1932

Abstract

The promotive effect of auxin on shoot cell expansion provided the bioassay used to isolate this central plant hormone nearly a century ago. While the mechanisms underlying auxin perception and signaling to regulate transcription have largely been elucidated, how auxin controls cell expansion is only now attaining molecular-level definition. The good news is that the decades-old acid growth theory invoking plasma membrane H+-ATPase activation is still useful. The better news is that a mechanistic framework has emerged, wherein Small Auxin Up RNA (SAUR) proteins regulate protein phosphatases to control H+-ATPase activity. In this review, we focus on rapid auxin effects, their relationship to H+-ATPase activation and other transporters, and dependence on TIR1/AFB signaling. We also discuss how some observations, such as near-instantaneous effects on ion transport and root growth, do not fit into a single, comprehensive explanation of how auxin controls cell expansion, and where more research is warranted.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-073019-025907
2020-04-29
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-073019-025907.html?itemId=/content/journals/10.1146/annurev-arplant-073019-025907&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abel S, Oeller PW, Theologis A 1994. Early auxin-induced genes encode short-lived nuclear proteins. PNAS 91:326–30
    [Google Scholar]
  2. 2. 
    Abel S, Theologis A. 1996. Early genes and auxin action. Plant Physiol 111:9–17
    [Google Scholar]
  3. 3. 
    Adamowski M, Li L, Friml J 2019. Reorientation of cortical microtubule arrays in the hypocotyl of Arabidopsis thaliana is induced by the cell growth process and independent of auxin signaling. Int. J. Mol. Sci. 20:e3337
    [Google Scholar]
  4. 4. 
    Andres-Robin A, Reymond MC, Dupire A, Battu V, Dubrulle N et al. 2018. Evidence for the regulation of gynoecium morphogenesis by ETTIN via cell wall dynamics. Plant Physiol 178:1222–32
    [Google Scholar]
  5. 5. 
    Arsuffi G, Braybrook SA. 2018. Acid growth: an ongoing trip. J. Exp. Bot. 69:137–46
    [Google Scholar]
  6. 6. 
    Barbez E, Dünser K, Gaidora A, Lendl T, Busch W 2017. Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. PNAS 114:E4884–93Demonstrates that auxin-mediated apoplastic acidification promotes root cell elongation and high auxin levels trigger FERONIA-dependent root apoplastic alkalization.
    [Google Scholar]
  7. 7. 
    Baskin TI. 2015. Auxin inhibits expansion rate independently of cortical microtubules. Trends Plant Sci 20:471–72
    [Google Scholar]
  8. 8. 
    Bates GW, Goldsmith MH. 1983. Rapid response of the plasma-membrane potential in oat coleoptiles to auxin and other weak acids. Planta 159:231–37
    [Google Scholar]
  9. 9. 
    Becker D, Hedrich R. 2002. Channelling auxin action: modulation of ion transport by indole-3-acetic acid. Auxin Molecular Biology C Perrot-Rechenmann, G Hagen 349–56 Dordrecht, Neth.: Springer Neth.
    [Google Scholar]
  10. 10. 
    Béziat C, Kleine-Vehn J. 2018. The road to auxin-dependent growth repression and promotion in apical hooks. Curr. Biol. 28:R519–25
    [Google Scholar]
  11. 11. 
    Calderón Villalobos LI, 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. 8:477–85
    [Google Scholar]
  12. 12. 
    Cao M, Chen R, Li P, Yu Y, Zheng R et al. 2019. TMK1-mediated auxin signalling regulates differential growth of the apical hook. Nature 568:240–43Demonstrates auxin-dependent cleavage of the TMK1 kinase domain and its regulation of noncanonical Aux/IAAs during apical hook development.
    [Google Scholar]
  13. 13. 
    Chae K, Isaacs CG, Reeves PH, Maloney GS, Muday GK et al. 2012. Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J 71:684–97
    [Google Scholar]
  14. 14. 
