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Different Phytohormonal Responses on Satsuma Mandarin (Citrus unshiu) Leaves Infected with Host-Compatible or Host-Incompatible Elsinoë fawcettii

  • Shin, Kihye (Citrus Research Institute, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Paudyal, Dilli Prasad (Citrus Research Institute, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Lee, Seong Chan (Citrus Research Institute, National Institute of Horticultural and Herbal Science, Rural Development Administration) ;
  • Hyun, Jae Wook (Citrus Research Institute, National Institute of Horticultural and Herbal Science, Rural Development Administration)
  • Received : 2020.12.13
  • Accepted : 2021.04.23
  • Published : 2021.06.01

Abstract

Citrus scab, caused by the fungal pathogen Elsinoë fawcettii, is one of the most important fungal diseases affecting Citrus spp. Citrus scab affects young tissues, including the leaves, twigs, and fruits, and produces severe fruit blemishes that reduce the market value of fresh fruits. To study the molecular responses of satsuma mandarin (C. unshiu) to E. fawcettii, plant hormone-related gene expression was analyzed in response to host-compatible (SM16-1) and host-incompatible (DAR70024) isolates. In the early phase of infection by E. fawcettii, jasmonic acid- and salicylic acid-related gene expression was induced in response to infection with the compatible isolate. However, as symptoms advanced during the late phase of the infection, the jasmonic acid- and salicylic acid-related gene expression was downregulated. The gene expression patterns were compared between compatible and incompatible interactions. As scabs were accompanied by altered tissue growth surrounding the infection site, we conducted gibberellic acid- and abscisic acid-related gene expression analysis and assessed the content of these acids during scab symptom development. Our results showed that gibberellic and abscisic acid-related gene expression and hormonal changes were reduced and induced in response to the infection, respectively. Accordingly, we propose that jasmonic and salicylic acids play a role in the early response to citrus scab, whereas gibberellic and abscisic acids participate in symptom development.

Keywords

Acknowledgement

This study was supported by Project No. PJ01440101 for horticultural science and technological developments by the National Institute of Horticultural and Herbal Science, Rural Development Administration, Republic of Korea.

