Building beauty: Understanding how hormone signaling regulates petal patterning and morphogenesis.

Elena Salvi, Edwige Moyroud
Author Information
  1. Elena Salvi: The Sainsbury Laboratory, University of Cambridge, 47 Bateman Street, Cambridge, CB2 1LR, UK.
  2. Edwige Moyroud: The Sainsbury Laboratory, University of Cambridge, 47 Bateman Street, Cambridge, CB2 1LR, UK. ORCID

Abstract

The corolla of flowering plants provides pivotal functions for the reproduction of angiosperms, directly impacting the fitness of individuals. Different petal shapes and patterns contribute to these functions and, thus, participate in the production of morphological diversity and the emergence of new species. During petal morphogenesis, the coordination of cell fate specification, cell division, and cell expansion is coherent and robust across the petal blade and is set according to proximo-distal, medio-lateral, and abaxial-adaxial axes. However, the mechanisms specifying petal polarity and controlling cell behavior in a position-dependent manner as petals develop remain poorly understood. In this review, we draw parallels with other evolutionarily related plant lateral organs such as leaves to argue that hormones likely play central, yet largely unexplored, roles in such coordination. By examining petal development in Arabidopsis and other angiosperms, we frame what are the knowns and the unknowns of hormones contributions to petal morphogenesis and patterning. Finally, we argue that using emerging model organisms can provide invaluable information to tackle questions that have long remained unanswered, broadening our understanding by allowing us to investigate petal morphogenesis and the tinkering of phytohormone signaling through an evolutionary lens.

