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
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
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
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
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
Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285
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
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
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
Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373
Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445
Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559
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
Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743
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
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
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
Gil P, Green PJ (1997) Regulatory activity exerted by the SAUR-AC1 promoter region in transgenic plants. Plant Mol Biol 34:803–808
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol 49:373–385
Hartweck LM (2008) Gibberellin signaling. Planta 229:1–13
Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645
Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451
Li Y, Hagen G, Guilfoyle TJ (1991) An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3:1167–1175
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
McClure BA, Guilfoyle T (1989) Rapid redistribution of auxin-regulated RNAs during gravitropism. Science 243:91–93
Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126:467–475
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
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675
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
Schwechheimer C, Willige BC (2009) Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 12:57–62
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
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
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
Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55:197–223
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
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
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
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
Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487
Vert G, Chory J (2011) Crosstalk in cellular signaling: background noise or the real thing? Dev Cell 21:985–991
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
Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735
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
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
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
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
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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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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DOI: https://doi.org/10.1007/s00299-013-1406-5