Auxin regulation of gibberellin biosynthesis in the roots of pea (Pisum sativum)
Diana E. Weston A , James B. Reid A and John J. Ross A BA School of Plant Science, University of Tasmania, Hobart, Tasmania 7001, Australia.
B Corresponding author. Email: john.ross@utas.edu.au
Functional Plant Biology 36(4) 362-369 https://doi.org/10.1071/FP08301
Submitted: 24 November 2008 Accepted: 6 February 2009 Published: 1 April 2009
Abstract
Auxin promotes GA biosynthesis in the aboveground parts of plants. However, it has not been demonstrated previously that this interaction occurs in roots. To understand the interactions between auxin and GAs in these organs, we treated wild-type pea (Pisum sativum L.) roots with the inhibitors of auxin action, p-chlorophenoxyisobutyric acid (PCIB) and yokonolide B (YkB), and with the auxin transport inhibitor N-1-naphthylphthalamic acid (NPA). These compounds generally downregulated GA synthesis genes and upregulated GA deactivation genes, and reduced the level of the bioactive GA1. These effects indicate that in pea roots, auxin at normal endogenous levels stimulates GA biosynthesis. We show also that supra-optimal levels of exogenous auxin reduce the endogenous level of bioactive GA in roots, although the effect appears too small to account for the strong growth-inhibitory effect of high auxin levels.
Additional keywords: DELLA, feedback, interaction.
Acknowledgements
We thank Dr Noel Davies (Central Science Laboratory, University of Tasmania, Australia), Ian Cummings, Tracey Winterbottom and Jennifer Smith for technical assistance, Gregory Jordan for statistical analyses, Professor Lewis Mander for deuterated and 14C-labelled GAs and the Australian Research Council for financial assistance. Yokonolide B was kindly provided by Dr Ken-ichiro Hayashi and Dr Hiroshi Nozaki (Okayama University of Science).
Bhalerao RP,
Eklöf J,
Ljung K,
Marchant A,
Bennett M, Sandberg G
(2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. The Plant Journal 29, 325–332.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Biswas KK,
Ooura C,
Higuchi K,
Miyazaki Y, Van Nguyen V ,
et al
.
(2007) Genetic characterization of mutants resistant to the antiauxin p-chlorophenoxyisobutyric acid (PCIB) reveals that AAR3, a gene encoding a DCN1-like protein, regulates responses to the synthetic auxin 2,4-dichlorophenoxyacetic acid in Arabidopsis roots. Plant Physiology 145, 773–785.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Desgagné-Penix I, Sponsel VM
(2008) Expression of gibberellin 20-oxidase1 (AtGA20ox1) in Arabidopsis seedlings with altered auxin status is regulated at multiple levels. Journal of Experimental Botany 59, 2057–2070.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Evans ML,
Ishikawa H, Estelle MA
(1994) Responses of Arabidopsis roots to auxin studied with high temporal resolution: comparison of wild type and auxin-response mutants. Planta 194, 215–222.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Frigerio M,
Alabadí D,
Pérez-Gómez J,
García-Cárcel L,
Phillips AL,
Hedden P, Blázquez MA
(2006) Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. Plant Physiology 142, 553–563.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fu X, Harberd NP
(2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421, 740–743.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hayashi K,
Jones AM,
Ogino K,
Yamazoe A,
Oono Y,
Inoguchi M,
Kondo H, Nozaki H
(2003) Yokonolide B, a novel inhibitor of auxin action, blocks degradation of AUX/IAA factors. Journal of Biological Chemistry 278, 23797–23806.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jager CE,
Symons GM,
Glancy NE,
Reid JB, Ross JJ
(2007) Evidence that the mature leaves contribute auxin to the immature tissues of pea (Pisum sativum L.). Planta 226, 361–368.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lester DR,
Ross JJ,
Davies PJ, Reid JB
(1997) Mendel’s stem length gene (LE) encodes a gibberellin 3β-hydroxylase. The Plant Cell 9, 1435–1443.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lester DR,
Ross JJ,
Smith JJ,
Elliott RC, Reid JB
(1999) Gibberellin 2-oxidation and the SLN gene of Pisum sativum. The Plant Journal 19, 65–73.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ljung K,
Hull AK,
Celenza J,
Yamada M,
Estelle M,
Normanly J, Sandberg G
(2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. The Plant Cell 17, 1090–1104.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Martin DN,
Proebsting WM,
Parks TD,
Dougherty WG,
Lange T,
Lewis MJ,
Gaskin P, Hedden P
(1996) Feed-back regulation of gibberellin biosynthesis and gene expression in Pisum sativum L. Planta 200, 159–166.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
O’Neill DP, Ross JJ
(2002) Auxin regulation of the gibberellin pathway in pea. Plant Physiology 130, 1974–1982.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Oono Y,
Ooura C,
Rahman A,
Aspuria ET,
Hayashi K,
Tanaka A, Uchimiya H
(2003)
p-Chlorophenoxyisobutyric acid impairs auxin response in Arabidopsis root. Plant Physiology 133, 1135–1147.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ozga JA,
Yu J, Reinecke DM
(2003) Pollination-, development-, and auxin specific regulation of gibberellin 3β-hydroxylase gene expression in pea fruits and seeds. Plant Physiology 131, 1137–1146.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ross JJ, Reid JB
(1989) Intenode length in Pisum. Biochemical expression of the le gene in darkness. Physiologia Plantarum 76, 164–172.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ross JJ,
O’Neill DP,
Smith JJ,
Kerckhoffs LHJ, Elliott RC
(2000) Evidence that auxin promotes gibberellin A1 biosynthesis in pea. The Plant Journal 21, 547–552.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ross JJ,
O’Neill DP, Rathbone DA
(2003) Auxin-gibberellin interactions in pea: integrating the old with the new. Journal of Plant Growth Regulation 22, 99–108.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Silva T, Davies PJ
(2007) Hormone growth responses of roots of shoot height mutants of pea. Physiologia Plantarum 129, 813–821.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Silverstone AL,
Jung H,
Dill A,
Kawaide H,
Kamiya Y, Sun T
(2001) Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. The Plant Cell 13, 1555–1565.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
van Huizen R,
Ozga JA, Reinecke DM
(1997) Seed and hormonal regulation of gibberellin 20-oxidase expression in pea pericarp. Plant Physiology 115, 123–128.
|
CAS |
PubMed |
Weston DE,
Elliott RC,
Lester DR,
Rameau C,
Reid JB,
Murfet IC, Ross JJ
(2008) The Pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiology 147, 199–205.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wolbang CM, Ross JJ
(2001) Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. Planta 214, 153–157.
|
CAS |
PubMed |
Wolbang CM,
Chandler PM,
Smith JJ, Ross JJ
(2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiology 134, 769–776.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yaxley JR,
Ross JJ,
Sherriff LJ, Reid JB
(2001) Gibberellin biosynthesis mutations and root development in pea. Plant Physiology 125, 627–633.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zentella R,
Zhang Z,
Park M,
Thomas SG, Endo A ,
et al
.
(2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. The Plant Cell 19, 3037–3057.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
