A review on the role of ethylene in the pathogenicity and resistance against cotton pathogens

Document Type : Review

Authors

1 Agricultural Engineering Department, Minab Higher Education center, University of Hormozgan, Bandar abbas.

2 Department of Agriculture, Minab Higher Education Center, University of Hormozgan, Bandar Abbas, Iran.

3 1- Department of Plant Protection, Faculty of Agriculture, Agricultural Sciences and Natural Resources University of Khuzestan, Mollasani, Iran.

10.22092/ijcr.2024.365896.1216

Abstract

Background and objectives: Ethylene is a plant hormone with specific gaseous form that plays key role in many growth and development processes. Biosynthesis and signaling pathway of ethylene has been well undertaken by a wide number of studies. In addition to its function as a plant growth regulator, ethylene is involved in phenomena such as pathogenesis and defense responses in plants. Also, ethylene exhibits antagonistic and synergistic effects on other defense hormones like salicylic acid, jasmonic acid and abscisic acid, regulating various defense responses through activating different transcription factors in its complicated signaling pathway. Dual function of ethylene in two completely different processes, pathogenesis and resistance, clearly shows this complexity. Investigation of spatial patterns of ethylene shows its local and systemic activity in the induction of plant defense genes. The cotton plant (Gossypium hirsutum L.) as an economically important crop, is attacked by a number of pests and plant pathogens that significantly reduce the quantity and quality of the cotton product. One of the most important pathogens is the soil fungus Verticillium dahliae, which causes verticillium wilt disease in cotton and is highly destructive pathogen. This pathogen causes symptoms such as wilting, chlorosis and necrosis in the cotton plants. In this paper, we attempted to review the results of previous studies on the interaction between ethylene and cotton diseases for illustrating a clearer picture of ethylene role in both pathogenesis and resistance processes against cotton pathogens.
 
Conclusion: Ethylene plays a role in signaling during cotton-fungus V. dahliae interaction, and some components involved in ethylene signaling positively regulate cotton resistance to V. dahliae. On the other hand, in the cotton plants with defoliation symptoms induced by the fungus V. dahliae, the ethylene production is directly related to the severity of verticillium wilt in cotton. As a result, it seems that ethylene plays multiple and complex roles in regulating the immunity of cotton plant against V. dahliae fungus, which is involved in increasing the resistance and sensitivity of the cotton plants. Knowing more about the role of ethylene in cotton plants and identifying the positive and negative regulators of ethylene could be a promising option in order to generate disease resistance against plant pathogens.
 

