Evolution of the Auxin Response Factors from charophyte ancestors

English version

Autoři: Raquel Martin-Arevalillo ^aff001; Emmanuel Thévenon ^aff002; Fanny Jégu ^aff002; Thomas Vinos-Poyo ^aff002; Teva Vernoux ^aff001; François Parcy ^aff002; Renaud Dumas ^aff002
Působiště autorů: Laboratoire de Reproduction et Développement des Plantes, Univ. Lyon, ENS de Lyon, UCB Lyon1, CNRS, INRA, Lyon, France ^aff001; Univ. Grenoble Alpes, CNRS, CEA, INRA, IRIG-DBSCI-LPCV, Grenoble, France ^aff002
Vyšlo v časopise: Evolution of the Auxin Response Factors from charophyte ancestors. PLoS Genet 15(9): e1008400. doi:10.1371/journal.pgen.1008400
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008400

Souhrn

Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most ‘ancient’ ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares many features with modern ARFs: it is capable of oligomerization, interacts with the TOPLESS co-repressor and specifically binds Auxin Response Elements as dimer. In addition, CaARF possesses a DNA-binding specificity that differs from class A and B ARFs and that was maintained in class C ARF along plants evolution. Phylogenetic evidence together with CaARF biochemical properties indicate that the different classes of ARFs likely arose from an ancestral proto-ARF protein with class C-like features. The foundation of auxin signalling would have thus happened from a pre-existing hormone-independent transcriptional regulation together with the emergence of a functional hormone perception complex.

Klíčová slova:

Algae – Arabidopsis thaliana – DNA-binding proteins – Sequence alignment – Sequence databases – Sequence motif analysis – Auxins – Plant evolution

Zdroje

1. Finet C, Berne-Dedieu A, Scutt CP, Marletaz F. Evolution of the ARF gene family in land plants: Old domains, new tricks. Molecular Biology and Evolution. 2013;30 : 45–56. doi: 10.1093/molbev/mss220 22977118

2. Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, et al. Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. Cell. 2017 Oct;171(2):287–304.e15. doi: 10.1016/j.cell.2017.09.030 28985561

3. Delwiche CF, Cooper ED. The evolutionary origin of a terrestrial flora. Current Biology. 2015;25(19):R899–910. doi: 10.1016/j.cub.2015.08.029 26439353

4. Domozych DS, Popper ZA, Sørensen I. Charophytes: Evolutionary Giants and Emerging Model Organisms. Frontiers in plant science. 2016;7(October):1470. doi: 10.3389/fpls.2016.01470 27777578

5. Finet C, Timme RE, Delwiche CF, Marlétaz F. Multigene Phylogeny of the Green Lineage Reveals the Origin and Diversification of Land Plants. Current Biology. 2010 Dec;20(24):2217–22. doi: 10.1016/j.cub.2010.11.035 21145743

6. Vries J De Archibald JM. Plant evolution: landmarks on the path to terrestrial life. New Phytologist. 2018;217(4):1428–34. doi: 10.1111/nph.14975 29318635

7. Lemieux C, Otis C, Turmel M. A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biology [Internet]. 2007 Dec [cited 2019 Jun 3];5(1). Available from: https://bmcbiol.biomedcentral.com/articles/10.1186/1741-7007-5-2

8. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nature Communications [Internet]. 2014 Dec [cited 2018 Nov 21];5(1). Available from: http://www.nature.com/articles/ncomms4978

9. Domozych DS, Domozych CE. Multicellularity in green algae: upsizing in a walled complex. Frontiers in Plant Science. 2014;5(649):1–8.

10. Umen JG. Green Algae and the Origins of Multicellularity in the Plant Kingdom. Cold Spring Harbor Perspectives in Biology. 2014;6(11):1–27.

11. Timme RE, Bachvaroff TR, Delwiche CF. Broad Phylogenomic Sampling and the Sister Lineage of Land Plants. Joly S, editor. PLoS ONE. 2012 Jan 13;7(1):e29696. doi: 10.1371/journal.pone.0029696 22253761

12. Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS. 2014;111(45):4859–68.