    Chen X, Grandont L, Li H, Hauschild R, Paque S et al. 2014. Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules. Nature 516:90–93
    [Google Scholar]
  15. 15. 
    Chen Y, Hao X, Cao J 2014. Small auxin upregulated RNA (SAUR) gene family in maize: identification, evolution, and its phylogenetic comparison with Arabidopsis, rice, and sorghum. J. Integr. Plant Biol. 56:133–50
    [Google Scholar]
  16. 16. 
    Cleland R. 1971. Instability of the growth-limiting proteins of the Avena coleoptile and their pool size in relation to auxin. Planta 99:1–11
    [Google Scholar]
  17. 17. 
    Cleland R. 1973. Auxin-induced hydrogen ion excretion from Avena coleoptiles. PNAS 70:3092–93
    [Google Scholar]
  18. 18. 
    Cleland RE. 1975. Auxin-induced hydrogen ion excretion: correlation with growth, and control by external pH and water stress. Planta 127:233–42
    [Google Scholar]
  19. 19. 
    Cleland RE. 1976. Fusicoccin-induced growth and hydrogen ion excretion in Avena coleoptiles: relation to auxin responses. Planta 128:201–6
    [Google Scholar]
  20. 20. 
    Cosgrove DJ. 2005. Growth of the plant cell wall. Nat. Rev. Mol. Cell Biol. 6:850–61
    [Google Scholar]
  21. 21. 
    Cosgrove DJ. 2015. Plant expansins: diversity and interactions with plant cell walls. Curr. Opin. Plant Biol. 25:162–72
    [Google Scholar]
  22. 22. 
    Dahlke RI, Fraas S, Ullrich KK, Heinemann K, Romeiks M et al. 2017. Protoplast swelling and hypocotyl growth depend on different auxin signaling pathways. Plant Physiol 175:982–94
    [Google Scholar]
  23. 23. 
    Dai N, Wang W, Patterson SE, Bleecker AB 2013. The TMK subfamily of receptor-like kinases in Arabidopsis display an essential role in growth and a reduced sensitivity to auxin. PLOS ONE 8:e60990
    [Google Scholar]
  24. 24. 
    Darwin C, Darwin FE. 1880. The Power of Movement in Plants New York: D. Appleton
  25. 25. 
    del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C 2006. The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18:2224–35
    [Google Scholar]
  26. 26. 
    Dharmasiri N, Dharmasiri S, Estelle M 2005. The F-box protein TIR1 is an auxin receptor. Nature 435:441–45
    [Google Scholar]
  27. 27. 
    Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M et al. 2005. Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9:109–19
    [Google Scholar]
  28. 28. 
    Dindas J, Scherzer S, Roelfsema MRG, von Meyer K, Müller HM et al. 2018. AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type Ca2+ signaling. Nat. Commun. 9:1174Demonstrates that IAA influx triggers Ca2+-coupled depolarization in root hairs and this response is diminished in tir1/afb and cngc14 mutants.
    [Google Scholar]
  29. 29. 
    Dreher KA, Brown J, Saw RE, Callis J 2006. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 18:699–714
    [Google Scholar]
  30. 30. 
    Dünser K, Gupta S, Herger A, Feraru MI, Ringli C, Kleine-Vehn J 2019. Extracellular matrix sensing by FERONIA and Leucine-Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. EMBO J 38:e100353
    [Google Scholar]
  31. 31. 
    Evans ML. 1976. A new sensitive root auxanometer: preliminary studies of the interaction of auxin and acid pH in the regulation of intact root elongation. Plant Physiol 58:599–601
    [Google Scholar]
  32. 32. 
    Evans ML, Ishikawa H, Estelle MA 1994. Responses of Arabidopsis roots to auxin studies with high temporal resolution: Comparison of wild type and auxin-response mutants. Planta 194:215–22
    [Google Scholar]
  33. 33. 