Keywords

References

  1. New Phytol. 2016 Jul;211(2):708-18 [PMID: 26987355]
  2. Plant Physiol. 1995 Mar;107(3):695-702 [PMID: 12228393]
  3. Nature. 2020 Aug;584(7822):602-607 [PMID: 32641831]
  4. Mol Plant. 2014 Oct;7(10):1533-44 [PMID: 25053833]
  5. Ann Bot. 2021 Nov 9;128(7):931-942 [PMID: 34508638]
  6. Int J Mol Sci. 2019 Aug 20;20(16): [PMID: 31434317]
  7. PLoS Biol. 2009 Apr 21;7(4):e1000090 [PMID: 19385720]
  8. Kybernetik. 1972 Dec;12(1):30-9 [PMID: 4663624]
  9. Essays Biochem. 2022 Dec 8;66(6):753-768 [PMID: 36205404]
  10. Front Plant Sci. 2023 Jun 23;14:1190373 [PMID: 37426957]
  11. Plant Cell. 2011 Jan;23(1):69-80 [PMID: 21224426]
  12. Plant Cell. 2011 Mar;23(3):973-83 [PMID: 21421811]
  13. Plants (Basel). 2018 Dec 25;8(1): [PMID: 30585196]
  14. Evodevo. 2021 Dec 15;12(1):14 [PMID: 34911578]
  15. J Exp Biol. 2021 Jun 15;224(12): [PMID: 34161560]
  16. Curr Opin Plant Biol. 2023 Dec;76:102460 [PMID: 37775406]
  17. Plant Cell. 2013 Jul;25(7):2482-503 [PMID: 23821642]
  18. New Phytol. 2020 Sep;227(5):1392-1405 [PMID: 32356309]
  19. Nat Rev Genet. 2011 Jan;12(1):43-55 [PMID: 21164524]
  20. Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):22008-13 [PMID: 19959665]
  21. J Exp Bot. 2016 Dec;67(22):6473-6480 [PMID: 27838638]
  22. Plants (Basel). 2020 Apr 04;9(4): [PMID: 32260328]
  23. Development. 1998 Sep;125(17):3497-508 [PMID: 9693152]
  24. J Theor Biol. 1969 Oct;25(1):1-47 [PMID: 4390734]
  25. Front Plant Sci. 2023 Jun 28;14:1142748 [PMID: 37457338]
  26. Plant Signal Behav. 2010 Sep;5(9):1134-7 [PMID: 20724826]
  27. J Biol Chem. 1997 Oct 3;272(40):24747-50 [PMID: 9312067]
  28. Development. 1996 Apr;122(4):1093-102 [PMID: 8620836]
  29. Development. 2022 Sep 1;149(17): [PMID: 35950915]
  30. Development. 2013 Jan 1;140(1):185-94 [PMID: 23175631]
  31. New Phytol. 2013 Jan;197(2):490-502 [PMID: 23253334]
  32. Front Plant Sci. 2021 Oct 27;12:745507 [PMID: 34777425]
  33. Plant Physiol. 2021 Oct 5;187(2):590-602 [PMID: 35237816]
  34. PLoS Genet. 2011 May;7(5):e1001388 [PMID: 21637781]
  35. PLoS Genet. 2017 Jun 23;13(6):e1006851 [PMID: 28644898]
  36. Am J Bot. 2001 Oct;88(10):1711-41 [PMID: 21669604]
  37. Proc Natl Acad Sci U S A. 2012 Aug 14;109(33):13452-7 [PMID: 22847437]
  38. Plant Physiol. 2017 Nov;175(3):1144-1157 [PMID: 28894023]
  39. J Exp Bot. 2020 May 30;71(10):2886-2897 [PMID: 32016398]
  40. Semin Cell Dev Biol. 2018 Jul;79:3-15 [PMID: 28941876]
  41. Elife. 2017 Dec 19;6: [PMID: 29254518]
  42. Plant J. 2018 Jun;94(5):867-879 [PMID: 29570883]
  43. Plant J. 2009 Dec;60(6):1070-80 [PMID: 19765234]
  44. J Exp Bot. 2021 Oct 13;72(19):6768-6788 [PMID: 34343283]
  45. New Phytol. 2011 Apr;190(1):113-124 [PMID: 21232060]
  46. Nat Plants. 2024 Mar;10(3):412-422 [PMID: 38409292]
  47. Nature. 2017 Oct 26;550(7677):469-474 [PMID: 29045384]
  48. Front Plant Sci. 2021 Aug 04;12:718091 [PMID: 34421972]
  49. New Phytol. 2020 Dec;228(6):1972-1985 [PMID: 32533864]
  50. Int J Dev Biol. 2009;53(8-10):1597-608 [PMID: 19247940]
  51. Trends Cell Biol. 1999 Dec;9(12):M65-8 [PMID: 10611686]
  52. New Phytol. 2017 Oct;216(2):350-354 [PMID: 27915467]
  53. Nat Commun. 2023 Aug 8;14(1):4763 [PMID: 37553331]
  54. Nat Plants. 2017 Oct;3(10):803-813 [PMID: 28970478]
  55. Sci Adv. 2024 Sep 13;10(37):eadp5574 [PMID: 39270029]
  56. Sci Rep. 2018 Aug 1;8(1):11542 [PMID: 30069009]
  57. Development. 2005 Feb;132(3):429-38 [PMID: 15634696]
  58. Plant Cell. 2020 Nov;32(11):3452-3468 [PMID: 32917737]
  59. Nature. 2007 Jun 7;447(7145):706-9 [PMID: 17554306]
  60. New Phytol. 2018 Jul;219(2):728-742 [PMID: 29681133]
  61. Curr Biol. 2020 Mar 9;30(5):802-814.e8 [PMID: 32155414]
  62. New Phytol. 2011 Jan;189(2):602-15 [PMID: 21039563]
  63. Development. 2004 Mar;131(5):1055-64 [PMID: 14973286]
  64. Nature. 2021 Apr;592(7856):768-772 [PMID: 33828298]
  65. Plant Cell. 2005 May;17(5):1434-48 [PMID: 15805484]
  66. J Exp Bot. 2024 Jul 23;75(14):4360-4372 [PMID: 38666596]
  67. Cell Rep. 2020 Mar 17;30(11):3904-3916.e3 [PMID: 32187558]
  68. New Phytol. 2024 Jul;243(1):240-257 [PMID: 38725421]
  69. Nat Plants. 2015 Jan 08;1:14007 [PMID: 27246054]
  70. Science. 2014 Feb 14;343(6172):780-3 [PMID: 24531971]
  71. Nature. 2014 Nov 6;515(7525):125-129 [PMID: 25156253]
  72. Curr Biol. 2012 Jul 10;22(13):1183-7 [PMID: 22683264]
  73. Science. 2023 Jun 23;380(6651):1275-1281 [PMID: 37347863]
  74. Planta. 1989 Aug;179(1):89-96 [PMID: 24201426]
