Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth

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The study of plant development is generally carried out in the absence of physical injury. However, damage to plant organs through biotic and abiotic insult is common in nature. Under these conditions the jasmonate pathway that has a low activity in unstressed vegetative tissues imposes its activity on cell division and elongation. Such jasmonate-dependent growth restriction can strongly impact plant productivity. Taking roots as a model, we show that it is possible to manipulate regulatory layers in jasmonate signalling such that cell division and cell elongation can be constrained differently. This approach may lead to future strategies to alter organ growth. Moreover, during this study we identified a novel mutant in a key regulator of the jasmonate pathway. This mutant generated a positive regulator of jasmonate signalling that was so active that we were able to show that hormone synthesis can be completely uncoupled from hormone responses, suggesting ways to modify traits of potential agronomic importance.

Vyšlo v časopise: Multilayered Organization of Jasmonate Signalling in the Regulation of Root Growth. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005300
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005300

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1. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T. Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia. 2003;135(4):601–5. Epub 2005/10/18. doi: 10.1007/s00442-003-1228-1 16228257.

2. Yan Y, Stolz S, Chetelat A, Reymond P, Pagni M, Dubugnon L, et al. A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell. 2007;19(8):2470–83. Epub 2007/08/07. doi: 10.1105/tpc.107.050708 17675405; PubMed Central PMCID: PMC2002611.

3. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, et al. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(19):E1192–200. Epub 2012/04/25. doi: 10.1073/pnas.1201616109 22529386; PubMed Central PMCID: PMC3358897.

4. Zhang Y, Turner JG. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PloS one. 2008;3(11):e3699. Epub 2008/11/13. doi: 10.1371/journal.pone.0003699 19002244; PubMed Central PMCID: PMC2577035.

5. Browse J. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu Rev Plant Biol. 2009;60:183–205. Epub 2008/11/26. doi: 10.1146/annurev.arplant.043008.092007 19025383.

6. 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(6):1021–58. Epub 2013/04/06. doi: 10.1093/aob/mct067 23558912; PubMed Central PMCID: PMC3662512.

7. Acosta IF, Gasperini D, Chetelat A, Stolz S, Santuari L, Farmer EE. Role of NINJA in root jasmonate signaling. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(38):15473–8. Epub 2013/09/05. doi: 10.1073/pnas.1307910110 24003128; PubMed Central PMCID: PMC3780868.

8. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, et al. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol. 2009;5(5):344–50. Epub 2009/04/08. doi: 10.1038/nchembio.161 19349968.

9. Staswick PE, Tiryaki I. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell. 2004;16(8):2117–27. Epub 2004/07/20. doi: 10.1105/tpc.104.023549 15258265; PubMed Central PMCID: PMC519202.

10. Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Perez AC, et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature. 2010;464(7289):788–91. Epub 2010/04/03. doi: 10.1038/nature08854 20360743; PubMed Central PMCID: PMC2849182.

11. Shyu C, Figueroa P, Depew CL, Cooke TF, Sheard LB, Moreno JE, et al. JAZ8 lacks a canonical degron and has an EAR motif that mediates transcriptional repression of jasmonate responses in Arabidopsis. Plant Cell. 2012;24(2):536–50. Epub 2012/02/14. doi: 10.1105/tpc.111.093005 22327740; PubMed Central PMCID: PMC3315231.

12. Wang L, Kim J, Somers DE. Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(2):761–6. Epub 2012/12/26. doi: 10.1073/pnas.1215010110 23267111; PubMed Central PMCID: PMC3545823.

13. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature. 2007;448(7154):666–71. Epub 2007/07/20. doi: 10.1038/nature06006 17637675.

14. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature. 2007;448(7154):661–5. Epub 2007/07/20. doi: 10.1038/nature05960 17637677.