    Felle H, Peters W, Palme K 1991. The electrical response of maize to auxins. Biochim. Biophys. Acta Biomembr. 1064:199–204
    [Google Scholar]
  34. 34. 
    Fendrych M, Akhmanova M, Merrin J, Glanc M, Hagihara S et al. 2018. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants 4:453–59Reveals rapid nontranscriptional roles of the TIR1/AFB receptor system in auxin-mediated root growth inhibition.
    [Google Scholar]
  35. 35. 
    Fendrych M, Leung J, Friml J 2016. TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife 5:e19048Together with Reference 115, reveals that constitutive GFP-SAUR19 expression confers auxin-independent hypocotyl elongation and apoplastic acidification.
    [Google Scholar]
  36. 36. 
    Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V et al. 2018. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28:666–75.e5
    [Google Scholar]
  37. 37. 
    Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK et al. 2011. Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. PNAS 108:20231–35
    [Google Scholar]
  38. 38. 
    Frias I, Caldeira MT, Perez-Castineira JR, Navarro-Avino JP, Culianez-Macia FA et al. 1996. A major isoform of the maize plasma membrane H+-ATPase: characterization and induction by auxin in coleoptiles. Plant Cell 8:1533–44
    [Google Scholar]
  39. 39. 
    Fuglsang AT, Visconti S, Drumm K, Jahn T, Stensballe A et al. 1999. Binding of 14–3–3 protein to the plasma membrane H+-ATPase AHA2 involves the three C-terminal residues Tyr946-Thr-Val and requires phosphorylation of Thr947. J. Biol. Chem. 274:36774–80
    [Google Scholar]
  40. 40. 
    Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y 2015. Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. PNAS 112:2275–80
    [Google Scholar]
  41. 41. 
    Gjetting KS, Ytting CK, Schulz A, Fuglsang AT 2012. Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J. Exp. Bot. 63:3207–18
    [Google Scholar]
  42. 42. 
    Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M 2001. Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–76
    [Google Scholar]
  43. 43. 
    Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M 1998. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. PNAS 95:7197–202
    [Google Scholar]
  44. 44. 
    Hager A, Debus G, Edel HG, Stransky H, Serrano R 1991. Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane H+-ATPase. Planta 185:527–37
    [Google Scholar]
  45. 45. 
    Hager A, Menzel H, Krauss A 1971. Experiments and hypothesis concerning the primary action of auxin in elongation growth. Planta 100:47–75
    [Google Scholar]
  46. 46. 
    Harmer SL, Brooks CJ. 2018. Growth-mediated plant movements: hidden in plain sight. Curr. Opin. Plant Biol. 41:89–94
    [Google Scholar]
  47. 47. 
    Haruta M, Gray WM, Sussman MR 2015. Regulation of the plasma membrane proton pump (H+-ATPase) by phosphorylation. Curr. Opin. Plant Biol. 28:68–75
    [Google Scholar]
  48. 48. 
    Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR 2014. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–11
    [Google Scholar]
  49. 49. 
    Hayashi K, Neve J, Hirose M, Kuboki A, Shimada Y et al. 2012. Rational design of an auxin antagonist of the SCFTIR1 auxin receptor complex. ACS Chem. Biol. 7:590–98
    [Google Scholar]
  50. 50. 
    Hayashi Y, Nakamura S, Takemiya A, Takahashi Y, Shimazaki K, Kinoshita T 2010. Biochemical characterization of in vitro phosphorylation and dephosphorylation of the plasma membrane H+-ATPase. Plant Cell Physiol 51:1186–96
    [Google Scholar]
  51. 51. 
    Hocq L, Pelloux J, Lefebvre V 2017. Connecting homogalacturonan-type pectin remodeling to acid growth. Trends Plant Sci 22:20–29
    [Google Scholar]
  52. 52. 
