Light affects tissue patterning of the hypocotyl in the shade-avoidance response

English version

Autoři: Esther Botterweg-Paredes ^aff001; Anko Blaakmeer ^aff001; Shin-Young Hong ^aff001; Bin Sun ^aff001; Lorenzo Mineri ^aff001; Valdeko Kruusvee ^aff001; Yakun Xie ^aff004; Daniel Straub ^aff005; Delphine Ménard ^aff007; Edouard Pesquet ^aff007; Stephan Wenkel ^aff001
Působiště autorů: Copenhagen Plant Science Centre, University of Copenhagen, Thorvaldsensvej, Denmark ^aff001; Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Copenhagen, Denmark ^aff002; NovoCrops Center, University of Copenhagen, Thorvaldsensvej, Denmark ^aff002; Department of Biosciences, University of Milan, Milan, Italy ^aff003; Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Copenhagen, Denmark ^aff003; Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Germany ^aff004; Department of Biosciences, University of Milan, Milan, Italy ^aff004; Quantitative Biology Center (QBiC), University of Tübingen, Auf der Morgenstelle, Tübingen, Germany ^aff005; Centre for Plant Molecular Biology (ZMBP), University of Tübingen, Germany ^aff005; Microbial Ecology, Center for Applied Geoscience, University of Tübingen, Tübingen, Germany ^aff006; Quantitative Biology Center (QBiC), University of Tübingen, Auf der Morgenstelle, Tuebingen, Germany ^aff006; Arrhenius Laboratories, Department of Ecology, Environment and Plant Sciences (DEEP), Stockholm University, Stockholm, Sweden ^aff007; Microbial Ecology, Center for Applied Geoscience, University of Tübingen, Tuebingen, Germany ^aff007; NovoCrops Center, University of Copenhagen, Thorvaldsensvej, Denmark ^aff008; Arrhenius Laboratories, Department of Ecology, Environment and Plant Sciences (DEEP), Stockholm University, Stockholm, Sweden ^aff008
Vyšlo v časopise: Light affects tissue patterning of the hypocotyl in the shade-avoidance response. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008678
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008678

Souhrn

Plants have evolved strategies to avoid shade and optimize the capture of sunlight. While some species are tolerant to shade, plants such as Arabidopsis thaliana are shade-intolerant and induce elongation of their hypocotyl to outcompete neighboring plants. We report the identification of a developmental module acting downstream of shade perception controlling vascular patterning. We show that Arabidopsis plants react to shade by increasing the number and types of water-conducting tracheary elements in the vascular cylinder to maintain vascular density constant. Mutations in genes affecting vascular patterning impair the production of additional xylem and also show defects in the shade-induced hypocotyl elongation response. Comparative analysis of the shade-induced transcriptomes revealed differences between wild type and vascular patterning mutants and it appears that the latter mutants fail to induce sets of genes encoding biosynthetic and cell wall modifying enzymes. Our results thus set the stage for a deeper understanding of how growth and patterning are coordinated in a dynamic environment.

Klíčová slova:

Arabidopsis thaliana – Auxins – Gene expression – Genetically modified plants – Hypocotyl – Seedlings – Transcription factors – White light

Zdroje

1. Roig-Villanova I, Bou-Torrent J, Galstyan A, Carretero-Paulet L, Portoles S, Rodriguez-Concepcion M, et al. Interaction of shade avoidance and auxin responses: a role for two novel atypical bHLH proteins. Embo j. 2007;26(22):4756–67. Epub 2007/10/20. doi: 10.1038/sj.emboj.7601890 17948056; PubMed Central PMCID: PMC2080812.

2. Sorin C, Salla-Martret M, Bou-Torrent J, Roig-Villanova I, Martinez-Garcia JF. ATHB4, a regulator of shade avoidance, modulates hormone response in Arabidopsis seedlings. Plant J. 2009;59(2):266–77. Epub 2009/04/28. doi: 10.1111/j.1365-313X.2009.03866.x 19392702.

3. Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erickson E, et al. Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell. 2012;24(4):1398–419. Epub 2012/04/21. doi: 10.1105/tpc.112.095711 22517317; PubMed Central PMCID: PMC3398554.

4. Hersch M, Lorrain S, de Wit M, Trevisan M, Ljung K, Bergmann S, et al. Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis. Proc Natl Acad Sci U S A. 2014;111(17):6515–20. Epub 2014/04/16. doi: 10.1073/pnas.1320355111 24733935; PubMed Central PMCID: PMC4035961.

