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Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses.

Dobritzsch S, Weyhe M, Schubert R, Dindas J, Hause G, Kopka J, Hause B - BMC Biol. (2015)

Bottom Line: In contrast to the male sterile phenotype of Arabidopsis mutants, the tomato mutant jai1-1 exhibits female sterility with additional severe effects on stamen and pollen development.Application of jasmonates to flowers of transgenic plants affected in jasmonate biosynthesis diminished expression of ethylene-related genes, whereas the double mutant jai1-1 NeverRipe (ethylene insensitive) showed a complementation of jai1-1 phenotype in terms of dehiscence and pollen release.Our data suggest an essential role of jasmonates in the temporal inhibition of ethylene production to prevent premature desiccation of stamens and to ensure proper timing in flower development.

View Article: PubMed Central - PubMed

Affiliation: Leibniz Institute of Plant Biochemistry, Weinberg 3, D06120, Halle, Germany. susanne.forner@ipb-halle.de.

ABSTRACT

Background: Jasmonates are well known plant signaling components required for stress responses and development. A prominent feature of jasmonate biosynthesis or signaling mutants is the loss of fertility. In contrast to the male sterile phenotype of Arabidopsis mutants, the tomato mutant jai1-1 exhibits female sterility with additional severe effects on stamen and pollen development. Its senescence phenotype suggests a function of jasmonates in regulation of processes known to be mediated by ethylene. To test the hypothesis that ethylene involved in tomato stamen development is regulated by jasmonates, a temporal profiling of hormone content, transcriptome and metabolome of tomato stamens was performed using wild type and jai1-1.

Results: Wild type stamens showed a transient increase of jasmonates that is absent in jai1-1. Comparative transcriptome analyses revealed a diminished expression of genes involved in pollen nutrition at early developmental stages of jai1-1 stamens, but an enhanced expression of ethylene-related genes at late developmental stages. This finding coincides with an early increase of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in jai1-1 and a premature pollen release from stamens, a phenotype similarly visible in an ethylene overproducing mutant. Application of jasmonates to flowers of transgenic plants affected in jasmonate biosynthesis diminished expression of ethylene-related genes, whereas the double mutant jai1-1 NeverRipe (ethylene insensitive) showed a complementation of jai1-1 phenotype in terms of dehiscence and pollen release.

Conclusions: Our data suggest an essential role of jasmonates in the temporal inhibition of ethylene production to prevent premature desiccation of stamens and to ensure proper timing in flower development.

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Related in: MedlinePlus

Transcript accumulation pattern of ethylene-related genes in developing stamens of wild type and jai1-1. Relative transcript levels of genes encoding ET-related TFs acting as ‘master regulators’ (a), ET biosynthetic enzymes (b), proteins involved in ET-signaling (c), and of ET-response genes (d). All transcript levels were determined by RT-qPCR and set in relation to SlTIP41. The inset in each diagram visualizes the signal intensity obtained from microarray analysis. Mean values ± SD are shown. Data of the same developmental stage were compared between wild type and jai1-1 by Student’s t-test (*P ≤0.05, **P ≤0.01, n = 3). ET, ethylene; SD, standard deviation.
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Fig4: Transcript accumulation pattern of ethylene-related genes in developing stamens of wild type and jai1-1. Relative transcript levels of genes encoding ET-related TFs acting as ‘master regulators’ (a), ET biosynthetic enzymes (b), proteins involved in ET-signaling (c), and of ET-response genes (d). All transcript levels were determined by RT-qPCR and set in relation to SlTIP41. The inset in each diagram visualizes the signal intensity obtained from microarray analysis. Mean values ± SD are shown. Data of the same developmental stage were compared between wild type and jai1-1 by Student’s t-test (*P ≤0.05, **P ≤0.01, n = 3). ET, ethylene; SD, standard deviation.

Mentions: For a validation of these selected candidates, we used a new set of plants and all defined developmental stages of stamen to determine their relative transcript levels by quantitative RT-PCR (Figure 4). Transcript levels of all selected genes were at the detection limit at early developmental stages of WT stamens and started to rise earliest in stage 5 (SGN-U578128) or stage 6 (SGN-U592775). In stamens of jai1-1, however, these transcripts were detected at earlier stages and to higher levels. These data suggest that the absence of JA/JA-Ile and/or jasmonate signaling in jai1-1 stamen might lead to an early or premature ET biosynthesis and action and subsequently might contribute to the early senescence and dehiscence observed in stamen of jai1-1.Figure 4


Dissection of jasmonate functions in tomato stamen development by transcriptome and metabolome analyses.