    Jain M, Tyagi AK, Khurana JP 2006. Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics 88:360–71
    [Google Scholar]
  53. 53. 
    Jelich-Ottmann C, Weiler EW, Oecking C 2001. Binding of regulatory 14–3–3 proteins to the C terminus of the plant plasma membrane H+-ATPase involves part of its autoinhibitory region. J. Biol. Chem. 276:39852–57
    [Google Scholar]
  54. 54. 
    Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ et al. 2009. Auxin transport through non-hair cells sustains root-hair development. Nat. Cell Biol. 11:78–84
    [Google Scholar]
  55. 55. 
    Jurado S, Abraham Z, Manzano C, López-Torrejón G, Pacios LF, Del Pozo JC 2010. The Arabidopsis cell cycle F-box protein SKP2A binds to auxin. Plant Cell 22:3891–904
    [Google Scholar]
  56. 56. 
    Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud JL, Boutry M 2005. Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14–3–3 proteins converts a dimer into a hexamer. PNAS 102:11675–80
    [Google Scholar]
  57. 57. 
    Kepinski S, Leyser O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–51
    [Google Scholar]
  58. 58. 
    Kinoshita T, Nishimura M, Shimazaki K 1995. Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of Fava bean. Plant Cell 7:1333–42
    [Google Scholar]
  59. 59. 
    Kinoshita T, Shimazaki K. 1999. Blue light activates the plasma membrane H+-ATPase by phosphorylation of the C-terminus in stomatal guard cells. EMBO J 18:5548–58
    [Google Scholar]
  60. 60. 
    Knauss S, Rohrmeier T, Lehle L 2003. The auxin-induced maize gene ZmSAUR2 encodes a short-lived nuclear protein expressed in elongating tissues. J. Biol. Chem. 278:23936–43
    [Google Scholar]
  61. 61. 
    Kutschera U. 1994. The current status of the acid-growth hypothesis. New Phytol 126:549–69
    [Google Scholar]
  62. 62. 
    Kutschera U, Briggs WR. 1987. Rapid auxin-induced stimulation of cell wall synthesis in pea internodes. PNAS 84:2747–51
    [Google Scholar]
  63. 63. 
    Kutschera U, Niklas KJ. 2007. The epidermal-growth-control theory of stem elongation: an old and a new perspective. J. Plant Physiol. 164:1395–409
    [Google Scholar]
  64. 64. 
    Kutschera U, Schopfer P. 1985. Evidence against the acid-growth theory of auxin action. Planta 163:483–93
    [Google Scholar]
  65. 65. 
    Kutschera U, Schopfer P. 1986. Effect of auxin and abscisic acid on cell wall extensibility in maize coleoptiles. Planta 167:527–35
    [Google Scholar]
  66. 66. 
    Lee RD, Cho HT. 2013. Auxin, the organizer of the hormonal/environmental signals for root hair growth. Front. Plant Sci. 4:448
    [Google Scholar]
  67. 67. 
    Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M 1993. Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161–64
    [Google Scholar]
  68. 68. 
    Leyser HM, Pickett FB, Dharmasiri S, Estelle M 1996. Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. Plant J 10:403–13
    [Google Scholar]
  69. 69. 
    Liao H, Tang R, Zhang X, Luan S, Yu F 2017. FERONIA receptor kinase at the crossroads of hormone signaling and stress responses. Plant Cell Physiol 58:1143–50
    [Google Scholar]
  70. 70. 
    Lockhart JA. 1965. An analysis of irreversible plant cell elongation. J. Theor. Biol. 8:264–75
    [Google Scholar]
  71. 71. 
    Löfke C, Dünser K, Scheuring D, Kleine-Vehn J 2015. Auxin regulates SNARE-dependent vacuolar morphology restricting cell size. eLife 4:e05868
    [Google Scholar]
  72. 72. 
