biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 63:654-661, 2019 | DOI: 10.32615/bp.2019.071

Response of two Arabidopsis ecotypes Columbia-0 and Dijon-G to necrotrophic and biotrophic pathogens

Y.H. LEE1 +,Y.J. KIM1, J.Y. MOON2, H.J. KIM1, J.M. PARK2, I.S. HWANG3, J.K. HONG1,*
Department of Horticultural Science, Gyeongnam National University of Science and Technology,
1 Jinju 52725, Republic of Korea
2 and Biotechnology, Daejeon 34141, Republic of Korea
3 Department of Horticultural Biotechnology, Kyung Hee University, Yongin 17104, Republic of Korea

Arabidopsis thaliana L. ecotype Dijon-G (Di-G) showed a different symptom development during pathogenesis compared to ecotype Columbia-0 (Col-0). Previously, it has been shown that Di-G has a higher susceptibility to necrotrophic fungus Alternaria brassicicola than Col-0. In this study, Di-G showed enhanced disease susceptibility to necrotrophic fungi Botrytis cinerea, Sclerotinia sclerotiorum, and Sclerotium rolfsii known to secrete oxalic acid (OA) as a pathogenicity factor. Treatment with 50 and 100 mM OA resulted in a more leaf tissue collapse in Di-G than in Col-0. The OA also up-regulated expression of the salicylic acid (SA)-inducible pathogenesis-related gene 1 (PR1) and down-regulated expression of the jasmonic acid/ethylene-inducible defensin PDF1.2 gene in Di-G. By contrast, Di-G was resistant to hemibiotrophic fungus Colletotrichum higginsianum and biotrophic Turnip crinkle virus (TCV) infections. Application of 0.5 mM SA resulted in a higher accumulation of endogenous SA and in a preferential expression of SA-responsive genes in Di-G. Salicylic acid accelerated OA-triggered plant cell death and attenuated PDF1.2 expression in Di-G. These results suggest that the enhanced susceptibility of Di-G to necrotrophic pathogen infections might be mediated by attenuated JA-ethylene defence signalling and/or heightened SA-related defence signalling. Interaction of SA-signalling with OA secretion might be also involved in the enhanced susceptibility of Di-G.

Keywords: oxalic acid, pathogenesis-related gene PR1, plant defensin gene PDF1.2, salicylic acid.

Received: May 2, 2018; Revised: April 8, 2019; Accepted: May 6, 2019; Published online: October 22, 2019  Show citation

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LEE, Y.H., MOON, J.Y., KIM, H.J., PARK, J.M., HWANG, I.S., & HONG, J.K. (2019). Response of two Arabidopsis ecotypes Columbia-0 and Dijon-G to necrotrophic and biotrophic pathogens. Biologia plantarum, 63, Article 654-661. https://doi.org/10.32615/bp.2019.071
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    References

