The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development

English version České info

Plants have evolved sophisticated systems for adaptation to their natural habitat. In response to developmental and environmental cues, plants produce and perceive jasmonate (JA) signals, which induce degradation of JASMONATE-ZIM-Domain (JAZ) proteins and derepress the JAZ-repressed transcription factors to regulate diverse aspects of defense responses and developmental processes. Here, we identified the bHLH subgroup IIId transcription factors (bHLH3, bHLH13, bHLH14 and bHLH17) as novel targets of JAZs. These bHLH subgroup IIId transcription factors act as transcription repressors and function redundantly to negatively regulate JA responses. The quadruple mutant bhlh3 bhlh13 bhlh14 bhlh17 showed severe sensitivity to JA-inhibited root growth and JA-induced anthocyanin accumulation, and exhibited obvious increase in JA-regulated plant defense against pathogen infection and insect attack. Transgenic plants overexpressing bHLH13 or bHLH17 displayed reduced JA responses. Furthermore, these bHLH factors functioned as transcription repressors to antagonize the transcription activators, such as MYC2 and the WD-repeat/bHLH/MYB complex, through binding to their target sequences. Coordinated regulation of JA responses by transcription activators and repressors would benefit plants by allowing fine regulation of defense and development, and survival in their frequently changing environment.

Vyšlo v časopise: The bHLH Subgroup IIId Factors Negatively Regulate Jasmonate-Mediated Plant Defense and Development. PLoS Genet 9(7): e32767. doi:10.1371/journal.pgen.1003653
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003653

Souhrn

Zdroje

1. VanstraelenM, BenkovaE (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28: 463–487.

2. JonesJD, DanglJL (2006) The plant immune system. Nature 444: 323–329.

3. SpoelSH, DongX (2008) Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe 3: 348–351.

4. SchallerA, StintziA (2009) Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochemistry 70: 1532–1538.

5. WasternackC, HauseB (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot

6. CreelmanRA, MulletJE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48: 355–381.

7. StaswickPE, SuWP, HowellSH (1992) Methyl jasmonate inhibition of root-growth and induction of a leaf protein are decreased in an Arabidopsis thaliana Mutant. Proc Natl Acad Sci USA 89: 6837–6840.

8. FeysBJF, BenedettiCE, PenfoldCN, TurnerJG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751–759.

9. SunJ, XuY, YeS, JiangH, ChenQ, et al. (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21: 1495–1511.

10. ChenQ, SunJ, ZhaiQ, ZhouW, QiL, et al. (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23: 3335–3352.

11. McConnM, BrowseJ (1996) The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8: 403–416.

12. SongS, QiT, HuangH, RenQ, WuD, et al. (2011) The Jasmonate-ZIM Domain Proteins Interact with the R2R3-MYB Transcription Factors MYB21 and MYB24 to Affect Jasmonate-Regulated Stamen Development in Arabidopsis. Plant Cell 23: 1000–1013.

13. LiL, ZhaoY, McCaigBC, WingerdBA, WangJ, et al. (2004) The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126–143.

14. QiT, SongS, RenQ, WuD, HuangH, et al. (2011) The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana. Plant Cell 23: 1795–1814.

15. YoshidaY, SanoR, WadaT, TakabayashiJ, OkadaK (2009) Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136: 1039–1048.

16. LackmanP, Gonzalez-GuzmanM, TillemanS, CarqueijeiroI, PerezAC, et al. (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci U S A 108: 5891–5896.

17. YanJ, LiH, LiS, YaoR, DengH, et al. (2013) The Arabidopsis F-Box Protein CORONATINE INSENSITIVE1 Is Stabilized by SCFCOI1 and Degraded via the 26S Proteasome Pathway. Plant Cell doi:10.1105/tpc.112.105486.

18. ShanX, WangJ, ChuaL, JiangD, PengW, et al. (2011) A role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 155: 751–764.

19. RobsonF, OkamotoH, PatrickE, HarrisSR, WasternackC, et al. (2010) Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell 22: 1143–1160.

20. YanYX, StolzS, ChetelatA, ReymondP, PagniM, et al. (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19: 2470–2483.

