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Science China Life Sciences

, Volume 57, Issue 1, pp 145–154 | Cite as

Amino acid substitutions of GLY98, LEU245 and GLU543 in COI1 distinctively affect jasmonate-regulated male fertility in Arabidopsis

  • Huang Huang
  • CuiLi Wang
  • HaiXia Tian
  • Yu Sun
  • DaoXin XieEmail author
  • SuSheng SongEmail author
Open Access
Research Paper Tsinghua Special Issue

Abstract

Jasmonate (JA) regulates various plant defense and developmental processes. The F-box protein CORONATINE INSENSITIVE 1 (COI1) perceives JA signals to mediate diverse plant responses including male fertility, root growth, anthocyanin accumulation, and defense against abiotic and biotic stresses. In this study, we carried out genetic, physiological and biochemical analysis on a series of coi1 mutant alleles, and found that different amino acid mutations in COI1 distinctively affect JA-regulated male fertility in Arabidopsis. All the JA responses are disrupted by the COI1 mutations W467* in coi1-1, Q343* (coi1-6), G369E (coi1-4), G98D (coi1-5), G155E (coi1-7), D452A (coi1-9) and L490A (coi1-10), though the coi1-5 mutant (COI1G98D) contains adequate COI1 protein (∼60% of wild-type). Interestingly, the low basal level of COI1E543K in the coi1-8 mutant (∼10% of wild-type COI1 level) is sufficient for maintaining male fertility (∼50% of wild-type fertility); the coi1-2 mutant with low level of COI1L245F (∼10% of wild-type) is male sterile under normal growth condition (22°C) but male fertile (∼80% of wild-type fertility) at low temperature (16°C); however, both coi1-2 and coi1-8 are defective in the other JA responses (root growth, anthocyanin accumulation, and plant response to the pathogen Pst DC3000 infection).