    1. Ahmad, S., Van Hulten, M., Martin, J., Pieterse, C.M.J., Van Wees, S.C.M., Ton, J.: Genetic dissection of basal defence responsiveness in accessions of Arabidopsis thaliana. - Plant Cell Environ. 34: 1191-1206, 2011. Go to original source...
    2. Bouchabke, O., Chang, F., Simon, M., Voisin, R., Pelletier, G., Durand-Tardif, M.: Natural variation in Arabidopsis thaliana as a tool for highlighting differential drought responses. - PLoS ONE 3: e1705, 2008. Go to original source...
    3. Brosché, M., Merilo, E., Mayer, F., Pechter, P., Puzõrjova, I., Brader, G., Kangasjärvi, J., Kollist, H.: Natural variation in ozone sensitivity among Arabidopsis thaliana accessions and its relation to stomatal conductance. - Plant Cell Environ. 33: 914-925, 2010 Go to original source...
    4. Chandra-Shekara, A.C., Navarre, D., Kachroo, A., Kang, H.-G., Klessig, D., Kachroo, P.: Signaling requirements and role of salicylic acid in HRT- and rrt-mediated resistance to turnip crinkle virus in Arabidopsis. - Plant J. 40: 647-659, 2004 Go to original source...
    5. Chatfield, S.P., Raizada, M.N.: Ethylene and shoot regeneration: hookless1 modulates de novo shoot organogenesis in Arabidopsis thaliana. - Plant Cell Rep. 27: 655-666, 2008. Go to original source...
    6. Clough, S.J., Bent, A.F.: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. - Plant J. 16: 735-743, 1998. Go to original source...
    7. Dempsey, D.A., Pathirana, M.S., Wobbe, K.K., Klessig, D.F.: Identification of an Arabidopsis locus required for resistance to turnip crinkle virus. - Plant J. 11: 301-311, 1997. Go to original source...
    8. Denby, K.J., Kumar, P., Kliebenstein, D.J.: Identification of Botrytis cinerea susceptibility loci in Arabidopsis thaliana. - Plant J. 38: 473-486, 2004. Go to original source...
    9. Falk, A., Feys, B.J., Frost, L.N., Jones, J.D.G., Daniels, M.J., Parker, J.E.: EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. - Proc. nat. Acad. Sci. USA 96: 3292-3297, 1999. Go to original source...
    10. Ferrari, S., Plotnikova, J.M., De Lorenzo, G., Ausubel, F.M.: Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. - Plant J. 35: 193-205, 2003. Go to original source...
    11. Glazebrook, J.: Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. - Annu. Rev. Phytopathol. 43: 205-227, 2005. Go to original source...
    12. Guo, X., Stotz, H.U.: Defense against Sclerotinia sclerotiorum in Arabidopsis is dependent on jasmonic acid, salicylic acid, and ethylene signaling. - Mol. Plant-Microbe Interact. 20: 1384-1395, 2007. Go to original source...
    13. Hannah, M.A., Wiese, D., Freund, S., Fiehn, O., Heyer, A.G., Hincha, D.K.: Natural genetic variation of freezing tolerance in Arabidopsis. - Plant Physiol. 142: 98-112, 2006. Go to original source...
    14. Jirage, D., Tootle, T.L., Reuber, T.L., Frost, L.N., Feys, B.J., Parker, J.E., Ausubel, F.M., Glazebrook, J.: Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. - Proc. nat. Acad. Sci. USA 96: 13583-13588, 1999. Go to original source...
    15. Kachroo, P., Yoshioka, K., Shah, J., Dooner, H.K., Klessig, D.F.: Resistance to turnip mosaic virus in Arabidopsis is required by two host genes and is salicylic acid dependent but not NPR1, ethylene, and jasmonate independent. - Plant Cell 12: 677-690, 2000. Go to original source...
    16. Kang, H.G., Kuhl, J.C., Kachroo, P., Klessig, D.F.: CRT1, an Arabidopsis ATPase that interacts with diverse resistance proteins and modulates disease resistance to Turnip Crinkle Virus. - Cell Host Microbe 3: 48-57, 2008. Go to original source...
    17. Kover, P.X., Schaal, B.A.: Genetic variation for disease resistance and tolerance among Arabidopsis thaliana accessions. - Proc. nat. Acad. Sci. USA 99: 11270-11274, 2002. Go to original source...
