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Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light

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Abstract

Key message

The Arabidopsis SAUR36 , renamed RAG1 , integrates auxin and gibberellin signals to regulate apical hook maintenance in etiolated seedlings, hypocotyl elongation in the light and fertility.

Abstract

Phytohormone signalling intermediates integrate responses to developmental cues and the variety of environmental inputs thereby governing all aspects of plant growth and development. At the genetic level, interactions of different phytohormone signalling pathways lead to the regulation of overlapping sets of target genes. We have characterised SMALL AUXIN UP RNA 36 (SAUR36, At2g45210) whose expression is induced by auxins and repressed by gibberellins. Its expression appears to be restricted to elongating tissues. Germination responses to treatments with paclobutrazol and exogenous abscisic acid were affected in knock-out, knock-down as well as ectopic expression lines. At later stages of development, however, transgenic plants with reduced levels of SAUR36 expression appeared similar to wild-type plants, while ectopic expression of SAUR36 led to the absence of apical hooks in etiolated seedlings and longer hypocotyls in light-grown seedlings. Mature plants ectopically expressing SAUR36 further displayed strongly reduced fertility and wavy growth of inflorescence axes, the latter of which could be linked to defects in auxin transport. Taken together, our data suggest that SAUR36 plays a role in the regulation of seed germination by gibberellins and abscisic acid, light-dependent hypocotyl elongation as well as apical hook formation or maintenance. Therefore, we propose that it could act as one of the converging points of auxin and gibberellin signal integration in controlling key plant developmental events. Hence, we named the gene RESPONSE TO AUXINS AND GIBBERELLINS 1 (RAG1).

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Abbreviations

IAA:

Indole-3-acetic acid

NPA:

1-N-Naphthylphthalamic acid

PAC:

Paclobutrazol

SAUR:

SMALL AUXIN UP RNA

AmiR:

Artificial microRNA

RAG1:

RESPONSE TO AUXINS AND GIBBERELLINS1

References

  • Bailly A, Sovero V, Vincenzetti V, Santelia D, Bartnik D, Koenig BW, Mancuso S, Martinoia E, Geisler M (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817–21826

    Article  PubMed  CAS  Google Scholar 

  • Bouchard R, Bailly A, Blakeslee JJ, Oehring SC, Vincenzetti V, Lee OR, Paponov I, Palme K, Mancuso S, Murphy AS, Schulz B, Geisler M (2006) Immunophilin-like TWISTED DWARF1 modulates auxin efflux activities of Arabidopsis P-glycoproteins. J Biol Chem 281:30603–30612

    Article  PubMed  CAS  Google Scholar 

  • Cadman CS, Toorop PE, Hilhorst HW, Finch-Savage WE (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J 46:805–822

    Article  PubMed  CAS  Google Scholar 

  • Cao D, Cheng H, Wu W, Soo HM, Peng J (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142:509–525

    Article  PubMed  CAS  Google Scholar 

  • Chae K, Isaacs CG, Reeves PH, Maloney GS, Muday GK, Nagpal P, Reed JW (2012) Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J 71:684–697

    Article  PubMed  CAS  Google Scholar 

  • Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • de Jong M, Wolters-Arts M, Garcia-Martinez JL, Mariani C, Vriezen WH (2011) The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signalling during tomato fruit set and development. J Exp Bot 62:617–626

    Article  PubMed  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559

    Article  PubMed  CAS  Google Scholar 

  • Frigerio M, Alabadi D, Perez-Gomez J, Garcia-Carcel L, Phillips AL, Hedden P, Blazquez MA (2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiol 142:553–563

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  PubMed  CAS  Google Scholar 

  • Gao XH, Xiao SL, Yao QF, Wang YJ, Fu XD (2011) An updated GA signaling ‘relief of repression’ regulatory model. Mol Plant 4:601–606

    Article  PubMed  CAS  Google Scholar 

  • Gee MA, Hagen G, Guilfoyle TJ (1991) Tissue-specific and organ-specific expression of soybean auxin-responsive transcripts GH3 and SAURs. Plant Cell 3:419–430

