リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「Transcriptional induction of capsidiol synthesis genes by wounding can promote pathogen signal-induced capsidiol synthesis」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

Transcriptional induction of capsidiol synthesis genes by wounding can promote pathogen signal-induced capsidiol synthesis

Kojima, Tomoya Asakura, Nobuhide Hasegawa, Shiori Hirasawa, Taishi Mizuno, Yuri Takemoto, Daigo Katou, Shinpei 信州大学 DOI:10.1186/s12870-019-2204-1

2023.02.03

概要

Background Plants are exposed to various forms of environmental stress. Penetration by pathogens is one of the most serious environmental insults. Wounding caused by tissue damage or herbivory also affects the growth and reproduction of plants. Moreover, wounding disrupts physical barriers present at the plant surface and increases the risk of pathogen invasion. Plants cope with environmental stress by inducing a variety of responses. These stress responses must be tightly controlled, because their unnecessary induction is detrimental to plant growth. In tobacco, WIPK and SIPK, two wound-responsive mitogen-activated protein kinases, have been shown to play important roles in regulating wound responses. However, their contribution to downstream wound responses such as gene expression is not well understood. Results To identify genes regulated by WIPK and SIPK, the transcriptome of wounded WIPK/SIPK-suppressed plants was analyzed. Among the genes down-regulated in WIPK/SIPK-suppressed plants, the largest group consisted of those involved in the production of antimicrobial phytoalexins. Almost all genes involved in the biosynthesis of capsidiol, a major phytoalexin in tobacco, were transcriptionally induced by wounding in WIPK/SIPK-dependent and -independent manners. 5-epi-aristolochene synthase (EAS) is the committing enzyme for capsidiol synthesis, and the promoter of EAS4, a member of the EAS family, was analyzed. Reporter gene analysis revealed that at least two regions each 40-50 bp length were involved in activation of the EAS4 promoter by wounding, as well as by artificial activation of WIPK and SIPK. Unlike transcripts of the capsidiol synthesis genes, accumulation of EAS protein and capsidiol itself were not induced by wounding; however, wounding significantly enhanced their subsequent induction by a pathogen-derived elicitor. Conclusions Our results suggest a so-called priming phenomenon since the induction of EAS by wounding is only visible at the transcript level. By inducing transcripts, not the proteins, of EAS and possibly other capsidiol synthesis genes at wound sites, plants can produce large quantities of capsidiol quickly if pathogens invade the wound site, whereas plants can minimize energy loss and avoid the cytotoxic effects of capsidiol where pathogens do not gain entry during wound healing.

この論文で使われている画像

参考文献

1. Freeman BC, Beattie GA. An overview of plant defenses against pathogens and herbivores. Plant Health Instructor. 2008. https://doi.org/10.1094/PHI-I- 2008-0226-01.

2. Jones JDG, Dangl JL. The plant immune system. Nature. 2006;444:323–9.

3. Ahuja I, Kissen R, Bones AM. Phytoalexins in defense against pathogens. Trends Plant Sci. 2012;17:73–90.

4. Rodríguez-Concepción M, Boronat A. Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis. Curr Opin Plant Biol. 2015;25:17–22.

5. Widmann C, Gibson S, Jarpe MB, Johnson GL. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev. 1999;79:143–80.

6. MAPK Group. Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci. 2002;7:301–8.

7. Ren D, Liu Y, Yang KY, Han L, Mao G, Glazebrook J, et al. A fungal- responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A. 2008;105:5638–43.

8. Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell. 2011;23:1639–53.

9. Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, Shibuya N, et al. A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J. 2010;63:599–612.

10. Yang KY, Liu Y, Zhang S. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci U S A. 2001;98:741–6.

11. Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H. Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell. 2011;23:1153–70.

12. Seo S, Katou S, Seto H, Gomi K, Ohashi Y. The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J. 2007;49:899–909.

13. Wu J, Hettenhausen C, Meldau S, Baldwin IT. Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell. 2007;19:1096–122.