Keywords

Main Subjects

References

  1. Abdelsamad, N.A., MacIntosh, G.C., and Leandro, L.F. 2019. Induction of ethylene inhibits development of soybean sudden death syndrome by inducing defense-related genes and reducing Fusarium virguliforme PloS One. 14(5): 1-21.
  2. Arshad, M., and Frankenberger, W.T. 2012. Ethylene: agricultural sources and applications. Springer science & Business media.
  3. Bashan, Y. 1994. Symptom expression and ethylene production in leaf blight of cotton caused by Alternaria macrospora and Alternaria alternata alone and in combination. Canadian Journal of Botany, 72(11): 1574-1579.
  4. Bent, A.F., Innes, R.W., Ecker, J.R., and Staskawicz, B.J. 1992. Disease development in ethyleneinsensitive Arabidopsis thaliana infected with virulent and avirulent Pseudomonas and Xanthomonas Molecular Plant-Microbe Interaction, 5: 372–78.
  5. Blake, S.N., Barry, K.M., Gill, W.M., Reid, J.B., and Foo, E. 2016. The role of strigolactones and ethylene in disease caused by Pythium irregulare. Molecular Plant Pathology, 17(5): 680-690.
  6. Boller, T. 2018. Ethylene in pathogenesis and disease resistance. Pp. 293-314. In:K. Mattoo (ed.) The plant hormone ethylene. CRC Press, USA.
  7. Bu, B., Qiu, D., Zeng, H., Guo, L., Yuan, J., and Yang, X. 2014. A fungal protein elicitor PevD1 induces Verticillium wilt resistance in cotton. Plant Cell Reports, 33: 461–470.
  8. Chandan, R.K., Kumar, R., Swain, D.M., Ghosh, S., Bhagat, P.K., Patel, S., Bagler, G., Sinha, A.K., and Jha, G. 2020. A novel cross talk of AtRAV1, an ethylene responsive transcription factor with MAP kinases imparts broad spectrum disease resistance in plants. bioRxiv, 2020-01.
  9. Chen, L., Zhang, L., Li, D., Wang, F., and Yu, D. 2013. WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 110: E1963–E1971.
  10. Chohan, S., Perveen, R., Abid, M., Tahir, M. N., and Sajid, M. 2020. Cotton diseases and their management. Cotton Production and Uses: Agronomy, Crop Protection and Postharvest Technologies, 239-270.
  11. Constable, G.A., and Bange, M.P. 2015. The yield potential of cotton (Gossypium hirsutum). Field Crops Research, 182: 98-106.
  12. Daayf, F., Nicole, M., and Geiger, J.P. 1995. Differentiation of Verticillium dahliae populations on the basis of vegetative compatibility and pathogenicity on cotton. European Journal of Plant Pathology, 101: 69-79.
  13. De Vos, M., Van Zaanen, W., Koornneef, A., Korzelius, J., Dicke, M., Van Loon, L.C., and Pieterse, M.J. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiology, 142: 352–363.
  14. Delaat, A.M.M., and Vanloon, L.C. 1983. Regulation of ethylene biosynthesis in virus-infected tobacco-leaves. 3. The relationship between stimulated ethylene production and symptom expression in virus-infected tobacco-leaves. Physiological Plant Pathology, 22: 261–273.
  15. Di, X., Gomila, J., and Takken, F.L. 2017. Involvement of salicylic acid, ethylene and jasmonic acid signaling pathways in the susceptibility of tomato to Fusarium oxysporum. Molecular Plant Pathology, 18(7): 1024-1035.
  16. Diaz, J., ten Have, A., and van Kan, J.A. 2002. The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiology, 129: 1341–51.
  17. Fengming, S., and Zhong, Z. 1998. The correlation between inhibition of ethylene production and trifluralin-iinduced resitance of cotton seedlings against Fusarium oxysporum sp. vasinfectum. Zhi wu Sheng li xue bao= Acta Phytophysiologica Sinica, 24(2): 111-118.
  18. Foroud, N.A., Pordel, R., Goyal, R.K., Ryabova, D., Eranthodi, A., Chatterton, S., and Kovalchuk, I. 2019. Chemical Activation of the Ethylene Signaling Pathway Promotes Fusarium graminearum Resistance in Detached Wheat Heads. Phytopathology, 109(5): 796-803.
  19. Fu, P., Piao, Y., Zhan, Z., Zhao, Y., Pang, W., Li, X., and Piao, Z. 2019. Transcriptome Arofile of Brassica rapa Reveals the Involvement of Jasmonic Acid, Ethylene, and Brassinosteroid Signaling Pathways in Clubroot Resistance. Agronomy, 9(10): 589.
  20. Galis, I., Smith, J.L. and Jameson, P.E. 2004. Salicylic acid-, but not cytokinin induced, resistance to WClMV is associated with increased expression of SA-dependent resistance genes in Phaseolus vulgaris. Journal of Plant Physiology, 161: 459–466.
