Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 13, 222

Interactions Between Ethylene and Auxin Are Crucial to the Control of Grape (Vitis Vinifera L.) Berry Ripening

Affiliations

Interactions Between Ethylene and Auxin Are Crucial to the Control of Grape (Vitis Vinifera L.) Berry Ripening

Christine Böttcher et al. BMC Plant Biol.

Abstract

Background: Fruit development is controlled by plant hormones, but the role of hormone interactions during fruit ripening is poorly understood. Interactions between ethylene and the auxin indole-3-acetic acid (IAA) are likely to be crucial during the ripening process, since both hormones have been shown to be implicated in the control of ripening in a range of different fruit species.

Results: Grapevine (Vitis vinifera L.) homologues of the TRYPTOPHAN AMINOTRANSFERASE RELATED (TAR) and YUCCA families, functioning in the only characterized pathway of auxin biosynthesis, were identified and the expression of several TAR genes was shown to be induced by the pre-ripening application of the ethylene-releasing compound Ethrel. The induction of TAR expression was accompanied by increased IAA and IAA-Asp concentrations, indicative of an upregulation of auxin biosynthesis and conjugation. Exposure of ex planta, pre-ripening berries to the ethylene biosynthesis inhibitor aminoethoxyvinylglycine resulted in decreased IAA and IAA-Asp concentrations. The delayed initiation of ripening observed in Ethrel-treated berries might therefore represent an indirect ethylene effect mediated by increased auxin concentrations. During berry development, the expression of three TAR genes and one YUCCA gene was upregulated at the time of ripening initiation and/or during ripening. This increase in auxin biosynthesis gene expression was preceded by high expression levels of the ethylene biosynthesis genes 1-aminocyclopropane-1-carboxylate synthase and 1-aminocyclopropane-1-carboxylate oxidase.

Conclusions: In grape berries, members of both gene families involved in the two-step pathway of auxin biosynthesis are expressed, suggesting that IAA is produced through the combined action of TAR and YUCCA proteins in developing berries. The induction of TAR expression by Ethrel applications and the developmental expression patterns of auxin and ethylene biosynthesis genes indicate that elevated concentrations of ethylene prior to the initiation of ripening might lead to an increased production of IAA, suggesting a complex involvement of this auxin and its conjugates in grape berry ripening.