14. Niki T, Mitsuhara I, Seo S, Ohtsubo N, Ohashi Y. Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol. 1998;39:500–7.

15. Sato C, Seto Y, Nabeta K, Matsuura H. Kinetics of the accumulation of jasmonic acid and its derivatives in systemic leaves of tobacco (Nicotiana tabacum cv. Xanthi nc) and translocation of deuterium-labeled jasmonic acid from the wounding site to the systemic site. Biosci Biotechnol Biochem. 2009;73:1962–70.

16. Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, et al. Analysis of 1. 9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature. 1998;391:485–8.

17. Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange- Billiard C, et al. Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright Yellow-2 cells. J Biol Chem. 2003;278:26666–76.

18. Opitz S, Nes WD, Gershenzon J. Both methylerythritol phosphate and mevalonate pathways contribute to biosynthesis of each of the major isoprenoid classes in young cotton seedlings. Phytochemistry. 2014;98:110–9.

19. Yin S, Mei L, Newman J, Back K, Chappell J. Regulation of sesquiterpene cyclase gene expression. Plant Physiol. 1997;115:437–51.

20. Newman JD, Yin S, Chappell J. Characterization of the TAC box, a cis- element within an elicitor-inducible sesquiterpene cyclase promoter. Plant J. 1998;16:1–12.

21. Kobayashi M, Ishihama N, Yoshioka H, Takabatake R, Tsuda S, Seo S, et al. Analyses of the cis-regulatory regions responsible for the transcriptional activation of the N resistance gene by Tobacco mosaic virus. J Phytopathol. 2010;158:826–8.

22. Li G, Meng X, Wang R, Mao G, Han L, Liu Y, et al. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet. 2012;8:e1002767.

23. Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, et al. WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell. 2015;27:2645–63.

24. Kamoun S, van West P, de Jong AJ, de Groot KE, Vleeshouwers VGAA, Govers F. A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol Plant-Microbe Interact. 1997;10:13–20.

25. Darvill AG, Albersheim P. Phytoalexins and their elicitors-a defense against microbial infection in plants. Annu Rev Plant Physiol. 1984;35:243–75.

26. Shibata Y, Ojika M, Sugiyama A, Yazaki K, Jones DA, Kawakita K, et al. The full-size ABCG transporters Nb-ABCG1 and Nb-ABCG2 function in pre- and postinvasion defense against Phytophthora infestans in Nicotiana benthamiana. Plant Cell. 2016;28:1163–81.

27. Han L, Li GJ, Yang KY, Mao G, Wang R, Liu Y, et al. Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J. 2010;64:114–27.

28. Kurusu T, Hamada J, Nokajima H, Kitagawa Y, Kiyoduka M, Takahashi A, et al. Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol. 2010;153:678–92.

29. Shibata Y, Kawakita K, Takemoto D. Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid-mediated signaling pathways. Mol Plant-Microbe Interact. 2010;23:1130–42.

30. Takemoto D, Shibata Y, Ojika M, Mizuno Y, Imano S, Ohtsu M, et al. Resistance to Phytophthora infestans: exploring genes required for disease resistance in Solanaceae plants. J Gen Plant Pathol. 2018;84:312–20.

31. Singh AK, Kumar SR, Dwivedi V, Rai A, Pal S, Shasany AK, et al. A WRKY transcription factor from Withania somnifera regulates triterpenoid withanolide accumulation and biotic stress tolerance through modulation of phytosterol and defense pathways. New Phytol. 2017;215:1115–31.

32. Zang D, Wang J, Zhang X, Liu Z, Wang Y. Arabidopsis heat shock transcription factor HSFA7b positively mediates salt stress tolerance by binding to an E-box-like motif to regulate gene expression. J Exp Bot. 2019;70:5355–74.

33. Song N, Ma L, Wang W, Sun H, Wang L, Baldwin IT, et al. An ERF2-like transcription factor regulates production of the defense sesquiterpene capsidiol upon Alternaria alternate infection. J Exp Bot. 2019;70:5895–908.