  21. Genin, S., and Boucher, C. 2002. Ralstonia solanacearum: Secrets of a major pathogen unveiled by analysis of its genome. Molecular Plant Pathology, 3: 111–118.
  22. Gu, Y.Q., Wildermuth, M.C., Chakravarthy, S., Loh, Y.T., Yang, C., He, X., Han, Y., and Martin, G.B. 2002. Tomato transcription factors pti4, pti5, and pti6 activate defense responses when expressed in Arabidopsis. Plant Cell, 14: 817–31.
  23. Gautam, J.K., and Nandi, A.K. 2018. APD1, the unique member of Arabidopsis AP2 family influences systemic acquired resistance and ethylene-jasmonic acid signaling. Plant Physiology and Biochemistry, 133: 92-9.
  24. Guo, W., Jin, L., Miao, Y., He, X., Hu, Q., Guo, K., Zhu, L., and Zhang, X. 2016. An ethylene response-related factor, GbERF1-like, from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis. Plant Molecular Biology, 91(3): 305-18.
  25. Helliwell, E.E., Wang, Q., and Yang, Y. 2016. Ethylene biosynthesis and signaling is required for rice immune response and basal resistance against Magnaporthe oryzae Molecular Plant-Microbe Interactions, 29(11): 831-843.
  26. Hoffman, T., Schmidt, J.S., Zheng, X., and Bent, A. 1999. Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance. Plant Physiology, 119: 935-49.
  27. Jackson, M.B. 2018. Ethylene in root growth and development. Pp. 159-181. In:K. Mattoo (ed.) The plant hormone ethylene. CRC Press, USA.
  28. Jain, D., and Khurana, J.P. 2018. Role of pathogenesis-related (PR) proteins in plant defense mechanism. Pp. 265-281. In: Singh., and I.K. Singh (ed.), Molecular aspects of plant-pathogen interaction. Springer Press, Singapore.
  29. Jin, J.H., Zhang, H.X., Tan, J.Y., Yan, M.J., Li, D.W., Khan, A., and Gong, Z.H. 2016. A new ethylene-responsive factor CaPTI1 gene of pepper (Capsicum annuum) involved in the regulation of defense response to Phytophthora capsici. Frontiers in Plant Science, 6: 1217.
  30. Klosterman, S.J., Atallah, Z.K., Vallad, G.E., and Subbarao, K.V. 2009. Diversity, pathogenicity, and management of Verticillium Annual Review of Phytopathology, 47: 39-62.
  31. Lawrence, K., Hagan, A., Olsen, M., Faske, T., Hutmacher, R., Mueller, J., and Mehl, H. 2015. Cotton disease loss estimate committee report. Pp. 188-190. In: Proceedings of the 2015 Beltwide Cotton Conferences, San Antonio, TX. Cordova.
  32. Leon-Reyes, A., Spoel, S.H., De Lange, E.S., Abe, H., Kobayashi, M., Tsuda, S., Millenaar, F.F., Welschen, R.A., Ritsema, T., and Pieterse, C.M. 2009. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiology, 149(4): 1797-1809.
  33. Li, Z., Liu, H., Ding, Z., Yan, J., Yu, H., Pan, R., Hu, J., Guan, Y., and Hua, J. 2020. Low temperature enhances plant immunity via salicylic acid pathway genes that are repressed by ethylene. Plant Physiology, 182(1): 626-39.
  34. Li, Z., Zhang, Y., Ren, J., Jia, F., Zeng, H., Li, G., and Yang, X. 2022. Ethylene‐responsive factor ERF114 mediates fungal pathogen effector PevD1‐induced disease resistance in Arabidopsis thaliana. Molecular Plant Pathology, 23(6): 819-831.
  35. Liang, Y., Cui, S., Tang, X., Zhang, Y.I., Qiu, D., Zeng, H., Guo, L., Yuan, J., and Yang, X. 2018. An asparagine-rich protein Nbnrp1 modulate Verticillium dahliae protein PevD1-induced cell death and disease resistance in Nicotiana benthamiana. Frontiers in Plant Science, 9: 303.
  36. Liang, Y., Li, Z.E., Zhang, Y.I., Meng, F., Qiu, D., Zeng, H., Li, G., and Yang, X. 2021. Nbnrp1 mediates Verticillium dahliae effector PevD1-triggered defense responses by regulating sesquiterpenoid phytoalexins biosynthesis pathway in Nicotiana benthamiana. Gene, 768: 145280.
  37. Lucas, J.A. 2009. Plant Pathology and Plant Pathogens. John Wiley & Sons, USA, 265p.
  38. Lund, S.T., Stall, R.E., and Klee, H.J. 1998. Ethylene regulates the susceptible response to pathogen infection in tomato. The Plant Cell, 10(3): 371-382.
  39. Marco, S., and Levy, D. 1979. Involvement of ethylene in the development of cucumber mosaic virus-induced chlorotic lesions in cucumber cotyledons. Physiological Plant Pathology, 14: 235–244.