References

  1. Abdelkareem, A., Thagun, C., Nakayasu, M., Mizutani, M., Hashimoto, T. and Shoji, T. 2017. Jasmonate-induced biosynthesis of steroidal glycoalkaloids depends on COI1 proteins in tomato. Biochem. Biophys. Res. Commun. 489:206-210. https://doi.org/10.1016/j.bbrc.2017.05.132
  2. Antico, C. J., Colon, C., Banks, T. and Ramonell, K. M. 2012. Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens. Front. Biol. 7:48-56. https://doi.org/10.1007/s11515-011-1171-1
  3. Audenaert, K., De Meyer, G. B. and Hofte, M. M. 2002. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128:491-501. https://doi.org/10.1104/pp.010605
  4. Berens, M. L., Berry, H. M., Mine, A., Argueso, C. T. and Tsuda, K. 2017. Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 55:401-425. https://doi.org/10.1146/annurev-phyto-080516-035544
  5. Bitancourt, A. A. and Jenkins, A. E. 1936. Elsinoe fawcettii, the perfect stage of the citrus scab fungus. Phytopathology 26:393-395.
  6. Carvalho, K., de Campos, M. K. F., Pereira, L. F. P. and Vieira, L. G. E. 2010. Reference gene selection for real-time quantitative polymerase chain reaction normalization in "Swingle" citrumelo under drought stress. Anal. Biochem. 402:197-199. https://doi.org/10.1016/j.ab.2010.03.038
  7. Chung, K.-R. 2011. Elsinoe fawcettii and Elsinoe australis: the fungal pathogens causing citrus scab. Mol. Plant Pathol. 12:123-135. https://doi.org/10.1111/j.1364-3703.2010.00663.x
  8. De Vleesschauwer, D., Yang, Y., Cruz, C. V. and Hofte, M. 2010. Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol. 152:2036-2052. https://doi.org/10.1104/pp.109.152702
  9. Dewdney, J., Reuber, T. L., Wildermuth, M. C., Devoto, A., Cui, J., Stutius, L. M., Drummond, E. P. and Ausubel, F. M. 2000. Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 24:205-218. https://doi.org/10.1046/j.1365-313x.2000.00870.x
  10. Fan, W. and Dong, X. 2002. In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14:1377-1389. https://doi.org/10.1105/tpc.001628
  11. Finkelstein, R. R., Gampala, S. S. and Rock, C. D. 2002. Abscisic acid signaling in seeds and seedlings. Plant Cell 14 Suppl:S15-S45. https://doi.org/10.1105/tpc.010441
  12. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K. and Shinozaki, K. 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9:436-442. https://doi.org/10.1016/j.pbi.2006.05.014
  13. Gopal, K., Govindarajulu, B., Ramana, K. T. V., Kishore Kumar, C. S., Gopi, V., Gouri Sankar, T., Mukunda Lakshmi, L., Naga Lakshmi, T. and Sarada, G. 2014. Citrus scab (Elsinoe fawcettii): a review. Res. Rev. J. Agric. Allied Sci. 3:49-58.
  14. He, Y., Han, J., Liu, R., Ding, Y., Wang, J., Sun, L., Yang, X., Zeng, Y., Wen, W., Xu, J., Zhang, H., Yan, X., Chen, Z., Gu, Z., Chen, H., Tang, H., Deng, X. and Cheng, Y. 2018. Integrated transcriptomic and metabolomic analyses of a wax deficient citrus mutant exhibiting jasmonic acid-mediated defense against fungal pathogens. Hortic. Res. 5:43. https://doi.org/10.1038/s41438-018-0051-0
  15. Hok, S., Allasia, V., Andrio, E., Naessens, E., Ribes, E., Panabieres, F., Attard, A., Ris, N., Clement, M., Barlet, X., Marco, Y., Grill, E., Eichmann, R., Weis, C., Huckelhoven, R., Ammon, A., Ludwig-Muller, J., Voll, L. M. and Keller, H. 2014. The receptor kinase IMPAIRED OOMYCETE SUSCEPTIBILITY1 attenuates abscisic acid responses in Arabidopsis. Plant Physiol. 166:1506-1518. https://doi.org/10.1104/pp.114.248518
  16. Hyun, J.-W., Paudyal, D. P. and Hwang, R.-Y. 2015. Improved method to increase conidia production from isolates of different pathotypes of citrus scab pathogen Elsinoe spp. Res. Plant Dis. 21:231-234. https://doi.org/10.5423/RPD.2015.21.3.231
  17. Hyun, J.-W., Timmer, L. W., Lee, S.-C., Yun, S.-H., Ko, S.-W. and Kim, K.-S. 2001. Pathological characterization and molecular analysis of Elsinoe isolates causing scab diseases of citrus in Jeju Island in Korea. Plant Dis. 85:1013-1017. https://doi.org/10.1094/PDIS.2001.85.9.1013
  18. Hyun, J. W., Yi, S. H., Mackenzie, S. J., Timmer, L. W., Kim, K. S., Kang, S. K., Kwon, H. M. and Lim, H. C. 2009. Pathotypes and genetic relationship of worldwide collections of Elsinoe spp. causing scab diseases of citrus. Phytopathology 99:721-728. https://doi.org/10.1094/PHYTO-99-6-0721
  19. Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  20. Mauch-Mani, B. and Mauch, F. 2005. The role of abscisic acid in plant-pathogen interactions. Curr. Opin. Plant Biol. 8:409-414. https://doi.org/10.1016/j.pbi.2005.05.015
  21. Mafra, V., Kubo, K. S., Alves-Ferreira, M., Ribeiro-Alves, M., Stuart, R. M., Boava, L. P., Rodrigues, C. M. and Machado, M. A. 2012. Reference genes for accurate transcript normalization in citrus genotypes under different experimental conditions. PLoS ONE 7:e31263. https://doi.org/10.1371/journal.pone.0031263
  22. McAdam, E. L., Reid, J. B. and Foo, E. 2018. Gibberellins promote nodule organogenesis but inhibit the infection stages of nodulation. J. Exp. Bot. 69:2117-2130. https://doi.org/10.1093/jxb/ery046