21. HoweGA, JanderG (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59: 41–66.

22. LorenzoO, ChicoJM, Sanchez-SerranoJJ, SolanoR (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16: 1938–1950.

23. ThalerJS, HumphreyPT, WhitemanNK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17: 260–270.

24. HuP, ZhouW, ChengZ, FanM, WangL, et al. (2013) JAV1 Controls Jasmonate-Regulated Plant Defense. Mol Cell 50: 504–515.

25. WathugalaDL, HemsleyPA, MoffatCS, CremelieP, KnightMR, et al. (2012) The Mediator subunit SFR6/MED16 controls defence gene expression mediated by salicylic acid and jasmonate responsive pathways. New Phytol 195: 217–230.

26. SeoJS, JooJ, KimMJ, KimYK, NahmBH, et al. (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65: 907–921.

27. YanJ, ZhangC, GuM, BaiZ, ZhangW, et al. (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21: 2220–2236.

28. FonsecaS, ChiniA, HambergM, AdieB, PorzelA, et al. (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344–350.

29. ChiniA, FonsecaS, FernandezG, AdieB, ChicoJM, et al. (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666–671.

30. ThinesB, KatsirL, MelottoM, NiuY, MandaokarA, et al. (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448: 661–665.

31. KatsirL, SchilmillerAL, StaswickPE, HeSY, HoweGA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105: 7100–7105.

32. SheardLB, TanX, MaoH, WithersJ, Ben-NissanG, et al. (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468: 400–405.

33. BrowseJ (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol 60: 183–205.

34. SantnerA, EstelleM (2007) The JAZ proteins link jasmonate perception with transcriptional changes. Plant Cell 19: 3839–3842.

35. KazanK, MannersJM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17: 22–31.

36. PauwelsL, GoossensA (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23: 3089–3100.

37. De GeyterN, GholamiA, GoormachtigS, GoossensA (2012) Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci 17: 349–359.

38. ShanX, YanJ, XieD (2012) Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 15: 84–91.

39. NiuY, FigueroaP, BrowseJ (2011) Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot 62: 2143–2154.

40. Fernandez-CalvoP, ChiniA, Fernandez-BarberoG, ChicoJM, Gimenez-IbanezS, et al. (2011) The Arabidopsis bHLH Transcription Factors MYC3 and MYC4 Are Targets of JAZ Repressors and Act Additively with MYC2 in the Activation of Jasmonate Responses. Plant Cell 23: 701–715.

41. ChengZ, SunL, QiT, ZhangB, PengW, et al. (2011) The bHLH Transcription Factor MYC3 Interacts with the Jasmonate ZIM-Domain Proteins to Mediate Jasmonate Response in Arabidopsis. Mol Plant 4: 279–288.

42. ChengH, SongS, XiaoL, SooHM, ChengZ, et al. (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5: e1000440.

43. LiH, SunJ, XuY, JiangH, WuX, et al. (2007) The bHLH-type transcription factor AtAIB positively regulates ABA response in Arabidopsis. Plant Mol Biol 65: 655–665.

44. HeimMA, JakobyM, WerberM, MartinC, WeisshaarB, et al. (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20: 735–747.

45. Toledo-OrtizG, HuqE, QuailPH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15: 1749–1770.

46. GonzalezA, ZhaoM, LeavittJM, LloydAM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53: 814–827.

47. GlazebrookJ (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205–227.

48. ThommaBP, EggermontK, PenninckxIA, Mauch-ManiB, VogelsangR, et al. (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci U S A 95: 15107–15111.

49. Mene-SaffraneL, DubugnonL, ChetelatA, StolzS, Gouhier-DarimontC, et al. (2009) Nonenzymatic oxidation of trienoic fatty acids contributes to reactive oxygen species management in Arabidopsis. J Biol Chem 284: 1702–1708.

50. ParkJH, HalitschkeR, KimHB, BaldwinIT, FeldmannKA, et al. (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31: 1–12.

51. PenninckxIA, EggermontK, TerrasFR, ThommaBP, De SamblanxGW, et al. (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8: 2309–2323.

