1932

Abstract

This review focuses on the evolution of plant hormone signaling pathways. Like the chemical nature of the hormones themselves, the signaling pathways are diverse. Therefore, we focus on a group of hormones whose primary perception mechanism involves an Skp1/Cullin/F-box-type ubiquitin ligase: auxin, jasmonic acid, gibberellic acid, and strigolactone. We begin with a comparison of the core signaling pathways of these four hormones, which have been established through studies conducted in model organisms in the Angiosperms. With the advent of next-generation sequencing and advanced tools for genetic manipulation, the door to understanding the origins of hormone signaling mechanisms in plants beyond these few model systems has opened. For example, in-depth phylogenetic analyses of hormone signaling components are now being complemented by genetic studies in early diverging land plants. Here we discuss recent investigations of how basal land plants make and sense hormones. Finally, we propose connections between the emergence of hormone signaling complexity and major developmental transitions in plant evolution.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050718-100309
2020-04-29
2024-06-21
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-050718-100309.html?itemId=/content/journals/10.1146/annurev-arplant-050718-100309&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abe S, Sado A, Tanaka K, Kisugi T, Asami K et al. 2014. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. PNAS 111:5018084–89
    [Google Scholar]
  2. 2. 
    Abel S, Nguyen MD, Theologis A 1995. The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol 251:4533–49
    [Google Scholar]
  3. 3. 
    Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S et al. 2009. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr. Biol 19:141188–93
    [Google Scholar]
  4. 4. 
    Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K et al. 2011. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. PNAS 108:5020242–47
    [Google Scholar]
  5. 5. 
    Akiyama K, Matsuzaki K-I, Hayashi H 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:7043824–27
    [Google Scholar]
  6. 6. 
    Alabadí D, Blázquez MA. 2009. Molecular interactions between light and hormone signaling to control plant growth. Plant Mol. Biol. 69:4409–17
    [Google Scholar]
  7. 7. 
    Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT et al. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:755498–101
    [Google Scholar]
  8. 8. 
    Bai Y, Meng Y, Huang D, Qi Y, Chen M 2011. Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics 98:2128–36
    [Google Scholar]
  9. 9. 
    Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:6032960–63
    [Google Scholar]
  10. 10. 
    Bell E, Creelman RA, Mullet JE 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. PNAS 92:198675–79
    [Google Scholar]
  11. 11. 
    Bennett T, Brockington SF, Rothfels C, Graham SW, Stevenson D et al. 2014. Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure. Mol. Biol. Evol. 31:82042–60
    [Google Scholar]
  12. 12. 
    Bennett T, Liang Y, Seale M, Ward S, Müller D, Leyser O 2016. Strigolactone regulates shoot development through a core signalling pathway. Biol. Open 5:121806–20
    [Google Scholar]
  13. 13. 
    Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D 1998. Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:5791–800
    [Google Scholar]
  14. 14. 
    Bogaert KA, Blommaert L, Ljung K, Beeckman T, De Clerck O 2019. Auxin function in the brown alga Dictyota dichotoma. Plant Physiol 179:1280–99
    [Google Scholar]
  15. 15. 
    Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S et al. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:2287–304.e15
    [Google Scholar]
  16. 16. 
    Brewer PB, Yoneyama K, Filardo F, Meyers E, Scaffidi A et al. 2016. LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. PNAS 113:226301–6
    [Google Scholar]
  17. 17. 
    Briones-Moreno A, Hernández-García J, Vargas-Chávez C, Romero-Campero FJ, Romero JM et al. 2017. Evolutionary analysis of DELLA-associated transcriptional networks. Front. Plant Sci. 8:626
    [Google Scholar]
  18. 18. 
    Bürger M, Mashiguchi K, Lee HJ, Nakano M, Takemoto K et al. 2019. Structural basis of karrikin and non-natural strigolactone perception in Physcomitrella patens. Cell Rep 26:4855–65.e5
    [Google Scholar]
  19. 19. 
    Bythell-Douglas R, Rothfels CJ, Stevenson DWD, Graham SW, Wong GK-S et al. 2017. Evolution of strigolactone receptors by gradual neo-functionalization of KAI2 paralogues. BMC Biol 15:152
    [Google Scholar]
  20. 20. 