15. Cevik V, Kidd BN, Zhang P, Hill C, Kiddle S, Denby KJ, et al. MEDIATOR25 acts as an integrative hub for the regulation of jasmonate-responsive gene expression in Arabidopsis. Plant Physiol. 2012;160(1):541–55. Epub 2012/07/24. doi: 10.1104/pp.112.202697 22822211; PubMed Central PMCID: PMC3440227.

16. Chen R, Jiang H, Li L, Zhai Q, Qi L, Zhou W, et al. The Arabidopsis mediator subunit MED25 differentially regulates jasmonate and abscisic acid signaling through interacting with the MYC2 and ABI5 transcription factors. Plant Cell. 2012;24(7):2898–916. Epub 2012/07/24. doi: 10.1105/tpc.112.098277 22822206; PubMed Central PMCID: PMC3426122.

17. Kazan K, Manners JM. MYC2: the master in action. Molecular plant. 2013;6(3):686–703. Epub 2012/11/13. doi: 10.1093/mp/sss128 23142764.

18. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, et al. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell. 2007;19(7):2225–45. Epub 2007/07/10. doi: 10.1105/tpc.106.048017 17616737; PubMed Central PMCID: PMC1955694.

19. Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, et al. 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(2):701–15. Epub 2011/02/22. doi: 10.1105/tpc.110.080788 21335373; PubMed Central PMCID: PMC3077776.

20. Niu Y, Figueroa P, Browse J. Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot. 2011;62(6):2143–54. Epub 2011/02/16. doi: 10.1093/jxb/erq408 21321051; PubMed Central PMCID: PMC3060693.

21. Browse J. The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry. 2009;70(13–14):1539–46. Epub 2009/09/11. doi: 10.1016/j.phytochem.2009.08.004 19740496.

22. Feys B, 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(5):751–9. Epub 1994/05/01. doi: 10.1105/tpc.6.5.751 12244256; PubMed Central PMCID: PMC160473.

23. 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(7):1938–50. Epub 2004/06/23. doi: 10.1105/tpc.022319 15208388; PubMed Central PMCID: PMC514172.

24. Staswick PE, Su W, Howell SH. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proceedings of the National Academy of Sciences of the United States of America. 1992;89(15):6837–40. Epub 1992/08/01. 11607311; PubMed Central PMCID: PMC49599.

25. Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, et al. 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. 2011;23(9):3335–52. Epub 2011/09/29. doi: 10.1105/tpc.111.089870 21954460; PubMed Central PMCID: PMC3203420.

26. Larrieu A, Champion A, Legrand J, Lavenus J, Mast D, Brunoud G, et al. A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants. Nature communications. 2015;6:6043. Epub 2015/01/17. doi: 10.1038/ncomms7043 25592181.

27. Fuerst RA, Soni R, Murray JA, Lindsey K. Modulation of cyclin transcript levels in cultured cells of Arabidopsis thaliana. Plant Physiol. 1996;112(3):1023–33. Epub 1996/11/01. 8938409; PubMed Central PMCID: PMC158029.

28. Egelkrout EM, Mariconti L, Settlage SB, Cella R, Robertson D, Hanley-Bowdoin L. Two E2F elements regulate the proliferating cell nuclear antigen promoter differently during leaf development. Plant Cell. 2002;14(12):3225–36. Epub 2002/12/07. 12468739; PubMed Central PMCID: PMC151214.

29. Smolen GA, Pawlowski L, Wilensky SE, Bender J. Dominant alleles of the basic helix-loop-helix transcription factor ATR2 activate stress-responsive genes in Arabidopsis. Genetics. 2002;161(3):1235–46. Epub 2002/07/24. 12136026; PubMed Central PMCID: PMC1462177.

30. Goossens J, Swinnen G, Vanden Bossche R, Pauwels L, Goossens A. Change of a conserved amino acid in the MYC2 and MYC3 transcription factors leads to release of JAZ repression and increased activity. New Phytol. 2015. doi: 10.1111/nph.13398

31. Zhai Q, Yan L, Tan D, Chen R, Sun J, Gao L, et al. Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLoS Genet. 2013;9(4):e1003422. Epub 2013/04/18. doi: 10.1371/journal.pgen.1003422 23593022; PubMed Central PMCID: PMC3616909.

32. Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, et al. A regulatory network for coordinated flower maturation. PLoS Genet. 2012;8(2):e1002506. Epub 2012/02/22. doi: 10.1371/journal.pgen.1002506 22346763; PubMed Central PMCID: PMC3276552.

33. Schmidt L, Hummel GM, Schottner M, Schurr U, Walter A. Jasmonic acid does not mediate root growth responses to wounding in Arabidopsis thaliana. Plant, cell & environment. 2010;33(1):104–16. Epub 2009/11/10. doi: 10.1111/j.1365-3040.2009.02062.x 19895400.

34. Hummel GM, Naumann M, Schurr U, Walter A. Root growth dynamics of Nicotiana attenuata seedlings are affected by simulated herbivore attack. Plant, cell & environment. 2007;30(10):1326–36. Epub 2007/08/31. doi: 10.1111/j.1365-3040.2007.01718.x 17727422.

35. Noir S, Bomer M, Takahashi N, Ishida T, Tsui TL, Balbi V, et al. Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol. 2013;161(4):1930–51. Epub 2013/02/27. doi: 10.1104/pp.113.214908 23439917; PubMed Central PMCID: PMC3613466.

36. Zhu Z, An F, Feng Y, Li P, Xue L, A M, et al. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 2011;108(30):12539–44. Epub 2011/07/09. doi: 10.1073/pnas.1103959108 21737749; PubMed Central PMCID: PMC3145709.

37. Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, et al. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 2007;19(7):2197–212. Epub 2007/07/17. doi: 10.1105/tpc.107.052126 17630274; PubMed Central PMCID: PMC1955700.

38. Stepanova AN, Yun J, Likhacheva AV, Alonso JM. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 2007;19(7):2169–85. Epub 2007/07/17. doi: 10.1105/tpc.107.052068 17630276; PubMed Central PMCID: PMC1955696.

39. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, et al. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 2007;19(7):2186–96. Epub 2007/07/17. doi: 10.1105/tpc.107.052100 17630275; PubMed Central PMCID: PMC1955695.

40. Zhong GY, Burns JK. Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol. 2003;53(1–2):117–31. Epub 2004/02/06. 14756311.

41. Bhosale R, Jewell JB, Hollunder J, Koo AJ, Vuylsteke M, Michoel T, et al. Predicting gene function from uncontrolled expression variation among individual wild-type Arabidopsis plants. Plant Cell. 2013;25(8):2865–77. Epub 2013/08/15. doi: 10.1105/tpc.113.112268 23943861; PubMed Central PMCID: PMC3784585.

42. Widemann E, Miesch L, Lugan R, Holder E, Heinrich C, Aubert Y, et al. The amidohydrolases IAR3 and ILL6 contribute to jasmonoyl-isoleucine hormone turnover and generate 12-hydroxyjasmonic acid upon wounding in Arabidopsis leaves. J Biol Chem. 2013;288(44):31701–14. Epub 2013/09/21. doi: 10.1074/jbc.M113.499228 24052260; PubMed Central PMCID: PMC3814765.

43. Pauwels L, Goossens A. The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell. 2011;23(9):3089–100. Epub 2011/10/04. doi: 10.1105/tpc.111.089300 21963667; PubMed Central PMCID: PMC3203442.

44. Chini A, Fonseca S, Chico JM, Fernandez-Calvo P, Solano R. The ZIM domain mediates homo- and heteromeric interactions between Arabidopsis JAZ proteins. Plant J. 2009;59(1):77–87. Epub 2009/03/25. doi: 10.1111/j.1365-313X.2009.03852.x 19309455.

45. Chung HS, Howe GA. A critical role for the TIFY motif in repression of jasmonate signaling by a stabilized splice variant of the JASMONATE ZIM-domain protein JAZ10 in Arabidopsis. Plant Cell. 2009;21(1):131–45. Epub 2009/01/20. doi: 10.1105/tpc.108.064097 19151223; PubMed Central PMCID: PMC2648087.