5. Ni W, Xu SL, Tepperman JM, Stanley DJ, Maltby DA, Gross JD, et al. A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science. 2014;344(6188):1160–4. Epub 2014/06/07. doi: 10.1126/science.1250778 24904166; PubMed Central PMCID: PMC4414656.

6. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, Lopez-Vidriero I, et al. Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 2012;71(5):699–711. Epub 2012/04/28. doi: 10.1111/j.1365-313X.2012.05033.x 22536829.

7. Muller-Moule P, Nozue K, Pytlak ML, Palmer CM, Covington MF, Wallace AD, et al. YUCCA auxin biosynthetic genes are required for Arabidopsis shade avoidance. PeerJ. 2016;4:e2574. Epub 2016/10/21. doi: 10.7717/peerj.2574 27761349; PubMed Central PMCID: PMC5068344.

8. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, et al. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell. 2008;133(1):164–76. Epub 2008/04/09. doi: 10.1016/j.cell.2008.01.049 18394996; PubMed Central PMCID: PMC2442466.

9. Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, et al. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci U S A. 2011;108(45):18518–23. Epub 2011/10/26. doi: 10.1073/pnas.1108436108 22025721; PubMed Central PMCID: PMC3215067.

10. Ciarbelli AR, Ciolfi A, Salvucci S, Ruzza V, Possenti M, Carabelli M, et al. The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy. Plant Mol Biol. 2008;68(4–5):465–78. Epub 2008/09/02. doi: 10.1007/s11103-008-9383-8 18758690.

11. Devlin PF, Yanovsky MJ, Kay SA. A genomic analysis of the shade avoidance response in Arabidopsis. Plant Physiol. 2003;133(4):1617–29. Epub 2003/12/03. doi: 10.1104/pp.103.034397 14645734; PubMed Central PMCID: PMC300718.

12. Carabelli M, Sessa G, Baima S, Morelli G, Ruberti I. The Arabidopsis Athb-2 and -4 genes are strongly induced by far-red-rich light. Plant J. 1993;4(3):469–79. Epub 1993/09/01. doi: 10.1046/j.1365-313x.1993.04030469.x 8106086.

13. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C. Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 2008;53(2):312–23. Epub 2007/12/01. doi: 10.1111/j.1365-313X.2007.03341.x 18047474.

14. Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, et al. Linking photoreceptor excitation to changes in plant architecture. Genes & Development. 2012;26(8):785–90. doi: 10.1101/gad.187849.112 22508725

15. Causier B, Ashworth M, Guo W, Davies B. The TOPLESS Interactome: A Framework for Gene Repression in Arabidopsis. Plant Physiology. 2012;158(1):423–38. doi: 10.1104/pp.111.186999 22065421

16. Gallemi M, Molina-Contreras MJ, Paulisic S, Salla-Martret M, Sorin C, Godoy M, et al. A non-DNA-binding activity for the ATHB4 transcription factor in the control of vegetation proximity. New Phytol. 2017;216(3):798–813. Epub 2017/08/15. doi: 10.1111/nph.14727 28805249.

17. Procko C, Burko Y, Jaillais Y, Ljung K, Long JA, Chory J. The epidermis coordinates auxin-induced stem growth in response to shade. Genes Dev. 2016;30(13):1529–41. Epub 2016/07/13. doi: 10.1101/gad.283234.116 27401556; PubMed Central PMCID: PMC4949326.

18. Brandt R, Salla-Martret M, Bou-Torrent J, Musielak T, Stahl M, Lanz C, et al. Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. Plant J. 2012;72(1):31–42. Epub 2012/05/15. doi: 10.1111/j.1365-313X.2012.05049.x 22578006.

19. Merelo P, Xie Y, Brand L, Ott F, Weigel D, Bowman JL, et al. Genome-wide identification of KANADI1 target genes. PLoS One. 2013;8(10):e77341. Epub 2013/10/25. doi: 10.1371/journal.pone.0077341 24155946; PubMed Central PMCID: PMC3796457.

20. Xie Y, Straub D, Eguen T, Brandt R, Stahl M, Martinez-Garcia JF, et al. Meta-analysis of Arabidopsis KANADI1 direct target genes identifies basic growth-promoting module acting upstream of hormonal signaling pathways. Plant Physiol. 2015. Epub 2015/08/08. doi: 10.1104/pp.15.00764 26246448.