    Calderón Villalobos LIA, Lee S, De Oliveira C, Ivetac A, Brandt W et al. 2012. A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat. Chem. Biol. 8:5477–85
    [Google Scholar]
  21. 21. 
    Carlsson GH, Hasse D, Cardinale F, Prandi C, Andersson I 2018. The elusive ligand complexes of the DWARF14 strigolactone receptor. J. Exp. Bot. 69:92345–54
    [Google Scholar]
  22. 22. 
    Causier B, Ashworth M, Guo W, Davies B 2012. The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:1423–38
    [Google Scholar]
  23. 23. 
    Challis RJ, Hepworth J, Mouchel C, Waites R, Leyser O 2013. A role for MORE AXILLARY GROWTH1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol 161:41885–902
    [Google Scholar]
  24. 24. 
    Chini A, Fonseca S, Fernández G, Adie B, Chico JM et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:7154666–71
    [Google Scholar]
  25. 25. 
    Claeys H, De Bodt S, Inzé D 2014. Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci 19:4231–39
    [Google Scholar]
  26. 26. 
    Colebrook EH, Thomas SG, Phillips AL, Hedden P 2014. The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol. 217:67–75
    [Google Scholar]
  27. 27. 
    Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B et al. 2015. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:6247540–43
    [Google Scholar]
  28. 28. 
    Conn CE, Nelson DC. 2015. Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front. Plant Sci. 6:1219
    [Google Scholar]
  29. 29. 
    Davière J-M, Achard P. 2013. Gibberellin signaling in plants. Development 140:61147–51
    [Google Scholar]
  30. 30. 
    Davière J-M, Achard P. 2016. A pivotal role of DELLAs in regulating multiple hormone signals. Mol. Plant. 9:110–20
    [Google Scholar]
  31. 31. 
    de Lucas M, Davière J-M, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM et al. 2008. A molecular framework for light and gibberellin control of cell elongation. Nature 451:7177480–84
    [Google Scholar]
  32. 32. 
    de Saint Germain A, Clavé G, Badet-Denisot M-A, Pillot J-P, Cornu D et al. 2016. An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nat. Chem. Biol. 12:10787–94
    [Google Scholar]
  33. 33. 
    De Smet I, Voß U, Lau S, Wilson M, Shao N et al. 2011. Unraveling the evolution of auxin signaling. Plant Physiol 155:1209–21
    [Google Scholar]
  34. 34. 
    Delaux P-M, Xie X, Timme RE, Puech-Pages V, Dunand C et al. 2012. Origin of strigolactones in the green lineage. New Phytol 195:4857–71
    [Google Scholar]
  35. 35. 
    Demkura PV, Abdala G, Baldwin IT, Ballaré CL 2010. Jasmonate-dependent and -independent pathways mediate specific effects of solar ultraviolet B radiation on leaf phenolics and antiherbivore defense. Plant Physiol 152:21084–95
    [Google Scholar]
  36. 36. 
    Dharmasiri N, Dharmasiri S, Estelle M 2005. The F-box protein TIR1 is an auxin receptor. Nature 435:7041441–45
    [Google Scholar]
  37. 37. 
    Dorcey E, Urbez C, Blázquez MA, Carbonell J, Perez-Amador MA 2009. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J 58:2318–32
    [Google Scholar]
  38. 38. 
    Engel MS. 2015. Insect evolution. Curr. Biol. 25:19R868–72
    [Google Scholar]
  39. 39. 
    Evans MMS, Poethig RS. 1995. Gibberellins promote vegetative phase change and reproductive maturity in maize. Plant Physiol 108:2475–87
    [Google Scholar]
  40. 40. 
    Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico J-M, Gimenez-Ibanez S et al. 2011. 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 23:2701–15
    [Google Scholar]
  41. 41. 
    Flematti GR, Scaffidi A, Waters MT, Smith SM 2016. Stereospecificity in strigolactone biosynthesis and perception. Planta 243:61361–73
    [Google Scholar]
  42. 42. 
    Flores-Sandoval E, Eklund DM, Bowman JL 2015. A simple auxin transcriptional response system regulates multiple morphogenetic processes in the liverwort Marchantia polymorpha. PLOS Genet 11:5e1005207
    [Google Scholar]
  43. 43. 