46. Chico JM, Fernandez-Barbero G, Chini A, Fernandez-Calvo P, Diez-Diaz M, Solano R. Repression of Jasmonate-Dependent Defenses by Shade Involves Differential Regulation of Protein Stability of MYC Transcription Factors and Their JAZ Repressors in Arabidopsis. Plant Cell. 2014;26(5):1967–80. Epub 2014/05/16. doi: 10.1105/tpc.114.125047 24824488; PubMed Central PMCID: PMC4079362.

47. Farmer EE, Gasperini D, Acosta IF. The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol. 2014;204(2):282–8. Epub 2014/12/03. doi: 10.1111/nph.12897 25453132.

48. Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R. 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. 2002;31(1):1–12. Epub 2002/07/09. 12100478.

49. Gfeller A, Baerenfaller K, Loscos J, Chetelat A, Baginsky S, Farmer EE. Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. Plant Physiol. 2011;156(4):1797–807. Epub 2011/06/23. doi: 10.1104/pp.111.181008 21693672; PubMed Central PMCID: PMC3149931.

50. Chauvin A, Caldelari D, Wolfender JL, Farmer EE. Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol. 2013;197(2):566–75. Epub 2012/11/23. doi: 10.1111/nph.12029 23171345.

51. Schweizer F, Fernandez-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, et al. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell. 2013;25(8):3117–32. Epub 2013/08/15. doi: 10.1105/tpc.113.115139 23943862; PubMed Central PMCID: PMC3784603.

52. Glauser G, Dubugnon L, Mousavi SA, Rudaz S, Wolfender JL, Farmer EE. Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J Biol Chem. 2009;284(50):34506–13. Epub 2009/10/23. doi: 10.1074/jbc.M109.061432 19846562; PubMed Central PMCID: PMC2787311.

53. Mousavi SA, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature. 2013;500(7463):422–6. Epub 2013/08/24. doi: 10.1038/nature12478 23969459.

54. Wu Z, Irizarry R, Gentleman R, Murillo FM, Spencer F. A Model-Based Background Adjustment for Oligonucleotide Expression Arrays. Journal of the American Statistical Association. 2004;99:909–17.

55. Smyth GK. Limma: linear models for microarray data. In Gentleman R, Carey V, Dudoit S, Irizarry R and Huber W, editors. Bioinformatics and Computational Biology Solutions Using R and Bioconductor: Springer, New York; 2005, pp. 397–420.

56. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B. 1995;57:289–300.

57. De Sutter V, Vanderhaeghen R, Tilleman S, Lammertyn F, Vanhoutte I, Karimi M, et al. Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J. 2005;44(6):1065–76. Epub 2005/12/20. doi: 10.1111/j.1365-313X.2005.02586.x 16359398.

58. Vanden Bossche R, Demedts B, Vanderhaeghen R, Goossens A. Transient expression assays in tobacco protoplasts. Methods in molecular biology (Clifton, NJ). 2013;1011:227–39. Epub 2013/04/26. doi: 10.1007/978-1-62703-414-2_18 23616000.

59. Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W, et al. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(4):1380–5. Epub 2008/01/25. doi: 10.1073/pnas.0711203105 18216250; PubMed Central PMCID: PMC2234147.

60. Cuellar Perez A, Nagels Durand A, Vanden Bossche R, De Clercq R, Persiau G, Van Wees SC, et al. The non-JAZ TIFY protein TIFY8 from Arabidopsis thaliana is a transcriptional repressor. PloS one. 2014;9(1):e84891. Epub 2014/01/15. doi: 10.1371/journal.pone.0084891 24416306; PubMed Central PMCID: PMC3885651.

61. James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 1996;144(4):1425–36. Epub 1996/12/01. 8978031; PubMed Central PMCID: PMC1207695.