  40. Mishra, A., Khare, S., Trivedi, P. K., and Nath, P. 2008. Ethylene induced cotton leaf abscission is associated with higher expression of cellulase (GhCel1) and increased activities of ethylene biosynthesis enzymes in abscission zone. Plant Physiology and Biochemistry, 46(1): 54-63.
  41. Mysore, K.S., Crasta, O.R., Tuori, R.P., Folkerts, O., Swirsky, P.B., Martin, G.B. 2002. Comprehensive transcript profiling of Pto and Prf-mediated host defense responses to infection by Pseudomonas syringae tomato. Plant Journal, 32: 299–315.
  42. Nurimanguli, A.I.N.I., Wu, Y.L., Pan, Z. Y., An, Q.S., Shui, G.L., Shao, P.X., and NIE, X.H. 2023. Cotton ethylene response factor GhERF91 involved in the defense against Verticillium dahliae. Journal of Integrative Agriculture,
  43. Oku, H., and Shiraishi, T. 2017. Phytoalexins and host specificity in plant diseases. Pp. 41-60. In: Daniel (ed.), Handbook of Phytoalexin Metabolism and Action. Routledge Press. UK.
  44. Perato, S.M., Martínez-Zamora, M.G., Salazar, S.M., Díaz-Ricci, J.C. 2018. The elicitor AsES stimulates ethylene synthesis, induce ripening and enhance protection against disease naturally produced in avocado fruit. Scientia Horticulturae, 240: 288-292.
  45. Pieterse, C.M., van Wees, S.C., van Pelt, J.A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P.J., van Loon, L.C. 1998. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell, 10: 1571–80.
  46. Qadir, A., Hewett, E.W., Long, P.G., and Dilley, D.R. 2011. A non-ACC pathway for ethylene biosynthesis in Botrytis cinerea. Postharvest Biology and Technology, 62(3): 314-318.
  47. Robison, M.M., Griffith, M., Paulls, K.P., and Glick, B.R. 2001. Dual role for ethylene in susceptibility of tomato to Verticillium Journal of Phytopathology, 149: 385–388.
  48. Song, R., Li, J., Xie, C., Jian, W., and Yang, X. 2020. An overview of the molecular genetics of plant resistance to the Verticillium wilt pathogen Verticillium dahliae. International Journal of Molecular Sciences, 21(3): 1120.
  49. Stall, R.E., and Hall, C.B. 1984. Chlorosis and ethylene production in pepper leaves infected by Xanthomonas campestris vesicatoria. Phytopathology, 74: 373–375.
  50. Sun, H., Song, N., Ma, L., Li, J., Ma, L., Wu, J., and Wu, J. 2017. Ethylene signalling is essential for the resistance of Nicotiana attenuata against Alternaria alternata and phytoalexin scopoletin biosynthesis. Plant Pathology, 66(2): 277-284.
  51. Sun, X., Yu, G., Li, J., Liu, J., Wang, X., Zhu, G., Zhang, X., and Pan, H. 2018. AcERF2, an ethylene-responsive factor of Atriplex canescens, positively modulates osmotic and disease resistance in Arabidopsis thaliana. Plant Science, 274: 32-43.
  52. Tahmasebi, A., Zangeneh, M., Tahmasebi, A., Dizaji, A., and Koohi Habibi, M. 2010. Role of salicylic acid in resistance to plant viruses. Genetics in the 3rd Millennium 8:2203-2212. (In Persian).
  53. Tahmasebi, A., Dizaji, A., Zangeneh, M., and Koohi Habibi, M. 2011. Signal transduction pathways in resistance to plant viruses. Genetics in the 3rd Millennium, 9:2508-2520. (In Persian).
  54. Tarkowski, Ł.P., Van de Poel, B., Höfte, M., and Van den Ende, W. 2019. Sweet immunity: inulin boosts resistance of lettuce (Lactuca sativa) against grey mold (Botrytis cinerea) in an ethylene-dependent manner. International Journal of Molecular Sciences, 20(5): 1052.
  55. Tzeng, D.D., and De Vay, J.E. 1985. Physiological responses of Gossypium hirsutum to infection by defoliating and nondefoliating pathotypes of Verticillium dahliae Kleb. Physiological plant pathology, 26(1): 57-72.
  56. Vander Molen, G.E., Labavitch, J.M., Strand, L.L., and De Vay, J.E. 1983. Pathogen-induced vascular gels: ethylene as a host intermediate. Physiologia Plantarum, 59: 573–80.
  57. Veronese, P., Narasimhan, M.L., Stevenson, R.A., Zhu, J.K., Weller, S.C., Subbarao, K.V., and Bressan, R.A. 2003. Identification of a locus controlling Verticillium disease symptom response in Arabidopsis thaliana. The Plant Journal, 35(5): 574-587.
  58. Vilanova, L., Vall-llaura, N., Torres, R., Usall, J., Teixidó, N., Larrigaudière, C., and Giné-Bordonaba, J. 2017. Penicillium expansum (compatible) and Penicillium digitatum (non-host) pathogen infection differentially alter ethylene biosynthesis in apple fruit. Plant Physiology and Biochemistry, 120: 132-43.