52. EppleP, ApelK, BohlmannH (1997) ESTs reveal a multigene family for plant defensins in Arabidopsis thaliana. FEBS Lett 400: 168–172.

53. Berrocal-LoboM, MolinaA, SolanoR (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29: 23–32.

54. MasonHS, DeWaldDB, MulletJE (1993) Identification of a methyl jasmonate-responsive domain in the soybean vspB promoter. Plant Cell 5: 241–251.

55. MelottoM, UnderwoodW, KoczanJ, NomuraK, HeSY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969–980.

56. YangDL, YaoJ, MeiCS, TongXH, ZengLJ, et al. (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci U S A 109: E1192–1200.

57. PauwelsL, BarberoGF, GeerinckJ, TillemanS, GrunewaldW, et al. (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464: 788–791.

58. TiwariSB, WangXJ, HagenG, GuilfoyleTJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13: 2809–2822.

59. NesiN, DebeaujonI, JondC, PelletierG, CabocheM, et al. (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12: 1863–1878.

60. ZhangF, GonzalezA, ZhaoM, PayneCT, LloydA (2003) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130: 4859–4869.

61. MatsuiK, UmemuraY, Ohme-TakagiM (2008) AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J 55: 954–967.

62. ZimmermannIM, HeimMA, WeisshaarB, UhrigJF (2004) Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40: 22–34.

63. HouX, LeeLY, XiaK, YanY, YuH (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19: 884–894.

64. NakataM, MitsudaN, HerdeM, KooAJ, MorenoJE, et al. (2013) A bHLH-Type Transcription Factor, ABA-INDUCIBLE BHLH-TYPE TRANSCRIPTION FACTOR/JA-ASSOCIATED MYC2-LIKE1, Acts as a Repressor to Negatively Regulate Jasmonate Signaling in Arabidopsis. Plant Cell In Press: tpc.113.111112.

65. OhtaM, Ohme-TakagiM, ShinshiH (2000) Three ethylene-responsive transcription factors in tobacco with distinct transactivation functions. Plant J 22: 29–38.

66. GuoS, XuY, LiuH, MaoZ, ZhangC, et al. (2013) The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4: 1566.

67. TaoQ, GuoD, WeiB, ZhangF, PangC, et al. (2013) The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell 25: 421–437.

68. ZhuJ, JeongJC, ZhuY, SokolchikI, MiyazakiS, et al. (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci U S A 105: 4945–4950.

69. AbeH, Yamaguchi-ShinozakiK, UraoT, IwasakiT, HosokawaD, et al. (1997) Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell 9: 1859–1868.

70. BoterM, Ruiz-RiveroO, AbdeenA, PratS (2004) Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev 18: 1577–1591.

71. Laurie-BerryN, JoardarV, StreetIH, KunkelBN (2006) The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Molecular Plant-Microbe Interactions 19: 789–800.

72. HongGJ, XueXY, MaoYB, WangLJ, ChenXY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635–2648.

73. ShojiT, HashimotoT (2011) Tobacco MYC2 regulates jasmonate-inducible nicotine biosynthesis genes directly and by way of the NIC2-locus ERF genes. Plant Cell Physiol 52: 1117–1130.

74. ZhangY, TurnerJG (2008) Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS One 3: e3699.

75. DombrechtB, XueGP, SpragueSJ, KirkegaardJA, RossJJ, et al. (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19: 2225–2245.

76. ZhaiQ, YanL, TanD, ChenR, SunJ, et al. (2013) Phosphorylation-Coupled Proteolysis of the Transcription Factor MYC2 Is Important for Jasmonate-Signaled Plant Immunity. PLoS Genet 9: e1003422.

77. XieDX, FeysBF, JamesS, Nieto-RostroM, TurnerJG (1998) COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280: 1091–1094.

78. HellensRP, AllanAC, FrielEN, BolithoK, GraftonK, et al. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 13.

79. YooSD, ChoYH, SheenJ (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565–1572.

80. SalehA, Alvarez-VenegasR, AvramovaZ (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3: 1018–1025.

81. KatagiriF, ThilmonyR, HeSY (2002) The Arabidopsis thaliana-pseudomonas syringae interaction. Arabidopsis Book 1: e0039.