    Flores-Sandoval E, Eklund DM, Hong S-F, Alvarez JP, Fisher TJ et al. 2018. Class C ARFs evolved before the origin of land plants and antagonize differentiation and developmental transitions in Marchantia polymorpha. New Phytol 218:41612–30
    [Google Scholar]
  44. 44. 
    Fonouni-Farde C, Tan S, Baudin M, Brault M, Wen J et al. 2016. DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nat. Commun. 7:12636
    [Google Scholar]
  45. 45. 
    Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A et al. 2012. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. PNAS 109:3313446–51
    [Google Scholar]
  46. 46. 
    Gallego-Bartolomé J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabadí D 2010. Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol. Biol. Evol. 27:61247–56
    [Google Scholar]
  47. 47. 
    Gobena D, Shimels M, Rich PJ, Ruyter-Spira C, Bouwmeester H et al. 2017. Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. PNAS 114:174471–76
    [Google Scholar]
  48. 48. 
    Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA et al. 2008. Strigolactone inhibition of shoot branching. Nature 455:7210189–94
    [Google Scholar]
  49. 49. 
    Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M 2001. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:6861271–76
    [Google Scholar]
  50. 50. 
    Guo Y, Zheng Z, La Clair JJ, Chory J, Noel JP 2013. Smoke-derived karrikin perception by the α/β-hydrolase KAI2 from Arabidopsis. PNAS 110:208284–89
    [Google Scholar]
  51. 51. 
    Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG et al. 2015. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350:62671521–24
    [Google Scholar]
  52. 52. 
    Hamiaux C, Drummond RSM, Janssen BJ, Ledger SE, Cooney JM et al. 2012. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 22:212032–36
    [Google Scholar]
  53. 53. 
    Hayashi K-I, Horie K, Hiwatashi Y, Kawaide H, Yamaguchi S et al. 2010. Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol 153:31085–97
    [Google Scholar]
  54. 54. 
    Hernández-García J, Briones-Moreno A, Dumas R, Blázquez MA 2019. Origin of gibberellin-dependent transcriptional regulation by molecular exploitation of a transactivation domain in DELLA proteins. Mol. Biol. Evol. 36:5908–18
    [Google Scholar]
  55. 55. 
    Hirano K, Nakajima M, Asano K, Nishiyama T, Sakakibara H et al. 2007. The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens. Plant Cell 19:103058–79
    [Google Scholar]
  56. 56. 
    Hoffmann B, Proust H, Belcram K, Labrune C, Boyer F-D et al. 2014. Strigolactones inhibit caulonema elongation and cell division in the moss Physcomitrella patens. PLOS ONE 9:6e99206
    [Google Scholar]
  57. 57. 
    Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978
    [Google Scholar]
  58. 58. 
    Hua Z, Zou C, Shiu S-H, Vierstra RD 2011. Phylogenetic comparison of F-Box (FBX) gene superfamily within the plant kingdom reveals divergent evolutionary histories indicative of genomic drift. PLOS ONE 6:1e16219
    [Google Scholar]
  59. 59. 
    Huang H, Liu B, Liu L, Song S 2017. Jasmonate action in plant growth and development. J. Exp. Bot. 68:61349–59
    [Google Scholar]
  60. 60. 
    Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M et al. 2001. slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:5999–1010
    [Google Scholar]
  61. 61. 
    Iuchi S, Suzuki H, Kim Y-C, Iuchi A, Kuromori T et al. 2007. Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50:6958–66
    [Google Scholar]
  62. 62. 
    Jang G, Yi K, Pires ND, Menand B, Dolan L 2011. RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 138:112273–81
    [Google Scholar]
  63. 63. 
    Jasinski S, Tattersall A, Piazza P, Hay A, Martinez-Garcia JF et al. 2008. PROCERA encodes a DELLA protein that mediates control of dissected leaf form in tomato. Plant J 56:4603–12
    [Google Scholar]
  64. 64. 
    Jiang L, Liu X, Xiong G, Liu H, Chen F et al. 2013. DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:7480401–5
    [Google Scholar]
  65. 65. 