Figures

Figure 1
Figure 1
Delayed ripening of Shiraz berries after treatment with Ethrel. Changes in TSS, measured as degrees Brix, in field grown Shiraz berries treated (A) once in 2011 (20 days pre-veraison) or (C) twice in 2012 (8 and 1 days pre-veraison) with 300 μL L-1 Ethrel in 0.1% (v/v) Chemwet 1000 or 0.1% (v/v) Chemwet 1000 (Control). The same berry samples were used to measure changes in berry weight in (B) the 2011 and (D) the 2012 samples. Control, closed circles with solid lines; Ethrel, closed triangles with dashed line. All data represent means ± SE (n = 3). Asterisks indicate significant differences of the mean values of Ethrel-treated samples from the mean values of Control samples as determined with Student’s t-test (*p < 0.05, **p < 0.01).
Figure 2
Figure 2
Changes in the concentration of IAA and IAA-Asp in pre-veraison berries in response to Ethrel application. IAA (A, C) and the IAA-amino acid conjugate, IAA-Asp, (B, D) were quantified by LC-MS/MS in pre-veraison Shiraz berries from the 2011 trial (A, B) and the 2012 trial (C, D) at the indicated time points after treatment with a Control or Ethrel solution as described in Figure 1. Control, dark grey bars; Ethrel, light grey bars. FW, fresh weight. CV, veraison of Control fruit; EV, veraison of Ethrel-treated fruit. All data represent means ± SE (n = 3). Asterisks indicate significant differences of the mean values of Ethrel-treated samples from the mean values of Control samples as determined with Student’s t-test (*p < 0.05, ***p < 0.001).
Figure 3
Figure 3
Phylogenetic relationship of TAR and YUC protein sequences from grapevine and Arabidopsis. Unrooted trees of (A) TAR sequences and (B) YUC sequences were generated with the PHYLIP program [81] using the neighbour-joining method and a bootstrap test with 1000 iterations (bootstrap values are indicated at each node). The scale bar indicates genetic distance based on branch length. The predicted grapevine proteins are highlighted with a shaded background. Asterisks indicate grapevine sequences with EST entries in the NCBI database. At, Arabidopsis thaliana; Vv, Vitis vinifera. Accession numbers of the Arabidopsis protein sequences used in this analysis are provided in Additional file 3.
Figure 4
Figure 4
Transcription of selected auxin biosynthesis and GH3 genes in response to Ethrel in the 2011 trial. The expression of TAR1-TAR4, YUC1, GH3-1 and GH3-2 in pre-veraison Shiraz berries from the 2011 trial was analysed by qRT-PCR at the indicated time points after treatment with a Control or Ethrel solution (see Figure 1). Control, dark grey bars; Ethrel, light grey bars. All data represent means ± SE (n = 3). Asterisks indicate significant differences of the mean values of Ethrel-treated samples from the mean values of Control samples as determined with Student’s t-test (*p < 0.05, **p < 0.01).
Figure 5
Figure 5
Changes in transcript accumulation of selected auxin biosynthesis and GH3 genes in response to Ethrel in the 2012 trial. The expression of TAR1-TAR4, YUC1, GH3-1 and GH3-2 in pre-veraison Shiraz berries from the 2012 trial was analysed by qRT-PCR at the indicated time points after treatment with a Control or Ethrel solution (see Figure 1). Control, dark grey bars; Ethrel, light grey bars. CV, veraison of Control fruit; EV, veraison of Ethrel-treated fruit. All data represent means ± SE (n = 3). Asterisks indicate significant differences of the mean values of Ethrel-treated samples from the mean values of Control samples as determined with Student’s t-test (*p < 0.05, **p < 0.01).
Figure 6
Figure 6
Effect of Ethrel and AVG on auxin concentrations and the expression of selected auxin biosynthesis and GH3 genes in an ex planta experiment. IAA (A) and the IAA-amino acid conjugate, IAA-Asp, (B) were quantified by LC-MS/MS in ex planta pre-veraison Shiraz berries exposed to ReTain (125 mg L-1 AVG, 3% (w/v) sucrose), Ethrel (72 mg L-1 ethephon, 3% (w/v) sucrose), or Control (3% (w/v) sucrose) conditions for the indicated periods of time. FW, fresh weight. (C) Using the same tissues the expression of TAR1-TAR4, YUC1, GH3-1 and GH3-2 was analysed by qRT-PCR. Control, dark grey bars; Ethrel, light grey bars; AVG, white bars. Bars represent means ± SE (n = 3) and are denoted by a different letter if the means for each time point differ significantly (p < 0.05) using one-way ANOVA followed by Duncan’s post hoc test.
Figure 7
Figure 7
Expression profiles of selected auxin and ethylene biosynthesis genes throughout Shiraz berry development. The development of field-grown Shiraz berries was documented by changes in (A) TSS, (B) berry weight and (C) anthocyanin (A520 nm) accumulation. (D) Between 3–16 wpf the expression of TAR1-TAR4, YUC1, ACS1 and ACO1 was analysed by qRT-PCR. “v” indicates veraison as determined by the last time point before a significant increase (ANOVA followed by Duncan’s post hoc test) in TSS levels was recorded. All data represent means ± SE (n = 3) and for the gene expression data LSD values were determined at the p < 0.05 significance level.

Similar articles

See all similar articles

Cited by 23 PubMed Central articles

See all "Cited by" articles

References

    1. Rashotte AM, Chae HS, Maxwell BB, Kieber JJ. The interaction of cytokinin with other signals. Physiol Plant. 2005;13(2):184–194. doi: 10.1111/j.1399-3054.2005.00445.x. - DOI
    1. Rolland F, Moore B, Sheen J. Sugar sensing and signaling in plants. Plant Cell. 2002;13(suppl 1):S185–S205. - PMC - PubMed
    1. Teale WD, Ditengou FA, Dovzhenko AD, Li X, Molendijk AM, Ruperti B, Paponov I, Palme K. Auxin as a model for the integration of hormonal signal processing and transduction. Mol Plant. 2008;13(2):229–237. doi: 10.1093/mp/ssn006. - DOI - PubMed
    1. Weiss D, Ori N. Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol. 2007;13(3):1240–1246. doi: 10.1104/pp.107.100370. - DOI - PMC - PubMed
    1. Zhang S, Wei Y, Lu Y, Wang X. Mechanisms of brassinosteroids interacting with multiple hormones. Plant Signal Behav. 2009;13(12):1117–1120. doi: 10.4161/psb.4.12.9903. - DOI - PMC - PubMed

Publication types

MeSH terms

Feedback