    18. Lehner, A., Meimoun, P., Errakhi, R., Madiona, K., Barakate, M., Bouteau, F.: Toxic and signalling effects of oxalic acid. - Plant Signal Behav. 3: 746-748. 2008. Go to original source...
    19. Leisner, S.M., Howell, S.H.: Symptom variation in different Arabidopsis thaliana ecotypes produced by cauliflower mosaic virus. - Phytopathology 82: 1042-1046, 1992. Go to original source...
    20. Lempe, J., Balasubramanian, S., Sureshkumar, S., Singh, A., Schmid, M., Weigel, D.: Diversity of flowering responses in wild Arabidopsis thaliana strains. - PLoS Genetics 1: e6, 2005. Go to original source...
    21. Leon-Reyes, A., Van der Does, D., De Lange, E.S., Delker, C., Wasternack, C., Van Wees, S. C.M., Ritsema, T., Pieterse, C.M.J.: Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. - Planta 232:1423-1432, 2010. Go to original source...
    22. Leon-Reyes, A., Du, Y., Koornneef, A., Proietti, S., Körbes, A.P., Memelink, J., Pieterse, C.M.J., Ritsema, T.: Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. - Mol. Plant-Microbe Interact. 23: 187-197, 2010. Go to original source...
    23. Liu, G., Kennedy, R., Greenshields, D.L., Peng, G., Forseille, L., Selvaraj, G., Wei, Y.: Detached and attached Arabidopsis leaf assays reveal distinct defense responses against hemibiotrophic Colletotrichum spp. - Mol. Plant-Microbe Interact. 20: 1308-1319, 2007. Go to original source...
    24. Liu, S., Ziegler, J., Zeier, J., Birkenbihl, R.P., Somssich, I.E.: Botrytis cinerea B05.10 promotes disease development in Arabidopsis by suppressing WRKY33-mediated host immunity. - Plant Cell Environ. 40: 2189-2206, 2017. Go to original source...
    25. Mang, H.G., Laluk, K.A., Parsons, E.P., Kosma, D.K., Cooper, B.R., Park, H.C., AbuQamar, S., Boccongelli, C., Miyazaki, S., Consiglio, F., Chilosi, G., Bohnert, H.J., Bressan, R.A., Mengiste, T., Jenks, M.A.: The Arabidopsis RESURRECTION1 gene regulates a novel antagonistic interaction in plant defense to biotrophs and necrotrophs. - Plant Physiol. 151: 290-305, 2009. Go to original source...
    26. Martín, A.M., Cabrera y Poch, H.L., Martínez Herrera, D., Ponz, F.: Resistance to turnip mosaic potyvirus in Arabidopsis thaliana. - Mol. Plant-Microbe Interact. 12: 1016-1021, 1999. Go to original source...
    27. Martín, A.M., Martínez Herrera, D., Poch y Cabrera, H.L., Ponz, F.: Variability in the interactions between Arabidopsis thaliana ecotypes and oilseed rape mosaic tobamovirus. - Aust. J. Plant Physiol. 24: 275-281, 1997. Go to original source...
    28. Matthes, M.C., Pickett, J.A., Napier, J.A.: Natural variation in responsiveness of Arabidopsis thaliana to methyl jasmonate is developmentally regulated. - Planta 228: 1021-1028, 2008. Go to original source...
    29. Moon, J.Y., Lee, J.H., Oh, C.S., Kang, H,G., Park, J.M.: Endoplasmic reticulum stress responses function in the HRT-mediated hypersensitive response in Nicotiana benthamiana. - Mol. Plant Pathol. 17: 1382-1397, 2016. Go to original source...
    30. Mukherjee, A.K., Lev, S., Gepstein, S., Horwitz, B.A.: A compatible interaction of Alternaria brassicicola with Arabidopsis thaliana ecotype DiG: evidence for a specific transcriptional signature. - BMC Plant Biol. 9: 31. 2009. Go to original source...
    31. Nandi, A., Moeder, W., Kacchroo, P., Klessig, D.F., Shah, J.: Arabidopsis ssi2-conferred susceptibility to Botrytis cinerea is dependent on EDS5 and PAD4. - Mol. Plant-Microbe Interact. 18:363-370, 2005. Go to original source...
    32. Nam, J., Mattysse, A.G., Gelvin, S.B.: Differences in susceptibility of Arabidopsis ecotypes to crown gall disease may result from a deficiency in T-DNA integration. - Plant Cell 9: 317-333, 1997. Go to original source...