Keywords

COI1 coi1-2 coi1-5 coi1-8 jasmonate male fertility 

References

  1. 1.
    Browse J. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol, 2009, 60:183–205PubMedCrossRefGoogle Scholar
  2. 2.
    Wasternack C, Hause B. 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, 2013, 111:1021–1058PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D. 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, 2011, 23:1000–1013PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    McConn M, Browse J. The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell, 1996, 8:403–416PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Song S, Qi T, Huang H, Xie D. Regulation of stamen development by coordinated actions of jasmonate, auxin and gibberellin in Arabidopsis. Mol Plant, 2013, 6:1065–1073PubMedCrossRefGoogle Scholar
  6. 6.
    Staswick PE, Su WP, Howell SH. Methyl jasmonate inhibition of root-growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA, 1992, 89:6837–6840PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Feys BJF, Benedetti CE, Penfold CN, Turner JG. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male-sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell, 1994, 6:751–759PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Qi T, Song S, Ren Q, Wu D, Huang H, Chen Y, Fan M, Peng W, Ren C, Xie D. 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, 2011, 23:1795–1814PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K. Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development, 2009, 136:1039–1048PubMedCrossRefGoogle Scholar
  10. 10.
    Ueda J, Kato J. Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absinthium L.). Plant Physiol, 1980, 66:246–249PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Shan X, Wang J, Chua L, Jiang D, Peng W, Xie D. A role of Arabidopsis rubisco activase in jasmonate-induced leaf senescence. Plant Physiol, 2011, 155:751–764PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    De Geyter N, Gholami A, Goormachtig S, Goossens A. Transcriptional machineries in jasmonate-elicited plant secondary metabolism. Trends Plant Sci, 2012, 17:349–359PubMedCrossRefGoogle Scholar
  13. 13.
    Schweizer F, Fernandez-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell, 2013, 25:3117–3132PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell, 2012, 24:2635–2648PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Rao MV, Lee H, Creelman RA, Mullet JE, Davis KR. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell, 2000, 12:1633–1646PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J, 2011, 65:907–921PubMedCrossRefGoogle Scholar
  17. 17.
    Robson F, Okamoto H, Patrick E, Harris SR, Wasternack C, Brearley C, Turner JG. Jasmonate and phytochrome A signaling in Arabidopsis wound and shade responses are integrated through JAZ1 stability. Plant Cell, 2010, 22:1143–1160PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Howe GA, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol, 2008, 59:41–66PubMedCrossRefGoogle Scholar
  19. 19.
    McConn M, Creelman RA, Bell E, Mullet JE, Browse J. Jasmonate is essential for insect defense in Arabidopsis. Proc Natl Acad Sci USA, 1997, 94:5473–5477PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA. 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, 2004, 16:126–143PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell, 2004, 16:1938–1950PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Thaler JS, Humphrey PT, Whiteman NK. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci, 2012, 17:260–270PubMedCrossRefGoogle Scholar
  23. 23.
    Vijayan P, Shockey J, Levesque CA, Cook RJ, Browse J. A role for jasmonate in pathogen defense of Arabidopsis. Proc Natl Acad Sci USA, 1998, 95:7209–7214PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Hu P, Zhou W, Cheng Z, Fan M, Wang L, Xie D. JAV1 controls jasmonate-regulated plant defense. Mol Cell, 2013, 50:504–515PubMedCrossRefGoogle Scholar
  25. 25.
    Robert-Seilaniantz A, Grant M, Jones JD. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol, 2011, 49:317–343PubMedCrossRefGoogle Scholar
  26. 26.
    Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science, 1998, 280:1091–1094PubMedCrossRefGoogle Scholar
  27. 27.
    Ren CM, Pan JW, Peng W, Genschik P, Hobbie L, Hellmann H, Estelle M, Gao B, Peng JR, Sun CQ, Xie DX. Point mutations in Arabidopsis Cullin1 reveal its essential role in jasmonate response. Plant J, 2005, 42:514–524PubMedCrossRefGoogle Scholar
  28. 28.
    Xu LH, Liu FQ, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang DF, Xie DX. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell, 2002, 14:1919–1935PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Yan J, Li H, Li S, Yao R, Deng H, Xie Q, Xie D. The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26s proteasome pathway. Plant Cell, 2013, 25:486–498PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Yan J, Zhang C, Gu M, Bai Z, Zhang W, Qi T, Cheng Z, Peng W, Luo H, Nan F, Wang Z, Xie D. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell, 2009, 21:2220–2236PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R. The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 2007, 448:666–671PubMedCrossRefGoogle Scholar
  32. 32.
    Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature, 2007, 448:661–665PubMedCrossRefGoogle Scholar
  33. 33.
    Yan YX, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, Farmer EE. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell, 2007, 19:2470–2483PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature, 2010, 468:400–405PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R. (+)-7-iso-jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol, 2009, 5:344–350PubMedCrossRefGoogle Scholar
  36. 36.
    Niu Y, Figueroa P, Browse J. Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot, 2011, 62:2143–2154PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R. 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, 2011, 23:701–715PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Cheng Z, Sun L, Qi T, Zhang B, Peng W, Liu Y, Xie D. The bHLH transcription factor MYC3 interacts with the Jasmonate ZIM-domain proteins to mediate jasmonate response in Arabidopsis. Mol Plant, 2011, 4:279–288PubMedCrossRefGoogle Scholar
  39. 39.
    Zhu Z, An F, Feng Y, Li P, Xue L, Mu A, Jiang Z, Kim JM, To TK, Li W, Zhang X, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo H. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA, 2011, 108:12539–12544PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, Wu D, Guo H, Xie D. The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genet, 2013, 9:e1003653PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, Ohta H, Shirasu K. Basic helix-loop-helix transcription factors jasmonate-associated MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol, 2013, 163:291–304PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Nakata M, Mitsuda N, Herde M, Koo AJ, Moreno JE, Suzuki K, Howe GA, Ohme-Takagi M. 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, 2013, 25:1641–1656PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell, 1990, 2:755–767PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Katagiri F, Thilmony R, He SY. The Arabidopsis thaliana-pseudomonas syringae interaction. Arabidopsis Book, 2002, 1:e0039PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Ellis C, Turner JG. A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta, 2002, 215:549–556PubMedCrossRefGoogle Scholar
  46. 46.
    Westphal L, Scheel D, Rosahl S. The coi1-16 mutant harbors a second site mutation rendering PEN2 nonfunctional. Plant Cell, 2008, 20:824–826PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, Lee CM, Thomashow MF, Yang Y, He Z, He SY. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci USA, 2012, 109:E1192–1200PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Mandaokar A, Thines B, Shin B, Lange BM, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G, Browse J. Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J, 2006, 46:984–1008PubMedCrossRefGoogle Scholar
  49. 49.
    Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J. Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet, 2009, 5:e1000440PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© The Author(s) 2014

Authors and Affiliations

  1. 1.Tsinghua-Peking Center for Life Sciences, MOE Key Laboratory of Bioinformatics, School of Life SciencesTsinghua UniversityBeijingChina

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