13. Lavy M, Estelle M. Mechanisms of auxin signaling. Development. 2016;143 : 3226–9. doi: 10.1242/dev.131870 27624827

14. Leyser O. Auxin Signaling. Plant Physiology. 2018;176(1):465–79. doi: 10.1104/pp.17.00765 28818861

15. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM. Isolation of the Arabidopsis ABI3 Gene by Positional Cloning. THE PLANT CELL ONLINE. 1992 Oct 1;4(10):1251–61.

16. Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S. DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends in Plant Science. 2013;18(5):267–76. doi: 10.1016/j.tplants.2012.09.001 23040085

17. Galli M, Khakhar A, Lu Z, Chen Z, Sen S, Joshi T, et al. The DNA binding landscape of the maize AUXIN RESPONSE FACTOR family. Nature Communications. 2018 Oct 30;9(1):4526. doi: 10.1038/s41467-018-06977-6 30375394

18. O’Malley RC, Huang SC, Song L, Lewsey MG, Bartlett A, Nery JR, et al. Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape. Cell. 2016 May;165(5):1280–92. doi: 10.1016/j.cell.2016.04.038 27203113

19. Stigliani A, Martin-Arevalillo R, Lucas J, Bessy A, Vinos-Poyo T, Mironova V, et al. Capturing Auxin Response Factors Syntax Using DNA Binding Models. Molecular Plant. 2019 Jun;12(6):822–32. doi: 10.1016/j.molp.2018.09.010 30336329

20. Mutte SK, Kato H, Rothfels C, Melkonian M, Wong GK, Weijers D. Origin and evolution of the nuclear auxin response system. eLife. 2018;March 27(7):1–25.

21. Wang C, Liu Y, Li S-S, Han G-Z. Insights into the Origin and Evolution of the Plant Hormone Signaling Machinery. Plant Physiology. 2015;167(3):872–86. doi: 10.1104/pp.114.247403 25560880

22. Guilfoyle TJ. The PB1 Domain in Auxin Response Factor and Aux/IAA Proteins: A Versatile Protein Interaction Module in the Auxin Response. The Plant Cell. 2015;27 : 33–43. doi: 10.1105/tpc.114.132753 25604444

23. Nanao MH, Vinos-Poyo T, Brunoud G, Thévenon E, Mazzoleni M, Mast D, et al. Structural basis for oligomerization of auxin transcriptional regulators. Nature communications. 2014;5 : 3617. doi: 10.1038/ncomms4617 24710426

24. Korasick DA, Westfall CS, Goo S, Nanao MH, Dumas R, Hagen G. Molecular basis for AUXIN RESPONSE FACTOR protein interaction and the control of auxin response repression. PNAS. 2014;111(14):5427–32. doi: 10.1073/pnas.1400074111 24706860

25. Parcy F, Vernoux T, Dumas R. A Glimpse beyond Structures in Auxin-Dependent Transcription. Trends in Plant Science. 2016;21 : 574–83. doi: 10.1016/j.tplants.2016.02.002 26994657

26. Guilfoyle TJ, Hagen G. Getting a grasp on domain III/IV responsible for Auxin Response Factor–IAA protein interactions. Plant Science. 2012 Jul;190 : 82–8. doi: 10.1016/j.plantsci.2012.04.003 22608522

27. Szemenyei H, Hannon M, Long J a. TOPLESS Mediates Auxin-Dependent Transcriptional Repression During Arabidopsis Embryogenesis. Science. 2008;319 : 1384. doi: 10.1126/science.1151461 18258861

28. Wu MF, Yamaguchi N, Xiao J, Bargmann B, Estelle M, Sang Y, et al. Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate. eLife. 2015;13(4):1–20.

29. Dinesh DC, Villalobos LI a C, Abel S. Structural Biology of Nuclear Auxin Action. Trends in Plant Science. 2016;21(4):302–16. doi: 10.1016/j.tplants.2015.10.019 26651917

30. Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, et al. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Molecular Systems Biology. 2014 Apr 16;7(1):508–508.

31. Piya S, Shrestha SK, Binder B, Stewart CN, Hewezi T. Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science [Internet]. 2014 Dec 23 [cited 2018 Mar 14];5. Available from: http://journal.frontiersin.org/article/10.3389/fpls.2014.00744/abstract

32. Trigg SA, Garza RM, MacWilliams A, Nery JR, Bartlett A, Castanon R, et al. CrY2H-seq: a massively multiplexed assay for deep-coverage interactome mapping. Nature Methods. 2017 Aug;14(8):819–25. doi: 10.1038/nmeth.4343 28650476

33. Lavy M, Prigge MJ, Tao S, Shain S, Kuo A, Kirchsteiger K, et al. Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife. 2016;1(5).