34. Chassot C, Buchala A, Schoonbeek HJ, Métraux JP, Lamotte O. Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. Plant J. 2008;55:555–67.

35. Felix G, Duran JD, Volko S, Boller T. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 1999;18:265–76.

36. Choi D, Ward BL, Bostock RM. Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme a reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell. 1992;4:1333–44.

37. Yoshioka H, Yamada N, Doke N. cDNA cloning of sesquiterpene cyclase and squalene synthase, and expression of the genes in potato tuber infected with Phytophthora infestans. Plant Cell Physiol. 1999;40:993–8.

38. Yang Q, Trinh HX, Imai S, Ishihara A, Zhang L, Nakayashiki H, et al. Analysis of the involvement of hydroxyanthranilate hydroxycinnamoyltransferase and caffeoyl-CoA 3-O-methyltransferase in phytoalexin biosynthesis in oat. Mol Plant-Microbe Interact. 2004;17:81–9.

39. Keller H, Czernic P, Ponchet M, Ducrot PH, Back K, Chappell J, et al. Sesquiterpene cyclase is not a determining factor for elicitor- and pathogen-induced capsidiol accumulation in tobacco. Planta. 1998;205:467–76.

40. Wilkie GS, Dickson KS, Gray NK. Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem Sci. 2003;28:182–8.

41. Xu G, Greene GH, Yoo H, Liu L, Marqués J, Motley J, et al. Global translational reprogramming is a fundamental layer of immune regulation in plants. Nature. 2017;545:487–90.

42. Merchante C, Brumos J, Yun J, Hu Q, Spencer KR, Enríquez P, et al. Gene- specific translation regulation mediated by the hormone-signaling molecule EIN2. Cell. 2015;163:684–97.

43. Ohtsu M, Shibata Y, Ojika M, Tamura K, Hara-Nishimura I, Mori H, et al. Nucleoporin 75 is involved in the ethylene-mediated production of phytoalexin for the resistance of Nicotiana benthamiana to Phytophthora infestans. Mol Plant-Microbe Interact. 2014;27:1318–30.

44. Katou S, Asakura N, Kojima T, Mitsuhara I, Seo S. Transcriptome analysis of WIPK/SIPK-suppressed plants reveals induction by wounding of disease resistance-related genes prior to the accumulation of salicylic acid. Plant Cell Physiol. 2013;54:1005–15.

45. Odell JT, Nagy F, Chua NH. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature. 1985; 313:810–2.

46. Mitsuhara I, Ugaki M, Hirochika H, Ohshima M, Murakami T, Gotoh Y, et al. Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 1996;37:49–59.

47. Takabatake R, Ando Y, Seo S, Katou S, Tsuda S, Ohashi Y, et al. MAP kinases function downstream of HSP90 and upstream of mitochondria in TMV resistance gene N-mediated hypersensitive cell death. Plant Cell Physiol. 2007;48:498–510.

48. Higo K, Ugawa Y, Iwamoto M, Korenaga T. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 1999;27:297–300.

49. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002; 30:325–7.

50. Shahmuradov IA, Gammerman AJ, Hancock JM, Bramley PM, Solovyev VV. PlantProm: a database of plant promoter sequences. Nucleic Acids Res. 2003;31:114–7.

51. Yokoo S, Inoue S, Suzuki N, Amakawa N, Matsui H, Nakagami H, et al. Comparative analysis of plant isochorismate synthases reveals structural mechanisms underlying their distinct biochemical properties. Biosci Rep. 2018;38:BSR20171457.

52. Matsukawa M, Shibata Y, Ohtsu M, Mizutani A, Mori H, Wang P, et al. Nicotiana benthamiana calreticulin 3a is required for the ethylene- mediated production of phytoalexins and disease resistance against oomycete pathogen Phytophthora infestans. Mol Plant-Microbe Interact. 2013;26:880–92.

参考文献をもっと見る