    Jin Y, Liu H, Luo D, Yu N, Dong W et al. 2016. DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat. Commun. 7:12433
    [Google Scholar]
  66. 66. 
    Kapulnik Y, Delaux P-M, Resnick N, Mayzlish-Gati E, Wininger S et al. 2011. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:1209–16
    [Google Scholar]
  67. 67. 
    Kato H, Ishizaki K, Kouno M, Shirakawa M, Bowman JL et al. 2015. Auxin-mediated transcriptional system with a minimal set of components is critical for morphogenesis through the life cycle in Marchantia polymorpha. PLOS Genet 11:5e1005084
    [Google Scholar]
  68. 68. 
    Kazan K. 2015. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci 20:4219–29
    [Google Scholar]
  69. 69. 
    Kenrick P, Crane PR. 1997. The origin and early evolution of plants on land. Nature 389:33–39
    [Google Scholar]
  70. 70. 
    Kepinski S, Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:7041446–51
    [Google Scholar]
  71. 71. 
    Kim J, Harter K, Theologis A 1997. Protein–protein interactions among the Aux/IAA proteins. PNAS 94:2211786–91
    [Google Scholar]
  72. 72. 
    Lang D, Ullrich KK, Murat F, Fuchs J, Jenkins J et al. 2018. The Physcomitrella patens chromosome-scale assembly reveals moss genome structure and evolution. Plant J 93:3515–33
    [Google Scholar]
  73. 73. 
    Larrieu A, Champion A, Legrand J, Lavenus J, Mast D et al. 2015. A fluorescent hormone biosensor reveals the dynamics of jasmonate signalling in plants. Nat. Commun. 6:6043
    [Google Scholar]
  74. 74. 
    Lau S, Jürgens G, De Smet I 2008. The evolving complexity of the auxin pathway. Plant Cell 20:71738–46
    [Google Scholar]
  75. 75. 
    Lavy M, Prigge MJ, Tao S, Shain S, Kuo A et al. 2016. Constitutive auxin response in Physcomitrella reveals complex interactions between Aux/IAA and ARF proteins. eLife 5:e13325
    [Google Scholar]
  76. 76. 
    Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA et al. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:679–85
    [Google Scholar]
  77. 77. 
    Leyser O. 2018. Auxin signaling. Plant Physiol 176:1465–79
    [Google Scholar]
  78. 78. 
    Liang Y, Ward S, Li P, Bennett T, Leyser O 2016. SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms. Plant Cell 28:71581–601
    [Google Scholar]
  79. 79. 
    Li W, Nguyen KH, Chu HD, Van Ha C, Watanabe Y et al. 2017. The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana. PLOS Genet 13:11e1007076
    [Google Scholar]
  80. 80. 
    Liu J, Cheng X, Liu P, Sun J 2017. miR156-targeted SBP-box transcription factors interact with DWARF53 to regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat. Plant Physiol 174:31931–48
    [Google Scholar]
  81. 81. 
    Ljung K. 2013. Auxin metabolism and homeostasis during plant development. Development 140:5943–50
    [Google Scholar]
  82. 82. 
    Lopez-Obando M, Conn CE, Hoffmann B, Bythell-Douglas R, Nelson DC et al. 2016. Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens. Planta 243:61441–53
    [Google Scholar]
  83. 83. 
    Lopez-Obando M, de Villiers R, Hoffmann B, Ma L, de Saint Germain A et al. 2018. Physcomitrella patens MAX2 characterization suggests an ancient role for this F-box protein in photomorphogenesis rather than strigolactone signalling. New Phytol 219:2743–56
    [Google Scholar]
  84. 84. 
    MacMillan J. 2001. Occurrence of gibberellins in vascular plants, fungi, and bacteria. J. Plant Growth Regul. 20:4387–442
    [Google Scholar]
  85. 85. 
    Marín-de la Rosa N, Sotillo B, Miskolczi P, Gibbs DJ, Vicente J et al. 2014. Large-scale identification of gibberellin-related transcription factors defines group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners. Plant Physiol 166:21022–32
    [Google Scholar]
  86. 86. 
    Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H et al. 2011. The main auxin biosynthesis pathway in Arabidopsis. PNAS 108:4518512–17
    [Google Scholar]
  87. 87. 
    Massari ME, Murre C. 2000. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20:2429–40
    [Google Scholar]
  88. 88. 
    Masucci JD, Schiefelbein JW. 1994. The rhd6 mutation of Arabidopsis thaliana alters root-hair initiation through an auxin- and ethylene-associated process. Plant Physiol 106:41335–46
    [Google Scholar]
  89. 89. 
    Matasci N, Hung L-H, Yan Z, Carpenter EJ, Wickett NJ et al. 2014. Data access for the 1,000 Plants (1KP) project. Gigascience 3:17
    [Google Scholar]
  90. 90. 
    Miyazaki S, Hara M, Ito S, Tanaka K, Asami T et al. 2018. An ancestral gibberellin in a moss Physcomitrella patens. Mol. Plant 11:81097–100
    [Google Scholar]
  91. 91. 
    Miyazaki S, Katsumata T, Natsume M, Kawaide H 2011. The CYP701B1 of Physcomitrella patens is an ent-kaurene oxidase that resists inhibition by uniconazole-P. FEBS Lett 585:121879–83
    [Google Scholar]
  92. 92. 
    Monte I, Ishida S, Zamarreño AM, Hamberg M, Franco-Zorrilla JM et al. 2018. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat. Chem. Biol. 14:5480–88
    [Google Scholar]
  93. 93. 
    Moturu TR, Thula S, Singh RK, Nodzynski T, Vareková RS et al. 2018. Molecular evolution and diversification of the SMXL gene family. J. Exp. Bot. 69:92367–78
    [Google Scholar]
  94. 94. 
    Moyroud E, Glover BJ. 2017. The evolution of diverse floral morphologies. Curr. Biol. 27:17R941–51
    [Google Scholar]
  95. 95. 
    Murase K, Hirano Y, Sun T-P, Hakoshima T 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:7221459–63
    [Google Scholar]
  96. 96. 
    Mutte SK, Kato H, Rothfels C, Melkonian M, Wong GK-S, Weijers D 2018. Origin and evolution of the nuclear auxin response system. eLife 7:e33399
    [Google Scholar]
  97. 97. 
    Navarro L, Bari R, Achard P, Lisón P, Nemri A et al. 2008. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr. Biol. 18:9650–55
    [Google Scholar]
  98. 98. 
    Navarro-Quezada A, Schumann N, Quint M 2013. Plant F-box protein evolution is determined by lineage-specific timing of major gene family expansion waves. PLOS ONE 8:7e68672
    [Google Scholar]
  99. 99. 
    Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM 2012. Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu. Rev. Plant Biol. 63:107–30
    [Google Scholar]
  100. 100. 
    Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR et al. 2011. F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. PNAS 108:218897–902
    [Google Scholar]
  101. 101. 
    Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D et al. 2018. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174:2448–64.e24
    [Google Scholar]
  102. 102. 
    Oh E, Zhu J-Y, Bai M-Y, Arenhart RA, Sun Y, Wang Z-Y 2014. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife 3:e03031
    [Google Scholar]
  103. 103. 
    Ohtaka K, Hori K, Kanno Y, Seo M, Ohta H 2017. Primitive auxin response without TIR1 and Aux/IAA in the charophyte alga Klebsormidium nitens. Plant Physiol 174:31621–32
    [Google Scholar]
  104. 104. 
    Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W et al. 2010. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–91
    [Google Scholar]
  105. 105. 
    Peng J, Carol P, Richards DE, King KE, Cowling RJ et al. 1997. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:233194–205
    [Google Scholar]
  106. 106. 
    Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V et al. 2016. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr. Biol. 26:8987–98
    [Google Scholar]
  107. 107. 
    Prigge MJ, Lavy M, Ashton NW, Estelle M 2010. Physcomitrella patens auxin-resistant mutants affect conserved elements of an auxin-signaling pathway. Curr. Biol. 20:211907–12
    [Google Scholar]
  108. 108. 
    Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG et al. 2011. Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:81531–39
    [Google Scholar]
  109. 109. 