    PubMed  CAS  Google Scholar 

  • Geisler M, Kolukisaoglu HU, Bouchard R, Billion K, Berger J, Saal B, Frangne N, Koncz-Kalman Z, Koncz C, Dudler R, Blakeslee JJ, Murphy AS, Martinoia E, Schulz B (2003) TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19. Mol Biol Cell 14:4238–4249

    Article  PubMed  CAS  Google Scholar 

  • Gil P, Green PJ (1997) Regulatory activity exerted by the SAUR-AC1 promoter region in transgenic plants. Plant Mol Biol 34:803–808

    Article  PubMed  CAS  Google Scholar 

  • Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385

    Article  PubMed  CAS  Google Scholar 

  • Hartweck LM (2008) Gibberellin signaling. Planta 229:1–13

    Article  PubMed  CAS  Google Scholar 

  • Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645

    Article  PubMed  CAS  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Hagen G, Guilfoyle TJ (1991) An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3:1167–1175

    PubMed  CAS  Google Scholar 

  • Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007) Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development 134:1901–1910

    Article  PubMed  CAS  Google Scholar 

  • McClure BA, Guilfoyle T (1989) Rapid redistribution of auxin-regulated RNAs during gravitropism. Science 243:91–93

    Article  PubMed  CAS  Google Scholar 

  • Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475

    Article  PubMed  CAS  Google Scholar 

  • Park J-E, Kim Y-S, Yoon H-K, Park C-M (2007) Functional characterization of a small auxin-up RNA gene in apical hook development in Arabidopsis. Plant Sci 172:150–157

    Article  CAS  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675

    Article  CAS  Google Scholar 

  • Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18:1121–1133

    Article  PubMed  CAS  Google Scholar 

  • Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12:57–62

    Article  PubMed  CAS  Google Scholar 

  • Spartz AK, Lee SH, Wenger JP, Gonzalez N, Itoh H, Inzé D, Peer WA, Murphy AS, Overvoorde PJ, Gray WM (2012) The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion. Plant J 70:978–990

    Article  PubMed  CAS  Google Scholar 

  • Stamm P, Ravindran P, Mohanty B, Tan EL, Yu H, Kumar PP (2012) Insights into the molecular mechanism of RGL2-mediated inhibition of seed germination in Arabidopsis thaliana. BMC Plant Biol 12:179

    Article  PubMed  CAS  Google Scholar 

  • Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jurgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191

    Article  PubMed  CAS  Google Scholar 

  • Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223

    Article  PubMed  CAS  Google Scholar 

  • Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Dhonukshe P, Brewer P, Friml J (2006) Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci 63:2738–2754

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballare CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

    Article  PubMed  CAS  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    Article  PubMed  CAS  Google Scholar 

  • Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487

    Article  PubMed  CAS  Google Scholar 

  • Vert G, Chory J (2011) Crosstalk in cellular signaling: background noise or the real thing? Dev Cell 21:985–991

    Article  PubMed  CAS  Google Scholar 

  • Willige BC, Isono E, Richter R, Zourelidou M, Schwechheimer C (2011) Gibberellin regulates PIN-FORMED abundance and is required for auxin transport-dependent growth and development in Arabidopsis thaliana. Plant Cell 23:2184–2195

    Article  PubMed  CAS  Google Scholar 

  • Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317

    Article  PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Otegui MS, Spalding EP (2010) The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. Plant Cell 22:3295–3304

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251

    Article  PubMed  CAS  Google Scholar 

  • Yu H, Ito T, Wellmer F, Meyerowitz EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36:157–161

    Article  PubMed  CAS  Google Scholar 

  • Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun TP (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This project was partially supported by grant number R-154-000-154-720 from the National University of Singapore (NUS). PS was recipient of research scholarship from NUS.

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The authors declare no conflict of interest.

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Correspondence to Prakash P. Kumar.

Additional information

Communicated by P. Lakshmanan.

A contribution to the Special Issue: Plant Hormone Signalling.

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Stamm, P., Kumar, P.P. Auxin and gibberellin responsive Arabidopsis SMALL AUXIN UP RNA36 regulates hypocotyl elongation in the light. Plant Cell Rep 32, 759–769 (2013). https://doi.org/10.1007/s00299-013-1406-5

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