  23. Oliveira, M. B., Junior, M. L., Grossi-de-Sa, M. F. and Petrofeza, S. 2015. Exogenous application of methyl jasmonate induces a defense response and resistance against Sclerotinia sclerotiorum in dry bean plants. J. Plant Physiol. 182:13-22. https://doi.org/10.1016/j.jplph.2015.04.006
  24. Park, S.-Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.-F. F. Alfred, S. E., Bonetta, D., Finkelstein, R., Provart, N. J., Desveaux, D., Rodriguez, P. L., McCourt, P., Zhu, J.-K., Schroeder, J. I., Volkman, B. F. and Cutler, S. R. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068-1071. https://doi.org/10.1126/science.1173041
  25. Paudyal, D. P. and Hyun, J.-W. 2015. Physical changes in satsuma mandarin leaf after infection of Elsinoe fawcettii causing citrus scab disease. Plant Pathol. J. 31:421-427. https://doi.org/10.5423/PPJ.NT.05.2015.0086
  26. Paudyal, D. P., Hyun, J.-W. and Hwang, R.-Y. 2017. Infection and symptom development by citrus scab pathogen Elsinoe fawcettii on leaves of satsuma mandarin. Eur. J. Plant Pathol. 148:807-816. https://doi.org/10.1007/s10658-016-1136-y
  27. Rieu, I., Ruiz-Rivero, O., Fernandez-Garcia, N., Griffiths, J., Powers, S. J., Gong, F., Linhartova, T., Eriksson, S., Nilsson, O., Thomas, S. G., Phillips, A. L. and Hedden, P. 2008. The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J. 53:488-504. https://doi.org/10.1111/j.1365-313X.2007.03356.x
  28. Shanmugam, G., Jeon, J. and Hyun, J.-W. 2020. Draft genome sequences of Elsinoe fawcettii and Elsinoe australis causing scab diseases on citrus. Mol. Plant-Microbe Interact. 33:135-137. https://doi.org/10.1094/MPMI-06-19-0169-A
  29. Shigenaga, A. M. and Argueso, C. T. 2016. No hormone to rule them all: interactions of plant hormones during the responses of plants to pathogens. Semin. Cell Dev. Biol. 56:174-189.
  30. Shimizu, T., Tanizawa, Y., Mochizuki, T., Nagasaki, H., Yoshioka, T., Toyoda, A., Fujiyama, A., Kaminuma, E. and Nakamura, Y. 2017. Draft sequencing of the heterozygous diploid genome of Satsuma (Citrus unshiu Marc.) using a hybrid assembly approach. Front. Genet. 8:180. https://doi.org/10.3389/fgene.2017.00180
  31. Staswick, P. E., Tiryaki, I. and Rowe, M. L. 2002. Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405-1415. https://doi.org/10.1105/tpc.000885
  32. Sun, T.-P. 2008. Gibberellin metabolism, perception and signaling pathways in Arabidopsis. Arabidopsis Book 6:e0103. https://doi.org/10.1199/tab.0103
  33. Sussmilch, F. C., Brodribb, T. J. and McAdam, S. 2017. Up-regulation of NCED3 and ABA biosynthesis occur within minutes of a decrease in leaf turgor but AHK1 is not required. J. Exp. Bot. 68:2913-2918. https://doi.org/10.1093/jxb/erx124
  34. Stowe, B. B. and Yamaki, T. 1957. The history and physiological action of the gibberellins. Annu. Rev. Plant Physiol. 8:181-216. https://doi.org/10.1146/annurev.pp.08.060157.001145
  35. Timmer, L. W., Priest, M., Broadbent, P. and Tan, M.-K. 1996. Morphological and pathological characterization of species of Elsinoe causing scab diseases of citrus. Phytopathology 86:1032-1038. https://doi.org/10.1094/Phyto-86-1032
  36. Ton, J., Flors, V. and Mauch-Mani, B. 2009. The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14:310-317. https://doi.org/10.1016/j.tplants.2009.03.006
  37. Ueno, Y., Yoshida, R., Kishi-Kaboshi, M., Matsushita, A., Jiang, C.-J., Goto, S., Takahashi, A., Hirochika, H. and Takatsuji, H. 2015. Abiotic stresses antagonize the rice defence pathway through the tyrosine-dephosphorylation of OsMPK6. PLoS Pathog. 11:e1005231. https://doi.org/10.1371/journal.ppat.1005231
  38. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R. K., Kumar, V., Verma, R., Upadhyay, R. G., Pandey, M. and Sharma, S. 2017. Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowl-edge and future prospects. Front. Plant Sci. 8:161. https://doi.org/10.3389/fpls.2017.00161
  39. Wasilewska, A., Vlad, F., Sirichandra, C., Redko, Y., Jammes, F., Valon, C., Frei dit Frey, N. and Leung, J. 2008. An update on abscisic acid signaling in plants and more. Mol. Plant 1:198-217. https://doi.org/10.1093/mp/ssm022
  40. Wu, P.-C., Chen, C.-W., Choo, C. Y. L., Chen, Y.-K., Yago, J. I. and Chung, K.-R. 2020. Biotin biosynthesis affected by the NADPH oxidase and lipid metabolism is required for growth, sporulation and infectivity in the citrus fungal pathogen Alternaria alternata. Microbiol. Res. 241:126566. https://doi.org/10.1016/j.micres.2020.126566
  41. Yasuda, M., Ishikawa, A., Jikumaru, Y., Seki, M., Umezawa, T., Asami, T., Maruyama-Nakashita, A., Kudo, T., Shinozaki, K., Yoshida, S. and Nakashita, H. 2008. Antagonistic interaction between systemic acquired resistance and the abscisic acidmediated abiotic stress response in Arabidopsis. Plant Cell 20:1678-1692. https://doi.org/10.1105/tpc.107.054296
  42. Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J., Shinozaki, K. and Yamaguchi-Shinozaki, K. 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61:672-685. https://doi.org/10.1111/j.1365-313X.2009.04092.x