    Remington DL, Vision TJ, Guilfoyle TJ, Reed JW 2004. Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol 135:31738–52
    [Google Scholar]
  110. 110. 
    Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319:585964–69
    [Google Scholar]
  111. 111. 
    Roosjen M, Paque S, Weijers D 2018. Auxin Response Factors: output control in auxin biology. J. Exp. Bot. 69:2179–88
    [Google Scholar]
  112. 112. 
    Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L et al. 2011. Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones. Plant Physiol 155:2721–34
    [Google Scholar]
  113. 113. 
    Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M 2003. Involvement of auxin and a homeodomain-leucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130:204835–46
    [Google Scholar]
  114. 114. 
    Samodelov SL, Beyer HM, Guo X, Augustin M, Jia K-P et al. 2016. StrigoQuant: a genetically encoded biosensor for quantifying strigolactone activity and specificity. Sci. Adv. 2:11e1601266
    [Google Scholar]
  115. 115. 
    Sasse J, Simon S, Gübeli C, Liu G-W, Cheng X et al. 2015. Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Curr. Biol. 25:5647–55
    [Google Scholar]
  116. 116. 
    Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF et al. 2014. A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343:6171645–48
    [Google Scholar]
  117. 117. 
    Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW et al. 2014. Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:31221–32
    [Google Scholar]
  118. 118. 
    Schumann N, Navarro-Quezada A, Ullrich K 2011. Molecular evolution and selection patterns of plant F-box proteins with C-terminal kelch repeats. Plant Physiol 155:2835–50
    [Google Scholar]
  119. 119. 
    Seto Y, Yasui R, Kameoka H, Tamiru M, Cao M et al. 2019. Strigolactone perception and deactivation by a hydrolase receptor DWARF14. Nat. Commun. 10:191
    [Google Scholar]
  120. 120. 
    Shabek N, Ticchiarelli F, Mao H, Hinds TR, Leyser O, Zheng N 2018. Structural plasticity of D3-D14 ubiquitin ligase in strigolactone signalling. Nature 563:7733652–56
    [Google Scholar]
  121. 121. 
    Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G et al. 2010. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:7322400–5
    [Google Scholar]
  122. 122. 
    Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y et al. 2008. Structural basis for gibberellin recognition by its receptor GID1. Nature 456:7221520–23
    [Google Scholar]
  123. 123. 
    Shinohara N, Taylor C, Leyser O 2013. Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLOS Biol 11:1e1001474
    [Google Scholar]
  124. 124. 
    Silverstone AL, Ciampaglio CN, Sun T-P 1998. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:2155–69
    [Google Scholar]
  125. 125. 
    Singh DP, Jermakow AM, Swain SM 2002. Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 14:123133–47
    [Google Scholar]
  126. 126. 
    Skaar JR, Pagan JK, Pagano M 2013. Mechanisms and function of substrate recruitment by F-box proteins. Nat. Rev. Mol. Cell Biol. 14:6369–81
    [Google Scholar]
  127. 127. 
    Song X, Lu Z, Yu H, Shao G, Xiong J et al. 2017. IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res 27:91128–41
    [Google Scholar]
  128. 128. 
    Soundappan I, Bennett T, Morffy N, Liang Y, Stanga JP et al. 2015. SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27:113143–59
    [Google Scholar]
  129. 129. 
    Stanga JP, Morffy N, Nelson DC 2016. Functional redundancy in the control of seedling growth by the karrikin signaling pathway. Planta 243:61397–406
    [Google Scholar]
  130. 130. 
    Stanga JP, Smith SM, Briggs WR, Nelson DC 2013. SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol 163:1318–30
    [Google Scholar]
  131. 131. 
    Staswick PE. 2009. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol 150:31310–21
    [Google Scholar]
  132. 132. 
    Strader LC, Culler AH, Cohen JD, Bartel B 2010. Conversion of endogenous indole-3-butyric acid to indole-3-acetic acid drives cell expansion in Arabidopsis seedlings. Plant Physiol 153:41577–86
    [Google Scholar]
  133. 133. 
    Suzuki H, Park S-H, Okubo K, Kitamura J, Ueguchi-Tanaka M et al. 2009. Differential expression and affinities of Arabidopsis gibberellin receptors can explain variation in phenotypes of multiple knock-out mutants. Plant J 60:148–55
    [Google Scholar]
  134. 134. 
