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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

Premature dehiscence in stamens of jai1-1. (a) Osmolality in stamens of wild type and jai1-1 plants. (b) Occurrence of starch in anther tissues of wild type and jai1-1 plants. Sections of fresh stamens were stained with iodine potassium iodide resulting in a black and brownish coloration of amylose and amylopectin, respectively. Note the strong staining in stamen of wild type plants showing a high number of starch grains and high levels of amylopectin, whereas stamen of jai1-1 show only a few starch grains and almost no amylopectin. Bar represents 100 μm for all micrographs. (c) Relative water content in stamens of wild type and jai1-1. (d) Cross-sections of fresh stamens of the six developmental stages in wild type and jai1-1. Note the appearance of fluids in the locule of wild type stamen at stage 2 and 3 (arrow heads) being absent in jai1-1. In contrast, jai1-1 pollen appear whitish (arrows) at early developmental stages pointing to premature pollen desiccation and accumulation of desiccation-related substances. Mean values + SD of stamens of the developmental stages indicated are shown in (a) and (c). *P ≤0.05, ***P ≤0.001 according to Student’s t-test (n ≥ 8). SD, standard deviation.
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Fig6: Premature dehiscence in stamens of jai1-1. (a) Osmolality in stamens of wild type and jai1-1 plants. (b) Occurrence of starch in anther tissues of wild type and jai1-1 plants. Sections of fresh stamens were stained with iodine potassium iodide resulting in a black and brownish coloration of amylose and amylopectin, respectively. Note the strong staining in stamen of wild type plants showing a high number of starch grains and high levels of amylopectin, whereas stamen of jai1-1 show only a few starch grains and almost no amylopectin. Bar represents 100 μm for all micrographs. (c) Relative water content in stamens of wild type and jai1-1. (d) Cross-sections of fresh stamens of the six developmental stages in wild type and jai1-1. Note the appearance of fluids in the locule of wild type stamen at stage 2 and 3 (arrow heads) being absent in jai1-1. In contrast, jai1-1 pollen appear whitish (arrows) at early developmental stages pointing to premature pollen desiccation and accumulation of desiccation-related substances. Mean values + SD of stamens of the developmental stages indicated are shown in (a) and (c). *P ≤0.05, ***P ≤0.001 according to Student’s t-test (n ≥ 8). SD, standard deviation.

Mentions: Taken together, the enhanced content of sugars as well as amino acids known as protective compounds in response to osmotic stress [30] points to increasing water loss attributing to the premature dehiscence in jai1-1 stamens. Interestingly, the higher levels of osmotically active compounds coincided with a higher osmolality of the cellular fluid in jai1-1 stamens (Figure 6a). In all developmental stages, jai1-1 stamens exhibited a significantly increased osmolality, reaching at stage 6 about twice the levels measured in WT stamens. This was accompanied by a diminished accumulation of starch in stamens of jai1-1 in comparison to WT stamens as visualized by staining of fresh sections (Figure 6b).Figure 6


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)

Premature dehiscence in stamens of jai1-1. (a) Osmolality in stamens of wild type and jai1-1 plants. (b) Occurrence of starch in anther tissues of wild type and jai1-1 plants. Sections of fresh stamens were stained with iodine potassium iodide resulting in a black and brownish coloration of amylose and amylopectin, respectively. Note the strong staining in stamen of wild type plants showing a high number of starch grains and high levels of amylopectin, whereas stamen of jai1-1 show only a few starch grains and almost no amylopectin. Bar represents 100 μm for all micrographs. (c) Relative water content in stamens of wild type and jai1-1. (d) Cross-sections of fresh stamens of the six developmental stages in wild type and jai1-1. Note the appearance of fluids in the locule of wild type stamen at stage 2 and 3 (arrow heads) being absent in jai1-1. In contrast, jai1-1 pollen appear whitish (arrows) at early developmental stages pointing to premature pollen desiccation and accumulation of desiccation-related substances. Mean values + SD of stamens of the developmental stages indicated are shown in (a) and (c). *P ≤0.05, ***P ≤0.001 according to Student’s t-test (n ≥ 8). SD, standard deviation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Premature dehiscence in stamens of jai1-1. (a) Osmolality in stamens of wild type and jai1-1 plants. (b) Occurrence of starch in anther tissues of wild type and jai1-1 plants. Sections of fresh stamens were stained with iodine potassium iodide resulting in a black and brownish coloration of amylose and amylopectin, respectively. Note the strong staining in stamen of wild type plants showing a high number of starch grains and high levels of amylopectin, whereas stamen of jai1-1 show only a few starch grains and almost no amylopectin. Bar represents 100 μm for all micrographs. (c) Relative water content in stamens of wild type and jai1-1. (d) Cross-sections of fresh stamens of the six developmental stages in wild type and jai1-1. Note the appearance of fluids in the locule of wild type stamen at stage 2 and 3 (arrow heads) being absent in jai1-1. In contrast, jai1-1 pollen appear whitish (arrows) at early developmental stages pointing to premature pollen desiccation and accumulation of desiccation-related substances. Mean values + SD of stamens of the developmental stages indicated are shown in (a) and (c). *P ≤0.05, ***P ≤0.001 according to Student’s t-test (n ≥ 8). SD, standard deviation.
Mentions: Taken together, the enhanced content of sugars as well as amino acids known as protective compounds in response to osmotic stress [30] points to increasing water loss attributing to the premature dehiscence in jai1-1 stamens. Interestingly, the higher levels of osmotically active compounds coincided with a higher osmolality of the cellular fluid in jai1-1 stamens (Figure 6a). In all developmental stages, jai1-1 stamens exhibited a significantly increased osmolality, reaching at stage 6 about twice the levels measured in WT stamens. This was accompanied by a diminished accumulation of starch in stamens of jai1-1 in comparison to WT stamens as visualized by staining of fresh sections (Figure 6b).Figure 6

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