Abstract
Gibberellic acid (GA) is both necessary and sufficient to promote fiber elongation in cultured fertilized ovules of the upland cotton variety Coker 312. This is likely due to the temporal and spatial regulation of GA biosynthesis, perception, and subsequent signal transduction that leads to alterations in gene expression and morphology. Our results indicate that the initiation of fiber elongation by the application of GA to cultured ovules corresponds with increased expression of genes that encode xyloglucan endotransglycosylase/hydrolase (XTH) and expansin (EXP) that are involved in promoting cell elongation. To gain a better understanding of the GA signaling components in cotton, that lead to such changes in gene expression, two GA receptor genes (GhGID1a and GhGID1b) and two DELLA protein genes (GhSLR1a and GhSLR1b) that are orthologous to the rice GA receptor (GID1) and the rice DELLA gene (SLR1), respectively, were characterized. Similar to the GA biosynthetic genes, expression of GhGID1a and GhGID1b is under the negative regulation by GA while GA positively regulates GhSLR1a. Recombinant GST-GhGID1s showed GA-binding activity in vitro that was augmented in the presence of GhSLR1a, GhSLR1b, or rice SLR1, indicating complex formation between the receptors and repressor proteins. This was further supported by the GA-dependent interaction of these proteins in yeast cells. Ectopic expression of the GhGID1a in the rice gid1-3 mutant plants rescued the GA-insensitive dwarf phenotype, which demonstrates that it is a functional GA receptor. Furthermore, ectopic expression of GhSLR1b in wild type Arabidopsis led to reduced growth and upregulated expression of DELLA-responsive genes.
Similar content being viewed by others
References
Alvey L, Harberd NP (2005) DELLA proteins: integrators of multiple plant growth regulatory inputs? Physiol Plantarum 123:153–160
Beasley CA, Ting IP (1973) The effects of plant growth substances on in vitro fiber development from fertilized cotton ovules. Am J Bot 60:130–139
Beasley CA, Ting IP (1974) Effects of plant growth substances on in vitro fiber development from unfertilized cotton ovules. Am J Bot 61:188–194
Chen YN, Shen CY, Zhang ZL, Yan JQ (1988) Study of the fiber development of cotton ovules. Acta Biol Exp Sin 21:417–421
Chen JG, Du XM, Zhao HY, Zhou X (1996) Fluctuation in levels of endogenous plant hormones in ovules of normal and mutant cotton during flowering and their relation to fiber development. J Plant Growth Regul 15:173–177
Cho HT, Kende H (1997) Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell 9:1661–1671
Choi JH, Jung HY, Kim HS, Cho HG (2000) PhyloDraw: a phylogenetic tree drawing system. Bioinformatics 16:1056–1058
Chow B, McCourt P (2006) Plant hormone receptors: perception is everything. Genes Dev 20:1998–2008
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17
Davidonis GH (1999) Cotton fibers in vitro. In: Basra AS (ed) Cotton fibers. Food Products Press, p 74
Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA 98:14162–14167
Gokani SJ, Thaker VS (2002) Role of gibberellic acid in cotton fibre development. J Agric Sci 138:255–260
Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414
Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol 129:191–200
Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (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 13:999–1010
Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in Nuclei. Plant Cell 14:57–70
Iuchi S, Suzuki H, Kim YC, Iuchi A, Kuromori T, Ueguchi-Tanaka M, Asami T, Yamaguchi I, Matsuoka M, Kobayashi M, Nakajima M (2007) Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J 50:958–966
Lee Y, Kende H (2002) Expression of alpha-expansin and expansin-like genes in deepwater rice. Plant Physiol 130:1396–1405
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time PCR and the 2(-Delta Delta C(t)) method. Methods 25:402–408
Momtaz OA (1998) Effect of plant growth regulators on in vitro fiber development from unfertilized and fertilized Egyptian cotton ovules. Plant Growth Regul 25:159–164
Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M, Maeda T, Matsuoka M, Yamaguchi I (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889
Nicholas KB, Nicholas HB (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Multiple Sequence Alignment Editor & Shading Utility Version 2.7000
Nishitani K (1997) The role of endoxyloglucan transferase in the organization of plant cell walls. Int Rev Cytol 173:157–206
Ogawa M, Kusano T, Katsumi M, Sano H (2000) Rice gibberellin-insensitive gene homolog, OsGAI encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene 245:21–29
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205
Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119
Ryser U (1999) Cotton fiber initiation and histodifferentiation. In: Basra AS (ed) Cotton fibers. Food Products Press, pp 1–45
Seagull RW, Giavalis S (2004) Pre- and post-anthesis application of exogenous hormones alters fiber production in Gossypium hirsutum L. cultivar Maxxa GTO. J Cotton Sci 8:105–111
Shen TY, Chang SC, Yhn CC (1978) The growth of fibers on excised cotton ovules and the formation of seedlings. Acta Phytophysiol Sin 4:183–187
Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX (2006) Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664
Silverstone AL, Ciampaglio CN, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169
Smith RC, Matthews PR, Schunmann PHD, Chandler PM (1996) The regulation of leaf elongation and xyloglucan endotransglycosylase by gibberellin in ‘Himalaya’ barley (Hordeum vulgare L). J Exp Bot 47:1395–1404
Sponsel VM, Hedden P (2004) Gibberellin biosynthesis and inactivation In: Davis PJ (ed) Plant hormones. Kluwer Academic Publishers, pp 63–94
Sun T (2004) Gibberellin signal transduction in stem elongation & leaf growth. In: Davis PJ (ed) Plant hormones. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 304–320
Sun Y, Fokar M, Asami T, Yoshida S, Allen RD (2004) Characterization of the brassinosteroid insensitive 1 genes of cotton. Plant Mol Biol 54:221–232
Sun Y, Veerabomma S, Abdel-Mageed HA, Fokar M, Asami T, Yoshida S, Allen RD (2005) Brassinosteroid regulates fiber development on cultured cotton ovules. Plant Cell Physiol 46:1384–1391
Thomas SG, Hedden P (2006) Gibberellin metabolism and signal transduction. In: Hedden P, Thomas SG (eds) Plant hormone signaling, vol 24. Blackwell Publishing, pp 147–184
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YIC, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698
Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, Matsuoka M (2007) Molecular Interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–2155
Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12
Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186
Xu W, Campbell P, Vargheese AK, Braam J (1996) The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression. Plant J 9:879–889
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
Zheng ZR, Xu DW (1982) The role of plant hormones in the reproductive growth of cotton plants. Sci Agric Sin 5:40–47
Acknowledgments
We would like to thank Dr. Kan Wang from The Plant Transformation Facility at Iowa State University for rice transformations. This project was funded by a grant to L.A. and R.D.A. from Cotton Incorporated, Cary, NC, USA.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aleman, L., Kitamura, J., Abdel-mageed, H. et al. Functional analysis of cotton orthologs of GA signal transduction factors GID1 and SLR1. Plant Mol Biol 68, 1–16 (2008). https://doi.org/10.1007/s11103-008-9347-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-008-9347-z