34. Chandler JW. Auxin response factors. Plant, cell & environment. 2016;39 : 1014–28.

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

36. Causier B, Lloyd J, Stevens L, Davies B. TOPLESS co-repressor interactions and their evolutionary conservation in plants. Plant Signaling & Behavior. 2012;7(3):325–8.

37. Flores-Sandoval E, Eklund DM, Bowman JL. A Simple Auxin Transcriptional Response System Regulates Multiple Morphogenetic Processes in the Liverwort Marchantia polymorpha. PLoS Genetics. 2015;11(5):1–26.

38. Kato H, Ishizaki K, Kouno M, Shirakawa M, Bowman JL, Nishihama R, et al. Auxin-Mediated Transcriptional System with a Minimal Set of Components Is Critical for Morphogenesis through the Life Cycle in Marchantia polymorpha. PLoS Genetics. 2015;11(5):1–26.

39. Bowman JL, Briginshaw LN, Fisher TJ, Flores-Sandoval E. Something ancient and something neofunctionalized—evolution of land plant hormone signaling pathways. Current Opinion in Plant Biology. 2019 Feb;47 : 64–72. doi: 10.1016/j.pbi.2018.09.009 30339930

40. Flores-Sandoval E, Eklund DM, Hong S-F, Alvarez JP, Fisher TJ, Lampugnani ER, et al. Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. New Phytologist. 2018 Jun;218(4):1612–30. doi: 10.1111/nph.15090 29574879

41. Ohtaka K, Hori K, Kanno Y, Seo M, Ohta H. Primitive Auxin Response without TIR1 and Aux / IAA in the Charophyte Alga Klebsormidium nitens 1. Plant Physiology. 2017;174(July):1621–32.

42. Lemieux C, Otis C, Turmel M. Comparative Chloroplast Genome Analyses of Streptophyte Green Algae Uncover Major Structural Alterations in the Coleochaetophyceae and Zygnematophyceae. Frontiers in plant science. 2016;7(697).

43. Turmel M, Otis C, Lemieux C. Tracing the Evolution of Streptophyte Algae and Their. Genome Biology and Evolution. 2013;5(10):1817–35. doi: 10.1093/gbe/evt135 24022472

44. Matasci N, Hung L-H, Yan Z, Carpenter EJ, Wickett NJ, Mirarab S, et al. Data access for the 1,000 Plants (1KP) project. GIGA SCIENCE. 2014;3(17):1–10.

45. Swaminathan K, Peterson K, Jack T. The plant B3 superfamily. Trends in Plant Science. 2008;13(12):647–55. doi: 10.1016/j.tplants.2008.09.006 18986826

46. Boer DR, Freire-Rios A, Van Den Berg WAM, Saaki T, Manfield IW, Kepinski S, et al. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell. 2014;156(3):577–89. doi: 10.1016/j.cell.2013.12.027 24485461

47. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modelling, prediction and analysis. Nature Protocols. 2017;10(6):845–58.

48. Kagaya Y, Ohmiya K, Hattori T. RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Research. 1999;27(2):470–8. doi: 10.1093/nar/27.2.470 9862967

49. Martin-Arevalillo R, Nanao MH, Larrieu A, Vinos-poyo T, Mast D. Structure of the Arabidopsis TOPLESS corepressor provides insight into the evolution of transcriptional repression. PNAS. 2017;114(30):8107–12. doi: 10.1073/pnas.1703054114 28698367

50. Choi H, Seo M, Cho H. Two TPL-Binding Motifs of ARF2 Are Involved in Repression of Auxin Responses. Frontiers in Plant Science. 2018;9(372):1–9.

51. Ke J, Ma H, Gu X, Thelen A, Brunzelle JS, Li J. Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors. Science Advances. 2015;1(6):1–12.

52. Collins J, O’Grady K, Chen S, Gurley W. The C-terminal WD40 repeats on the TOPLESS co-repressor function as a protein–protein interaction surface. Plant Molecular Biology. 2019 May;100(1–2):47–58. doi: 10.1007/s11103-019-00842-w 30783952