  75. Curr Biol. 2019 Aug 19;29(16):R781-R785 [PMID: 31430470]
  76. J Exp Bot. 2022 Jun 2;73(11):3308-3318 [PMID: 35275176]
  77. Plant Cell. 1991 Jul;3(7):677-684 [PMID: 12324609]
  78. Plant Cell. 2017 Jun;29(6):1232-1247 [PMID: 28442597]
  79. Curr Opin Plant Biol. 2023 Oct;75:102443 [PMID: 37666097]
  80. PLoS Biol. 2010 Oct 19;8(10):e1000516 [PMID: 20976043]
  81. Nat Commun. 2019 Feb 6;10(1):619 [PMID: 30728357]
  82. Plant Cell. 2024 Jan 30;36(2):324-345 [PMID: 37804091]
  83. Curr Opin Plant Biol. 2021 Oct;63:102038 [PMID: 33940553]
  84. Planta. 2006 Jan;223(2):315-28 [PMID: 16208486]
  85. Dev Cell. 2013 Feb 25;24(4):438-45 [PMID: 23449474]
  86. Plant Cell. 2014 Dec;26(12):4718-32 [PMID: 25516601]
  87. New Phytol. 2014 Dec;204(4):1013-27 [PMID: 25103615]
  88. Curr Biol. 2022 Dec 19;32(24):5323-5334.e6 [PMID: 36423640]
  89. Plant Physiol. 1992 Jan;98(1):191-7 [PMID: 16668613]
  90. Front Plant Sci. 2020 Mar 06;11:249 [PMID: 32211004]
  91. Plant Physiol. 2024 Mar 29;194(4):2338-2353 [PMID: 38084893]
  92. Proc Natl Acad Sci U S A. 2020 Sep 8;117(36):22552-22560 [PMID: 32848061]
  93. Development. 2004 Aug;131(16):4035-45 [PMID: 15269176]
  94. Plant J. 2011 Mar;65(5):771-84 [PMID: 21235651]
  95. J Exp Bot. 2018 Jan 4;69(2):137-146 [PMID: 29211894]
  96. New Phytol. 2021 Jan;229(2):1147-1162 [PMID: 32880946]
  97. Curr Biol. 2024 Feb 26;34(4):755-768.e4 [PMID: 38272029]
  98. Dev Cell. 2013 Aug 26;26(4):405-15 [PMID: 23987513]
  99. Plant Physiol. 2001 Jan;125(1):112-4 [PMID: 11154310]
  100. C R Acad Sci III. 2001 Jun;324(6):523-30 [PMID: 11455874]
  101. Nature. 2007 Mar 8;446(7132):199-202 [PMID: 17344852]
  102. Curr Biol. 2012 Oct 9;22(19):1739-46 [PMID: 22902754]
  103. Proc Natl Acad Sci U S A. 2010 Jun 8;107(23):10754-9 [PMID: 20498057]
  104. Curr Biol. 2020 Nov 16;30(22):4425-4431.e3 [PMID: 32946752]
  105. Plant J. 2012 Sep;71(5):724-35 [PMID: 22507233]
  106. J Exp Bot. 2023 Aug 3;74(14):4093-4109 [PMID: 37102769]
  107. Curr Opin Plant Biol. 2014 Feb;17:116-25 [PMID: 24507503]
  108. Curr Biol. 2020 May 4;30(9):1626-1638.e3 [PMID: 32220322]
  109. J Exp Bot. 2021 Feb 27;72(5):1809-1821 [PMID: 33258902]
  110. PeerJ. 2017 May 31;5:e3382 [PMID: 28584713]
  111. PLoS Biol. 2013;11(4):e1001550 [PMID: 23653565]
  112. Curr Opin Plant Biol. 2022 Feb;65:102111 [PMID: 34543915]
  113. Plant J. 2019 Mar;97(5):805-824 [PMID: 30748050]
  114. Nat Commun. 2023 Nov 4;14(1):7106 [PMID: 37925502]
  115. Int J Mol Sci. 2023 Nov 16;24(22): [PMID: 38003605]
  116. Plant Physiol Biochem. 2023 Aug;201:107835 [PMID: 37348389]
  117. Arthropod Plant Interact. 2020;14(2):193-206 [PMID: 32215113]
  118. Curr Opin Plant Biol. 2005 Dec;8(6):593-9 [PMID: 16207533]
  119. Hortic Res. 2024 Jan 12;11(3):uhae015 [PMID: 38544551]
  120. BMC Genomics. 2019 Aug 22;20(1):668 [PMID: 31438840]
  121. J Exp Bot. 2021 May 4;72(10):3597-3610 [PMID: 33712842]
  122. Proc Biol Sci. 2012 Apr 22;279(1733):1640-5 [PMID: 22090381]
  123. Int J Mol Sci. 2024 Feb 23;25(5): [PMID: 38473825]
  124. BMC Plant Biol. 2021 Feb 17;21(1):98 [PMID: 33596836]
  125. Cell Rep. 2024 Jul 23;43(7):114444 [PMID: 38990723]
  126. Nat Commun. 2024 May 8;15(1):3895 [PMID: 38719832]
  127. Biol Rev Camb Philos Soc. 2021 Aug;96(4):1676-1693 [PMID: 33955646]
  128. Development. 1999 Dec;126(24):5635-44 [PMID: 10572040]
  129. Plant Physiol. 1994 Feb;104(2):321-326 [PMID: 12232083]
  130. New Phytol. 2016 Jan;209(2):485-98 [PMID: 26391543]
  131. New Phytol. 2021 Apr;230(1):218-227 [PMID: 33280125]
  132. New Phytol. 2023 Apr;238(1):125-141 [PMID: 36404129]
  133. Development. 2016 Dec 1;143(23):4425-4429 [PMID: 27789625]
  134. Plant J. 2013 Jun;74(6):893-904 [PMID: 23551385]
  135. New Phytol. 2019 Apr;222(2):1123-1138 [PMID: 30570752]
  136. PLoS Genet. 2024 Mar 5;20(3):e1011203 [PMID: 38442104]
  137. Development. 2011 Mar;138(5):839-48 [PMID: 21270053]
  138. Proc Natl Acad Sci U S A. 2009 Dec 29;106(52):22534-9 [PMID: 20007771]
  139. Development. 2015 Apr 1;142(7):1203-11 [PMID: 25804733]

Grants

  1. /Accademia Nazionale dei Lincei
  2. PTAG/022/Gatsby Charitable Foundation
  3. PTAG/122/Gatsby Charitable Foundation
  4. PTAG/073/Isaac Newton/ Wellcome Fund

MeSH Term

Flowers
Plant Growth Regulators
Signal Transduction
Morphogenesis
Arabidopsis
Magnoliopsida
Gene Expression Regulation, Plant

Chemicals

Plant Growth Regulators

Word Cloud

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