    Majda M, Robert S. 2018. The role of auxin in cell wall expansion. Int. J. Mol. Sci. 19:E951
    [Google Scholar]
  73. 73. 
    Marre E. 1979. Fusicoccin: A tool in plant physiology. Annu. Rev. Plant Physiol. 30:273–88
    [Google Scholar]
  74. 74. 
    Marten I, Lohse G, Hedrich R 1991. Plant growth hormones control voltage-dependent activity of anion channels in plasma membrane of guard cells. Nature 353:758–62
    [Google Scholar]
  75. 75. 
    Masuda Y, Yamamoto R. 1972. Control of auxin-induced stem elongation by the epidermis. Physiol. Plant. 27:109–15
    [Google Scholar]
  76. 76. 
    McClure BA, Guilfoyle T. 1987. Characterization of a class of small auxin-inducible soybean polyadenylated RNAs. Plant Mol. Biol. 9:611–23
    [Google Scholar]
  77. 77. 
    McClure BA, Hagen G, Brown CS, Gee MA, Guilfoyle TJ 1989. Transcription, organization, and sequence of an auxin-regulated gene cluster in soybean. Plant Cell 1:229–39
    [Google Scholar]
  78. 78. 
    McQueen-Mason S, Durachko DM, Cosgrove DJ 1992. Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4:1425–33
    [Google Scholar]
  79. 79. 
    Merlot S, Leonhardt N, Fenzi F, Valon C, Costa M et al. 2007. Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J 26:3216–26
    [Google Scholar]
  80. 80. 
    Moloney MM, Elliott MC, Cleland RE 1981. Acid growth effects in maize roots: evidence for a link between auxin-economy and proton extrusion in the control of root growth. Planta 152:285–91
    [Google Scholar]
  81. 81. 
    Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S 2009. Ca2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21:2341–56
    [Google Scholar]
  82. 82. 
    Monshausen GB, Miller ND, Murphy AS, Gilroy S 2011. Dynamics of auxin-dependent Ca2+ and pH signaling in root growth revealed by integrating high-resolution imaging with automated computer vision-based analysis. Plant J 65:309–18
    [Google Scholar]
  83. 83. 
    Nemhauser JL, Feldman LJ, Zambryski PC 2000. Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127:3877–88
    [Google Scholar]
  84. 84. 
    Nishitani K, Vissenberg K. 2007. Roles of the XTH protein family in the expanding cell. The Expanding Cell JP Verbelen, K Vissenberg 89–116 Heidelberg, Ger: Springer-Verlag
    [Google Scholar]
  85. 85. 
    Olsson A, Svennelid F, Ek B, Sommarin M, Larsson C 1998. A phosphothreonine residue at the C-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14–3–3 binding. Plant Physiol 118:551–55
    [Google Scholar]
  86. 86. 
    Owens T, Poole RJ. 1979. Regulation of cytoplasmic and vacuolar volumes by plant cells in suspension culture. Plant Physiol 64:900–4
    [Google Scholar]
  87. 87. 
    Pacheco-Villalobos D, Díaz-Moreno SM, van der Schuren A, Tamaki T, Kang YH et al. 2016. The effects of high steady state auxin levels on root cell elongation in Brachypodium. Plant Cell 28:1009–24
    [Google Scholar]
  88. 88. 
    Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD et al. 2005. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–56
    [Google Scholar]
  89. 89. 
    Paponov IA, Teale W, Lang D, Paponov M, Reski R et al. 2009. The evolution of nuclear auxin signalling. BMC Evol. Biol. 9:126
    [Google Scholar]
  90. 90. 
    Philippar K, Fuchs I, Luthen H, Hoth S, Bauer CS et al. 1999. Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism. PNAS 96:12186–91
    [Google Scholar]
  91. 91. 
    Philippar K, Ivashikina N, Ache P, Christian M, Luthen H et al. 2004. Auxin activates KAT1 and KAT2, two K+-channel genes expressed in seedlings of Arabidopsis thaliana. Plant J 37:815–27
    [Google Scholar]
  92. 92. 