21. Bou-Torrent J, Salla-Martret M, Brandt R, Musielak T, Palauqui JC, Martinez-Garcia JF, et al. ATHB4 and HAT3, two class II HD-ZIP transcription factors, control leaf development in Arabidopsis. Plant Signal Behav. 2012;7(11):1382–7. Epub 2012/08/25. doi: 10.4161/psb.21824 22918502; PubMed Central PMCID: PMC3548853.

22. Turchi L, Baima S, Morelli G, Ruberti I. Interplay of HD-Zip II and III transcription factors in auxin-regulated plant development. J Exp Bot. 2015;66(16):5043–53. Epub 2015/04/26. doi: 10.1093/jxb/erv174 25911742.

23. Merelo P, Ram H, Pia Caggiano M, Ohno C, Ott F, Straub D, et al. Regulation of MIR165/166 by class II and class III homeodomain leucine zipper proteins establishes leaf polarity. Proceedings of the National Academy of Sciences. 2016;113(42):11973–8. doi: 10.1073/pnas.1516110113 27698117

24. Reinhart BJ, Liu T, Newell NR, Magnani E, Huang T, Kerstetter R, et al. Establishing a framework for the Ad/abaxial regulatory network of Arabidopsis: ascertaining targets of class III homeodomain leucine zipper and KANADI regulation. Plant Cell. 2013;25(9):3228–49. Epub 2013/10/01. doi: 10.1105/tpc.113.111518 24076978; PubMed Central PMCID: PMC3809529.

25. Huang T, Harrar Y, Lin C, Reinhart B, Newell NR, Talavera-Rauh F, et al. Arabidopsis KANADI1 acts as a transcriptional repressor by interacting with a specific cis-element and regulates auxin biosynthesis, transport, and signaling in opposition to HD-ZIPIII factors. Plant Cell. 2014;26(1):246–62. Epub 2014/01/28. doi: 10.1105/tpc.113.111526 24464295; PubMed Central PMCID: PMC3963573.

26. Dolzblasz A, Nardmann J, Clerici E, Causier B, van der Graaff E, Chen J, et al. Stem Cell Regulation by Arabidopsis WOX Genes. Mol Plant. 2016;9(7):1028–39. Epub 2016/04/26. doi: 10.1016/j.molp.2016.04.007 27109605.

27. Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ. WOX4 promotes procambial development. Plant Physiol. 2010;152(3):1346–56. Epub 2010/01/02. doi: 10.1104/pp.109.149641 20044450; PubMed Central PMCID: PMC2832261.

28. Suer S, Agusti J, Sanchez P, Schwarz M, Greb T. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell. 2011;23(9):3247–59. Epub 2011/09/20. doi: 10.1105/tpc.111.087874 21926336; PubMed Central PMCID: PMC3203433.

29. Kucukoglu M, Nilsson J, Zheng B, Chaabouni S, Nilsson O. WUSCHEL-RELATED HOMEOBOX4 (WOX4)-like genes regulate cambial cell division activity and secondary growth in Populus trees. New Phytol. 2017;215(2):642–57. Epub 2017/06/14. doi: 10.1111/nph.14631 28609015.

30. Baima S, Forte V, Possenti M, Penalosa A, Leoni G, Salvi S, et al. Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol Plant. 2014;7(6):1006–25. Epub 2014/04/30. doi: 10.1093/mp/ssu051 24777988.

31. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Dolezal K, et al. TAA1-Mediated Auxin Biosynthesis Is Essential for Hormone Crosstalk and Plant Development. Cell. 2008;133(1):177–91. doi: 10.1016/j.cell.2008.01.047 18394997

32. Yamada M, Greenham K, Prigge MJ, Jensen PJ, Estelle M. The TRANSPORT INHIBITOR RESPONSE2 Gene Is Required for Auxin Synthesis and Diverse Aspects of Plant Development. Plant Physiol. 2009;151(1):168–79. doi: 10.1104/pp.109.138859 19625638

33. Zhong RQ, Ye ZH. amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels. Plant and Cell Physiology. 2004;45(4):369–85. WOS:000221037200002. doi: 10.1093/pcp/pch051 15111711

34. Zhong RQ, Ye ZH. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell. 1999;11(11):2139–52. WOS:000083980500009. doi: 10.1105/tpc.11.11.2139 10559440

35. Zhong R, Ye ZH. IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. Plant Cell. 1999;11(11):2139–52. Epub 1999/11/24. doi: 10.1105/tpc.11.11.2139 10559440; PubMed Central PMCID: PMC144121.

36. Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL, et al. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development. 2010;137(6):975–84. Epub 2010/02/25. doi: 10.1242/dev.047662 20179097.

37. Endo S, Pesquet E, Yamaguchi M, Tashiro G, Sato M, Toyooka K, et al. Identifying new components participating in the secondary cell wall formation of vessel elements in zinnia and Arabidopsis. Plant Cell. 2009;21(4):1155–65. Epub 2009/04/23. doi: 10.1105/tpc.108.059154 19383897; PubMed Central PMCID: PMC2685625.

38. Menard D, Serk H, Decou R, Pesquet E. Establishment and Utilization of Habituated Cell Suspension Cultures for Hormone-Inducible Xylogenesis. Methods Mol Biol. 2017;1544 : 37–57. Epub 2017/01/05. doi: 10.1007/978-1-4939-6722-3_4 28050827.

39. Derbyshire P, Menard D, Green P, Saalbach G, Buschmann H, Lloyd CW, et al. Proteomic Analysis of Microtubule Interacting Proteins over the Course of Xylem Tracheary Element Formation in Arabidopsis. Plant Cell. 2015;27(10):2709–26. Epub 2015/10/04. doi: 10.1105/tpc.15.00314 26432860; PubMed Central PMCID: PMC4682315.

40. Xie Y, Straub D, Eguen T, Brandt R, Stahl M, Martínez-García JF, et al. Meta-Analysis of Arabidopsis KANADI1 Direct Target Genes Identifies a Basic Growth-Promoting Module Acting Upstream of Hormonal Signaling Pathways. Plant Physiology. 2015;169 : 1240–53. doi: 10.1104/pp.15.00764 26246448

41. Ballare CL, Scopel AL, Sanchez RA. On the opportunity cost of the photosynthate invested in stem elongation reactions mediated by phytochrome. Oecologia. 1991;86(4):561–7. Epub 1991/05/01. doi: 10.1007/BF00318323 28313338.

42. Otsuga D, DeGuzman B, Prigge MJ, Drews GN, Clark SE. REVOLUTA regulates meristem initiation at lateral positions. The Plant Journal. 2001;25(2):223–36. WOS:000166980400010. doi: 10.1046/j.1365-313x.2001.00959.x 11169198

43. Laux T, Mayer KF, Berger J, Jurgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122(1):87–96. Epub 1996/01/01. 8565856.

44. Kim H-S, Kim SJ, Abbasi N, Bressan RA, Yun D-J, Yoo S-D, et al. The DOF transcription factor Dof5.1 influences leaf axial patterning by promoting Revoluta transcription in Arabidopsis. The Plant Journal. 2010;64(3):524–35. doi: 10.1111/j.1365-313X.2010.04346.x 20807212

45. Wenkel S, Emery J, Hou B-H, Evans MMS, Barton MK. A Feedback Regulatory Module Formed by LITTLE ZIPPER and HD-ZIPIII Genes. Plant Cell. 2007;19(11):3379–90. doi: 10.1105/tpc.107.055772 18055602

46. Pesquet E, Korolev AV, Calder G, Lloyd CW. The microtubule-associated protein AtMAP70-5 regulates secondary wall patterning in Arabidopsis wood cells. Curr Biol. 2010;20(8):744–9. Epub 2010/04/20. doi: 10.1016/j.cub.2010.02.057 20399097.

47. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, et al. Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol. 2010;Chapter 19:Unit 19.0.1–21. Epub 2010/01/14. doi: 10.1002/0471142727.mb1910s89 20069535; PubMed Central PMCID: PMC4264107.

48. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, et al. Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 2005;15(10):1451–5. Epub 2005/09/20. doi: 10.1101/gr.4086505 16169926; PubMed Central PMCID: PMC1240089.

49. Goecks J, Nekrutenko A, Taylor J. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol. 2010;11(8):R86. Epub 2010/08/27. doi: 10.1186/gb-2010-11-8-r86 20738864; PubMed Central PMCID: PMC2945788.

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