Subbarao, K. V., Kang, S., Veronese, P., Gold, S. E., Thomma, B. P. H. J., Chen, Z., Henrissat, B., Lee, Y.-H., Park, J., Garcia-Pedrajas, M. D., Barbara, D. J., Anchieta, A., de Jonge, R., Santhanam, P., Maruthachalam, K., Atallah, Z., Amyotte, S. G., Paz, Z., Inderbitzin, P., Hayes, R. J., Heiman, D. I., Young, S., Zeng, Q., Engels, R., Galagan, J., Cuomo, C. A., Dobinson, K. F., and Ma, L.-J. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathol. 7:e1002137.
Koressaar, T., and Remm, M. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289-1291.
Krikun, J., and Bernier, C. C. 1990. Morphology of microsclerotia of Verticillium dahliae in roots of gramineous plants. Can. J. Plant Pathol. 12:439-441.
Kroes, G. M. L. W., Loffler, H. J. M., Parlevliet, J. E., Keizer, L. C. P., and Lange, W. 1999. Interactions of Fusarium oxysporum f. sp. lini, the flax wilt pathogen, with flax and linseed. Plant Pathol. 48:491-498.
Marchal, M. E. 1940. Observations et recherches effectuées à la station de phytopathologie de l'état pendant l'année 1939. Bull. Inst. Agron. Gembloux 9:1-15.
Maruthachalam, K., Klosterman, S. J., Anchieta, A., Mou, B., and Subbarao, K. V. 2013. Colonization of spinach by Verticillium dahliae and effects of pathogen localization on the efficacy of seed treatments. Phytopathology 103: 268-280.
McCully, M. E. 2001. Niches for bacterial endophytes in crop plants: A plant biologist's view. Funct. Plant Biol. 28:983-990.
McDougall, B. M., and Rovira, A. D. 1970. Sites of exudation of 14 C-labelled compounds from wheat roots. New Phytol. 69:999-1003.
Mercado-Blanco, J., Collado-Romero, M., Parrilla-Araujo, S., Rodríguez- Jurado, D., and Jiménez-Díaz, R. M. 2003. Quantitative monitoring of colonization of olive genotypes by Verticillium dahliae pathotypes with real-time polymerase chain reaction. Physiol. Mol. Plant Pathol. 63: 91-105.
Millet, Y. A., Danna, C. H., Clay, N. K., Songnuan, W., Simon, M. D., Werck- Reichhart, D., and Ausubel, F. M. 2010. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973-990.
Morvan, C., Abdul-Hafez, A., Morvan, O., Jauneau, A., and Demarty, M. 1989. Physicochemical and biochemical studies of polysaccharides solubilized from under-retted flax. Plant Physiol. Biochem. 27:451-459.
Pegg, G. F., and Brady, B. L. 2002. Verticillium Wilts. CAB International, Oxford.
Plancot, B., Santaella, C., Jaber, R., Kiefer-Meyer, M. C., and Follet-Gueye, M.-L. 2013. Deciphering the responses of root border-like cells of Arabidopsis and flax to pathogen-derived elicitors. Plant Physiol. 163: 1584-1597.
Rashid, K. Y. 2003. Principal diseases of flax. Pages 102-133 in: Flax, the Genus Linum. A. Muir and N. Westcott, eds. Taylor & Francis, London.
Rick, C. M., Martin, F. M., and Gentile, A. 1959. Linkage of Verticillium resistance (Ve). Tomato Genet. Coop. 9:44.
Robb, E. J., Powell, D. A., and Street, P. F. S. 1989. Vascular coating: A barrier to colonization by the pathogen in Verticillium wilt of tomato. Can. J. Bot. 67: 600-607.
Robb, E. J., Street, P. F. S., and Busch, L. V. 1983. Basic fuchsin: A vascular dye in studies of Verticillium-infected chrysanthemum and tomato. Can. J. Bot. 61: 3355-3365.
Santhanam, P., van Esse, H. P., Albert, I., Faino, L., Nürnberger, T., and Thomma, B. P. 2013. Evidence for functional diversification within a fungal NEP1-like protein family. Mol. Plant-Microbe Interact. 26:278-286.
Schaible, L., Cannon, O. S., and Waddoups, V. 1951. Inheritance of resistance to Verticillium wilt in a tomato cross. Phytopathology 41:986-990.
Schreiber, L. R., and Green, R. J. 1963. Effect of root exudates on germination of conidia and microsclerotia of Verticillium albo-atrum inhibited by the soil fungistatic principle. Phytopathology 53:260-264.
Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., and Rozen, S. G. 2012. Primer3-New capabilities and interfaces. Nucleic Acids Res. 40:e115.
Valade, R., Cast, D., and Bert, F. 2015. Verticilliose du lin fibre, la prévention comme seule arme. Perspect. Agric. 424:30-32.
Vallad, G. E., Qin, Q.-M., Grube, R., Hayes, R. J., and Subbarao, K. V. 2006. Characterization of race-specific interactions among isolates of Verticillium dahliae pathogenic on lettuce. Phytopathology 96:1380-1387.
Vallad, G. E., and Subbarao, K. V. 2008. Colonization of Resistant and Susceptible Lettuce Cultivars by a Green Fluorescent Protein-Tagged Isolate of Verticillium dahliae. Phytopathology 98:871-885.
van Sumere, C. 1992. Retting of flax with special reference to enzyme-retting. Pages 157-198 in: The Biology and Processing of Flax. H. Sharma and C. Van Sumere, eds. M Publications, Belfast, Northern Ireland.
Wang, B., Yang, X., Zeng, H., Liu, H., Zhou, T., Guo, L., and Qiu, D. 2012. The purification and characterization of a novel hypersensitive-like responseinducing elicitor from Verticillium dahliae that induces resistance responses in tobacco. Appl. Microbiol. Biotechnol. 93:191-201.
Wang, J., Cai, Y., Gou, J., Mao, Y., Xu, Y., Jiang, W., and Chen, X. 2004. VdNEP, an elicitor from Verticillium dahliae, induces cotton plant wilting. Appl. Environ. Microb. 70:4989-4995.
Wilhelm, S. 1955. Longevity of the Verticillium wilt fungus in the laboratory and field. Phytopathology 45:180-181.
Yadeta, K. A., and Thomma, B. P. H. J. 2013. The xylem as battleground for plant hosts and vascular wilt pathogens. Front. Plant Sci. 4:97.
Zelko, I., Lux, A., Sterckeman, T., Martinka, M., Kollárová, K., and Lišková, D. 2012. An easy method for cutting and fluorescent staining of thin roots. Ann. Bot. 110:475-478.
Zhang, W., Jiang, T., Cui, X., Qi, F., and Jian, G. 2012. Colonization in cotton plants by a green fluorescent protein labelled strain of Verticillium dahliae. Eur. J. Plant Pathol. 135:867-876.
Zhao, P., Zhao, Y., Jin, Y., Zhang, T., and Guo, H. 2014. Colonization process of Arabidopsis thaliana roots by a green fluorescent protein-tagged isolate of Verticillium dahliae. Protein Cell 5:94-98.