    33. Narusaka, M., Yao, N., Iuchi, A., Iuchi, S., Shiraishi, T., Narusaka, Y.: Identification of Arabidopsis thaliana accession with resistance to Botrytis cinerea by natural variation analysis, and characterization of the resistance response. - Plant Biotechnol. 30: 89-95, 2013. Go to original source...
    34. Narusaka, Y., Narusaka, M., Park, P., Kubo, Y., Hirayama, T., Seki, M., Shiraishi, T., Ishida, J., Nakashima, M., Enju, A., Sakurai, T., Satou, M., Kobayashi, M., Shinozaki, K.: RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. - Mol. Plant-Microbe Interact. 17: 749-762, 2004. Go to original source...
    35. Nawrath, C., Heck, S., Parinthawong, N., Métraux, J.-P.: EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. - Plant Cell 14: 275-286, 2002. Go to original source...
    36. Nawrath, C., Métraux, J.-P.: Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. - Plant Cell 11: 1393-1404, 1999. Go to original source...
    37. Pan, X., Welti, R., Wang, X.: Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. - Nat. Protocol 5: 986-992, 2010. Go to original source...
    38. Park, J.M., Klessig, D.F.: HRT-mediated Turnip crinkle virus resistance in Arabidopsis. - Plant Pathol. J. 19: 19-23, 2003. Go to original source...
    39. Perchepied, L., Kroj, T., Tronchet, M., Loudet, O., Roby, D.: Natural variation in partial resistance to Pseudomonas syringae is controlled by two major QTLs in Arabidopsis thaliana. - PLoS ONE 1: e123, 2006. Go to original source...
    40. Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S., Van Wees, S.C.M.: Networking by small-molecule hormones in plant immunity. - Natur. chem. Biol. 5: 308-316, 2009. Go to original source...
    41. Rowe, H.C., Kliebenstein, D.J.: Complex genetic control natural variation in Arabidopsis thaliana resistance to Botrytis cinerea. - Genetics 180: 2237-2250, 2008. Go to original source...
    42. Schenk, P.M., Kazan, K., Manners, J.M., Anderson, J.P., Simpson, R.S., Wilson, I.W., Somerville, S.C., Maclean, D.J.: Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. - Plant Physiol. 132: 999-1010, 2003. Go to original source...
    43. Song, G.C., Lee, S., Hong, J., Choi, H.K., Hong, G.H., Bae, D.W., Mysore, K.S., Park, Y.-S., Ryu, C.-M.: Aboveground insect infestation attenuates belowground Agrobacterium-mediated genetic transformation. - New Phytol. 207: 148-158, 2015. Go to original source...
    44. Spoel, S.H., Johnson, J.S., Dong, X.: Regulation of trade offs between plant defenses against pathogens with different lifestyles. - Proc. nat. Acad. Sci. USA 104: 18842-18847, 2007. Go to original source...
    45. Van Leeuwen, H., Kliebenstein, D.J., West, M.A.L., Kim, K., Van Poecke, R., Katagiri, F., Michelmore, R.W., Doerge, R.W., St. Clair, D.A.: Natural variation among Arabidopsis thaliana accessions for transcriptome response to exogenous salicylic acid. - Plant Cell 19: 2099-2110, 2007. Go to original source...
    46. Van Wees, S.C.M., Chang, H.S., Zhu, T., Glazebrook, J.: Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. - Plant Physiol. 132: 606-617, 2003. Go to original source...
    47. Xiao, S., Calis, O., Patrick, E., Zhang, G., Charoenwattana, P., Muskett, P., Parker, J.E., Turner, J.G.: The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. - Plant J. 42: 95-110, 2005. Go to original source...
    48. Zhang, L., Ackley, A.R., Pilon-Smits, E.A.H.: Variation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. - J. Plant Physiol. 164: 327-336, 2007. Go to original source...

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