Dobritzsch S, Weyhe M, Schubert R, Dindas J, Hause G, Kopka J, Hause B - BMC Biol. (2015)

Transcript accumulation pattern of ethylene-related genes in developing stamens of wild type and jai1-1. Relative transcript levels of genes encoding ET-related TFs acting as ‘master regulators’ (a), ET biosynthetic enzymes (b), proteins involved in ET-signaling (c), and of ET-response genes (d). All transcript levels were determined by RT-qPCR and set in relation to SlTIP41. The inset in each diagram visualizes the signal intensity obtained from microarray analysis. Mean values ± SD are shown. Data of the same developmental stage were compared between wild type and jai1-1 by Student’s t-test (*P ≤0.05, **P ≤0.01, n = 3). ET, ethylene; SD, standard deviation.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4443647&req=5

Fig4: Transcript accumulation pattern of ethylene-related genes in developing stamens of wild type and jai1-1. Relative transcript levels of genes encoding ET-related TFs acting as ‘master regulators’ (a), ET biosynthetic enzymes (b), proteins involved in ET-signaling (c), and of ET-response genes (d). All transcript levels were determined by RT-qPCR and set in relation to SlTIP41. The inset in each diagram visualizes the signal intensity obtained from microarray analysis. Mean values ± SD are shown. Data of the same developmental stage were compared between wild type and jai1-1 by Student’s t-test (*P ≤0.05, **P ≤0.01, n = 3). ET, ethylene; SD, standard deviation.
Mentions: For a validation of these selected candidates, we used a new set of plants and all defined developmental stages of stamen to determine their relative transcript levels by quantitative RT-PCR (Figure 4). Transcript levels of all selected genes were at the detection limit at early developmental stages of WT stamens and started to rise earliest in stage 5 (SGN-U578128) or stage 6 (SGN-U592775). In stamens of jai1-1, however, these transcripts were detected at earlier stages and to higher levels. These data suggest that the absence of JA/JA-Ile and/or jasmonate signaling in jai1-1 stamen might lead to an early or premature ET biosynthesis and action and subsequently might contribute to the early senescence and dehiscence observed in stamen of jai1-1.Figure 4

Bottom Line: In contrast to the male sterile phenotype of Arabidopsis mutants, the tomato mutant jai1-1 exhibits female sterility with additional severe effects on stamen and pollen development.Application of jasmonates to flowers of transgenic plants affected in jasmonate biosynthesis diminished expression of ethylene-related genes, whereas the double mutant jai1-1 NeverRipe (ethylene insensitive) showed a complementation of jai1-1 phenotype in terms of dehiscence and pollen release.Our data suggest an essential role of jasmonates in the temporal inhibition of ethylene production to prevent premature desiccation of stamens and to ensure proper timing in flower development.

View Article: PubMed Central - PubMed

Affiliation: Leibniz Institute of Plant Biochemistry, Weinberg 3, D06120, Halle, Germany. susanne.forner@ipb-halle.de.

ABSTRACT

Background: Jasmonates are well known plant signaling components required for stress responses and development. A prominent feature of jasmonate biosynthesis or signaling mutants is the loss of fertility. In contrast to the male sterile phenotype of Arabidopsis mutants, the tomato mutant jai1-1 exhibits female sterility with additional severe effects on stamen and pollen development. Its senescence phenotype suggests a function of jasmonates in regulation of processes known to be mediated by ethylene. To test the hypothesis that ethylene involved in tomato stamen development is regulated by jasmonates, a temporal profiling of hormone content, transcriptome and metabolome of tomato stamens was performed using wild type and jai1-1.

Results: Wild type stamens showed a transient increase of jasmonates that is absent in jai1-1. Comparative transcriptome analyses revealed a diminished expression of genes involved in pollen nutrition at early developmental stages of jai1-1 stamens, but an enhanced expression of ethylene-related genes at late developmental stages. This finding coincides with an early increase of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) in jai1-1 and a premature pollen release from stamens, a phenotype similarly visible in an ethylene overproducing mutant. Application of jasmonates to flowers of transgenic plants affected in jasmonate biosynthesis diminished expression of ethylene-related genes, whereas the double mutant jai1-1 NeverRipe (ethylene insensitive) showed a complementation of jai1-1 phenotype in terms of dehiscence and pollen release.

Conclusions: Our data suggest an essential role of jasmonates in the temporal inhibition of ethylene production to prevent premature desiccation of stamens and to ensure proper timing in flower development.

Show MeSH
Related in: MedlinePlus