    Swarbreck SM, Guerringue Y, Matthus E, Jamieson FJC, Davies JM 2019. Impairment in karrikin but not strigolactone sensing enhances root skewing in Arabidopsis thaliana. Plant J 98:4607–21
    [Google Scholar]
  135. 135. 
    Szemenyei H, Hannon M, Long JA 2008. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:58681384–86
    [Google Scholar]
  136. 136. 
    Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV et al. 2007. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:7136640–45
    [Google Scholar]
  137. 137. 
    Tanaka J, Yano K, Aya K, Hirano K, Takehara S et al. 2014. Antheridiogen determines sex in ferns via a spatiotemporally split gibberellin synthesis pathway. Science 346:6208469–73
    [Google Scholar]
  138. 138. 
    Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A et al. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:7154661–65
    [Google Scholar]
  139. 139. 
    Tiwari SB, Hagen G, Guilfoyle T 2003. The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:2533–43
    [Google Scholar]
  140. 140. 
    Toh S, Holbrook-Smith D, Stogios PJ, Onopriyenko O, Lumba S et al. 2015. Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350:6257203–7
    [Google Scholar]
  141. 141. 
    Toh S, Holbrook-Smith D, Stokes ME, Tsuchiya Y, McCourt P 2014. Detection of parasitic plant suicide germination compounds using a high-throughput Arabidopsis HTL/KAI2 strigolactone perception system. Chem. Biol. 21:8988–98
    [Google Scholar]
  142. 142. 
    Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S et al. 2015. Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:6250864–68
    [Google Scholar]
  143. 143. 
    Ueda H, Kusaba M. 2015. Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 169:1138–47
    [Google Scholar]
  144. 144. 
    Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E et al. 2005. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:7059693–98
    [Google Scholar]
  145. 145. 
    Ulmasov T, Liu ZB, Hagen G, Guilfoyle TJ 1995. Composite structure of auxin response elements. Plant Cell 7:101611–23
    [Google Scholar]
  146. 146. 
    Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T et al. 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:7210195–200
    [Google Scholar]
  147. 147. 
    Urbanova T, Leubner-Metzger G. 2016. Gibberellins and seed germination. The Gibberellins, Annual Plant Reviews P Hedden, SG Thomas 253–84 Chichester, UK: Wiley
    [Google Scholar]
  148. 148. 
    Végh A, Incze N, Fábián A, Huo H, Bradford KJ et al. 2017. Comprehensive analysis of DWARF14-LIKE2 (DLK2) reveals its functional divergence from strigolactone-related paralogs. Front. Plant Sci. 8:1641
    [Google Scholar]
  149. 149. 
    Villaécija-Aguilar JA, Hamon-Josse M, Carbonnel S, Kretschmar A, Schmid C et al. 2019. SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis. PLOS Genet 15:8e1008327
    [Google Scholar]
  150. 150. 
    Walker CH, Siu-Ting K, Taylor A, O'Connell MJ, Bennett T 2019. Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation. BMC Biol 17:70
    [Google Scholar]
  151. 151. 
    Wallner E-S, López-Salmerón V, Belevich I, Poschet G, Jung I et al. 2017. Strigolactone- and karrikin-independent SMXL proteins are central regulators of phloem formation. Curr. Biol. 27:81241–47
    [Google Scholar]
  152. 152. 
    Wang L, Wang B, Jiang L, Liu X, Li X et al. 2015. Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-Like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27:113128–42
    [Google Scholar]
  153. 153. 
    Wang L, Waters MT, Smith SM 2018. Karrikin-KAI2 signalling provides Arabidopsis seeds with tolerance to abiotic stress and inhibits germination under conditions unfavourable to seedling establishment. New Phytol 219:2605–18
    [Google Scholar]
  154. 154. 
    Wasternack C, Strnad M. 2016. Jasmonate signaling in plant stress responses and development—active and inactive compounds. N. Biotechnol. 33:5604–13
    [Google Scholar]
  155. 155. 
    Waters MT, Gutjahr C, Bennett T, Nelson DC 2017. Strigolactone signaling and evolution. Annu. Rev. Plant Biol. 68:291–322
    [Google Scholar]
  156. 156. 
    Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK et al. 2012. Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. . Development 139:71285–95
    [Google Scholar]
  157. 157. 
    Waters MT, Scaffidi A, Moulin SLY, Sun YK, Flematti GR, Smith SM 2015. A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27:71925–44
    [Google Scholar]
  158. 158. 
    Weijers D, Wagner D. 2016. Transcriptional responses to the auxin hormone. Annu. Rev. Plant Biol. 67:539–74
    [Google Scholar]
  159. 159. 
    Weng J-K, Ye M, Li B, Noel JP 2016. Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166:4881–93
    [Google Scholar]
  160. 160. 
    Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E et al. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. PNAS 111:45E4859–68
    [Google Scholar]
  161. 161. 
    Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN et al. 2007. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:41209–20
    [Google Scholar]
  162. 162. 
    Xie X, Yoneyama K, Kisugi T, Uchida K, Ito S et al. 2013. Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol. Plant 6:1153–63
    [Google Scholar]
  163. 163. 
    Xie X, Yoneyama K, Yoneyama K 2010. The strigolactone story. Annu. Rev. Phytopathol. 48:93–117
    [Google Scholar]
  164. 164. 
    Xu G, Ma H, Nei M, Kong H 2009. Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. PNAS 106:3835–40
    [Google Scholar]
  165. 165. 
    Xu Y, Miyakawa T, Nakamura H, Nakamura A, Imamura Y et al. 2016. Structural basis of unique ligand specificity of KAI2-like protein from parasitic weed Striga hermonthica. Sci. Rep 6:31386
    [Google Scholar]
  166. 166. 
    Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M 2014. Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:2399–408
    [Google Scholar]
  167. 167. 
    Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T et al. 2008. The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148:31189–200
    [Google Scholar]
  168. 168. 
    Yao R, Ming Z, Yan L, Li S, Wang F et al. 2016. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536:7617469–73
    [Google Scholar]
  169. 169. 
    Yao R, Wang F, Ming Z, Du X, Chen L et al. 2017. ShHTL7 is a non-canonical receptor for strigolactones in root parasitic weeds. Cell Res 27:6838–41
    [Google Scholar]
  170. 170. 
    Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP 2007. Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr. Biol. 17:141225–30
    [Google Scholar]
  171. 171. 
    Yoneyama K, Mori N, Sato T, Yoda A, Xie X et al. 2018. Conversion of carlactone to carlactonoic acid is a conserved function of MAX1 homologs in strigolactone biosynthesis. New Phytol 218:41522–33
    [Google Scholar]
  172. 172. 
    Yoneyama K, Xie X, Yoneyama K, Kisugi T, Nomura T et al. 2018. Which are the major players, canonical or non-canonical strigolactones. J. Exp. Bot. 69:92231–39
    [Google Scholar]
  173. 173. 
    Yoshida H, Tanimoto E, Hirai T, Miyanoiri Y, Mitani R et al. 2018. Evolution and diversification of the plant gibberellin receptor GID1. PNAS 115:33E7844–53
    [Google Scholar]
  174. 174. 
    Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P et al. 2014. Genetic control of plant development by overriding a geometric division rule. Dev. Cell 29:175–87
    [Google Scholar]
  175. 175. 
    Zenser N, Ellsmore A, Leasure C, Callis J 2001. Auxin modulates the degradation rate of Aux/IAA proteins. PNAS 98:2011795–800
    [Google Scholar]
  176. 176. 
    Zhang Y, Cheng X, Wang Y, Díez-Simón C, Flokova K et al. 2018. The tomato MAX1 homolog, SlMAX1, is involved in the biosynthesis of tomato strigolactones from carlactone. New Phytol 219:1297–309
    [Google Scholar]
  177. 177. 
    Zhang Y, van Dijk ADJ, Scaffidi A, Flematti GR, Hofmann M et al. 2014. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 10:121028–33
    [Google Scholar]
  178. 178. 
    Zhou F, Lin Q, Zhu L, Ren Y, Zhou K et al. 2013. D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504:7480406–10
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-050718-100309
Loading
/content/journals/10.1146/annurev-arplant-050718-100309
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error