    Pitts RJ, Cernac A, Estelle M 1998. Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–60
    [Google Scholar]
  93. 93. 
    Procko C, Burko Y, Jaillais Y, Ljung K, Long JA, Chory J 2016. The epidermis coordinates auxin-induced stem growth in response to shade. Genes Dev 30:1529–41
    [Google Scholar]
  94. 94. 
    Quint M, Ito H, Zhang W, Gray WM 2005. Characterization of a novel temperature-sensitive allele of the CUL1/AXR6 subunit of SCF ubiquitin-ligases. Plant J 43:371–83
    [Google Scholar]
  95. 95. 
    Rayle DL. 1973. Auxin-induced hydrogen-ion secretion in Avena coleoptiles and its implications. Planta 114:63–73
    [Google Scholar]
  96. 96. 
    Rayle DL, Cleland R. 1970. Enhancement of wall loosening and elongation by acid solutions. Plant Physiol 46:250–53
    [Google Scholar]
  97. 97. 
    Rayle DL, Cleland RE. 1980. Evidence that auxin-induced growth of soybean hypocotyls involves proton excretion. Plant Physiol 66:433–37
    [Google Scholar]
  98. 98. 
    Rayle DL, Cleland RE. 1992. The Acid Growth Theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–74
    [Google Scholar]
  99. 99. 
    Ren H, Gray WM. 2015. SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol. Plant 8:1153–64
    [Google Scholar]
  100. 100. 
    Ren H, Park MY, Spartz AK, Wong JH, Gray WM 2018. A subset of plasma membrane-localized PP2C.D phosphatases negatively regulate SAUR-mediated cell expansion in Arabidopsis. PLOS Genet 14:e1007455Identifies PP2C.D2/D5/D6 as the primary effectors of PM-localized SAURs that regulate PM H+-ATPase phosphorylation/activity.
    [Google Scholar]
  101. 101. 
    Ruck A, Palme K, Venis MA, Napier RM, Felle HH 1993. Patch-clamp analysis establishes a role for an auxin binding protein in the auxin stimulation of plasma membrane current in Zea mays protoplasts. Plant J 4:41–46
    [Google Scholar]
  102. 102. 
    Ruegger M, Dewey E, Gray WM, Hobbie L, Turner J, Estelle M 1998. The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast Grr1p. Genes Dev 12:198–207
    [Google Scholar]
  103. 103. 
    Sachs J, Vines SH. 1882. Text-Book of Botany, Morphological and Physiological Oxford, UK: Clarendon
  104. 104. 
    Salehin M, Bagchi R, Estelle M 2015. SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27:9–19
    [Google Scholar]
  105. 105. 
    Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC 2016. Leaf epinasty and auxin: a biochemical and molecular overview. Plant Sci 253:187–93
    [Google Scholar]
  106. 106. 
    Scheitz K, Lüthen H, Schenck D 2013. Rapid auxin-induced root growth inhibition requires the TIR and AFB auxin receptors. Planta 238:1171–76
    [Google Scholar]
  107. 107. 
    Schenck D, Christian M, Jones A, Lüthen H 2010. Rapid auxin-induced cell expansion and gene expression: a four-decade-old question revisited. Plant Physiol 152:1183–85
    [Google Scholar]
  108. 108. 
    Scheuring D, Löfke C, Krüger F, Kittelmann M, Eisa A et al. 2016. Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression. PNAS 113:452–57
    [Google Scholar]
  109. 109. 
    Schopfer P. 1989. pH-dependence of extension growth in Avena coleoptiles and its implications for the mechanism of auxin action. Plant Physiol 90:202–7
    [Google Scholar]
  110. 110. 