  59. Wang, H., Lin, J., Chang, Y., and Jiang, C.Z. 2017. Comparative transcriptomic analysis reveals that ethylene/H2O2-mediated hypersensitive response and programmed cell death determine the compatible interaction of sand pear and Alternaria alternata. Frontiers in Plant Science, 8: 195.
  60. Wang, S., Han, K., Peng, J., Zhao, J., Jiang, L., Lu, Y., Zheng, H., Lin, L., Chen, J., and Yan, F. 2019. NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana. Molecular Plant Pathology, 20(7): 990-1004.
  61. Wang, J.H., Gu, K.D., Han, P.L., Yu, J.Q., Wang, C.K., Zhang, Q.Y., You, C.X., Hu, D.G., and Hao, Y.J. 2020. Apple ethylene response factor MdERF11 confers resistance to fungal pathogen Botryosphaeria dothidea. Plant Science, 291: 110351.
  62. Wang, T., Shaban, M., Shi, J., Wang, W., Liu, S., Nie, X., and Zhu, L. 2023. Attenuation of ethylene signaling increases cotton resistance to a defoliating strain of Verticillium dahliae. The Crop Journal, 11(1): 89-98.
  63. Wang, B., Yang, X., Zeng, H., Liu, H., Zhou, T., Tan, B., Yuan, J., Guo, L., and Qiu, D. 2012. The purification and characterization of a novel hypersensitive like response-inducing elicitor from Verticillium dahliae that induces resistance responses in tobacco. Applied Microbiology and Biotechnology, 93, 191–201.
  64. Weingart, H., Ullrich, H., Geider, K., and Völksch, B. 2001. The role of ethylene production in virulence of Pseudomonas syringae glycinea and phaseolicola. Phytopathology, 91(5): 511-518.
  65. Wiese, M.V., and DeVay, J.E. 1970. Growth regulator changes in cotton associated with defoliation caused by Verticillium albo-atrum. Plant Physiology, 45(3): 304-309.
  66. Yang, B., Wang, Y., Guo, B., Jing, M., Zhou, H., Li, Y., et al. 2019. The Phytophthora sojae RXLR effector Avh238 destabilizes soybean Type2 Gm ACS s to suppress ethylene biosynthesis and promote infection. New Phytologist, 222(1): 425-437.
  67. Yang, C., Li, W., Cao, J., Meng, F., Yu, Y., Huang, J., et al. 2017. Activation of ethylene signaling pathways enhances disease resistance by regulating ROS and phytoalexin production in rice. The Plant Journal, 89(2): 338-353.
  68. Yang, C.L., Liang, S., Wang, H.Y., Han, L.B., Wang, F.X., Cheng, H.Q., Wu, X.M., Qu, Z.L., Wu, J.H., and Xia, G.X. 2015. Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Molecular plant, 8(3): 399-411.
  69. Yuan, D.P., Zhang, C., Wang, Z.Y., Zhu, X.F., and Xuan, Y.H. 2018. RAVL1 activates brassinosteroids and ethylene signaling to modulate response to sheath blight disease in rice. Phytopathology, 108(9): 1104-13.
  70. Zhang, L., Wang, M., Li, N., Wang, H., Qiu, P., Pei, L., Xu, Z., Wang, T., Gao, E., Liu, J. and Liu, S. 2018. Long noncoding RNA s involve in resistance to Verticillium dahliae, a fungal disease in cotton. Plant biotechnology journal, 16(6): 1172-1185.
  71. Zhang, D.D., Wang, J., Wang, D., Kong, Z.Q., Zhou, L., Zhang, G.Y., Gui, Y.J., Li, J.J., Huang, J.Q., Wang, B.L., and Liu, C. 2019. Population genomics demystifies the defoliation phenotype in the plant pathogen Verticillium dahliae. New Phytologist, 222(2): 1012-1029.
  72. Zhao, S., Hong, W., Wu, J., Wang, Y., Ji, S., Zhu, S., Wei, C., Zhang, J., and Li, Y. 2017. A viral protein promotes host SAMS1 activity and ethylene production for the benefit of virus infection. Elife, 6: e27529.
  73. Zheng, X., Xing, J., Zhang, K., Pang, X., Zhao, Y., Wang, G., Zang, J., Huang, R., and Dong, J. 2019. Ethylene response factor ERF11 activates BT4 transcription to regulate immunity to Pseudomonas syringae. Plant Physiology, 180(2): 1132-1151.
  74. Zheng, H., Dong, L., Han, X., Jin, H., Yin, C., Han, Y., Li, B., Qin, H., Zhang, J., Shen, Q., and Zhang, K. 2020. The TuMYB46L‐TuACO3 module regulates ethylene biosynthesis in einkorn wheat defense to powdery mildew. The New Phytologist, 225(6): 2526.
  75. Zhu, L., Guo, J., Ma, Z., Wang, J., and Zhou, C. 2018. Arabidopsis transcription factor MYB102 increases plant susceptibility to aphids by substantial activation of ethylene biosynthesis. Biomolecules, 8(2): 39.
Iranian Journal of Cotton Researches
Volume 11, Issue 2
August 2023
Pages 23-36

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