    Shih HW, DePew CL, Miller ND, Monshausen GB 2015. The cyclic nucleotide-gated channel CNGC14 regulates root gravitropism in Arabidopsis thaliana. Curr. Biol 25:3119–25The cyclic nucleotide-gated channel, CNGC14, is required for rapid Ca2+ signaling and extracellular alkalization following gravitropic stimulation of roots.
    [Google Scholar]
  111. 111. 
    Shih HW, Miller ND, Dai C, Spalding EP, Monshausen GB 2014. The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24:1887–92
    [Google Scholar]
  112. 112. 
    Simonini S, Bencivenga S, Trick M, Østergaard L 2017. Auxin-induced modulation of ETTIN activity orchestrates gene expression in Arabidopsis. Plant Cell 29:1864–82
    [Google Scholar]
  113. 113. 
    Simonini S, Deb J, Moubayidin L, Stephenson P, Valluru M et al. 2016. A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis. Genes Dev 30:2286–96 Corrigendum. 2017 Genes Dev 31:1821
    [Google Scholar]
  114. 114. 
    Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H et al. 2012. The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70:978–90
    [Google Scholar]
  115. 115. 
    Spartz AK, Lor VS, Ren H, Olszewski NE, Miller ND et al. 2017. Constitutive expression of Arabidopsis SMALL AUXIN UP RNA19 (SAUR19) in tomato confers auxin-independent hypocotyl elongation. Plant Physiol 173:1453–62Demonstrates that constitutive GFP-SAUR19 expression confers increased cell wall extensibility and, together with Reference 35, auxin-independent hypocotyl elongation.
    [Google Scholar]
  116. 116. 
    Spartz AK, Ren H, Park MY, Grandt KN, Lee SH et al. 2014. SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26:2129–42Identifies SAUR-PP2C.D regulatory modules that modulate PM H+-ATPase phosphorylation/activity to regulate auxin-responsive cell expansion.
    [Google Scholar]
  117. 117. 
    Stamm P, Kumar PP. 2013. Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light. Plant Cell Rep 32:759–69
    [Google Scholar]
  118. 118. 
    Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY et al. 2008. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–91
    [Google Scholar]
  119. 119. 
    Stortenbeker N, Bemer M. 2019. The SAUR gene family: the plant's toolbox for adaptation of growth and development. J. Exp. Bot. 70:17–27
    [Google Scholar]
  120. 120. 
    Sun N, Wang J, Gao Z, Dong J, He H et al. 2016. Arabidopsis SAURs are critical for differential light regulation of the development of various organs. PNAS 113:6071–76
    [Google Scholar]
  121. 121. 
    Svennelid F, Olsson A, Piotrowski M, Rosenquist M, Ottman C et al. 1999. Phosphorylation of Thr-948 at the C terminus of the plasma membrane H+-ATPase creates a binding site for the regulatory 14–3–3 protein. Plant Cell 11:2379–91
    [Google Scholar]
  122. 122. 
    Szemenyei H, Hannon M, Long JA 2008. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–86
    [Google Scholar]
  123. 123. 
    Takahashi K, Hayashi K, Kinoshita T 2012. Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol 159:632–41Demonstrates auxin-induced increases in PM H+-ATPase C-terminal phosphorylation.
    [Google Scholar]
  124. 124. 
    Talbott LD, Ray PM. 1992. Changes in molecular size of previously deposited and newly synthesized pea cell wall matrix polysaccharides: effects of auxin and turgor. Plant Physiol 98:369–79
    [Google Scholar]
  125. 125. 
    Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV et al. 2007. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–45
    [Google Scholar]
  126. 126. 
    Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F et al. 2008. Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–76
    [Google Scholar]
  127. 127. 
    Tovar-Mendez A, Miernyk JA, Hoyos E, Randall DD 2014. A functional genomic analysis of Arabidopsis thaliana PP2C clade D. Protoplasma 251:265–71
    [Google Scholar]
  128. 128. 
    Uchida N, Takahashi K, Iwasaki R, Yamada R, Yoshimura M et al. 2018. Chemical hijacking of auxin signaling with an engineered auxin-TIR1 pair. Nat. Chem. Biol. 14:299–305Develops a synthetic auxin receptor system to demonstrate conclusively that TIR1/AFB receptors mediate acid growth.
    [Google Scholar]
  129. 129. 
    Vanhaeren H, Gonzalez N, Coppens F, De Milde L, Van Daele T et al. 2014. Combining growth-promoting genes leads to positive epistasis in Arabidopsis thaliana. eLife 3:e02252
    [Google Scholar]
  130. 130. 
    Vi SL, Trost G, Lange P, Czesnick H, Rao N et al. 2013. Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response. PNAS 110:13994–99
    [Google Scholar]
  131. 131. 
    Walsh TA, Neal R, Merlo AO, Honma M, Hicks GR et al. 2006. Mutations in an auxin receptor homolog AFB5 and in SGT1b confer resistance to synthetic picolinate auxins and not to 2,4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis. Plant Physiol 142:542–52
    [Google Scholar]
  132. 132. 
    Wang Z, Yang L, Liu Z, Lu M, Wang M et al. 2019. Natural variations of growth thermo-responsiveness determined by SAUR26/27/28 proteins in Arabidopsis thaliana. New Phytol 224:291–305
    [Google Scholar]
  133. 133. 
    Weijers D, Wagner D. 2016. Transcriptional responses to the auxin hormone. Annu. Rev. Plant Biol. 67:539–74
    [Google Scholar]
  134. 134. 
    Went FW. 1926. On growth accelerating substances in the coleoptile of Avena sativa. Proc. Kon. Akad. Wetensch 30:10–19
    [Google Scholar]
  135. 135. 
    Wildman SG. 1997. The auxin-A, B enigma: scientific fraud or scientific ineptitude. Plant Growth Regul 22:37–68
    [Google Scholar]
  136. 136. 
    Wong JH, Spartz AK, Park MY, Du M, Gray WM 2019. Mutation of a conserved motif of PP2C.D phosphatases confers SAUR immunity and constitutive activity. Plant Physiol 181:353–66
    [Google Scholar]
  137. 137. 
    Wu G, Cameron JN, Ljung K, Spalding EP 2010. A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and phytochrome B. Plant J 62:179–91
    [Google Scholar]
  138. 138. 
    Wu J, Liu S, He Y, Guan X, Zhu X et al. 2012. Genome-wide analysis of SAUR gene family in Solanaceae species. Gene 509:38–50
    [Google Scholar]
  139. 139. 
    Würtele M, Jelich-Ottmann C, Wittinghofer A, Oecking C 2003. Structural view of a fungal toxin acting on a 14–3–3 regulatory complex. EMBO J 22:987–94
    [Google Scholar]
  140. 140. 
    Xia L, Marquès-Bueno MM, Bruce CG, Karnik RA 2019. Unusual roles of secretory SNARE SYP132 in plasma membrane H+-ATPase traffic and vegetative plant growth. Plant Physiol 180:837–58
    [Google Scholar]
  141. 141. 
    Yang T, Poovaiah BW. 2000. Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J. Biol. Chem. 275:3137–43
    [Google Scholar]
  142. 142. 
    Žádníková P, Wabnik K, Abuzeineh A, Gallemi M, Van Der Straeten D et al. 2016. A model of differential growth-guided apical hook formation in plants. Plant Cell 28:2464–77
    [Google Scholar]
  143. 143. 
    Zimmermann S, Thomine S, Guern J, Barbier-Brygoo H 1994. An anion current at the plasma membrane of tobacco protoplasts shows ATP-dependent voltage regulation and is modulated by auxin. Plant J 6:707–16
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-073019-025907
Loading
/content/journals/10.1146/annurev-arplant-073019-025907
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