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Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis.

Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J - PLoS Genet. (2009)

Bottom Line: Further genetic and molecular studies demonstrate that GA suppresses DELLAs to mobilize the expression of the key JA biosynthesis gene DAD1, and this is consistent with the observation that the JA content in the young flower buds of the GA-deficient quadruple mutant ga1-3 gai-t6 rga-t2 rgl1-1 is much lower than that in the WT.We conclude that GA promotes JA biosynthesis to control the expression of MYB21, MYB24, and MYB57.Therefore, we have established a hierarchical relationship between GA and JA in that modulation of JA pathway by GA is one of the prerequisites for GA to regulate the normal stamen development in Arabidopsis.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Proteos, Singapore.

ABSTRACT
Precise coordination between stamen and pistil development is essential to make a fertile flower. Mutations impairing stamen filament elongation, pollen maturation, or anther dehiscence will cause male sterility. Deficiency in plant hormone gibberellin (GA) causes male sterility due to accumulation of DELLA proteins, and GA triggers DELLA degradation to promote stamen development. Deficiency in plant hormone jasmonate (JA) also causes male sterility. However, little is known about the relationship between GA and JA in controlling stamen development. Here, we show that MYB21, MYB24, and MYB57 are GA-dependent stamen-enriched genes. Loss-of-function of two DELLAs RGA and RGL2 restores the expression of these three MYB genes together with restoration of stamen filament growth in GA-deficient plants. Genetic analysis showed that the myb21-t1 myb24-t1 myb57-t1 triple mutant confers a short stamen phenotype leading to male sterility. Further genetic and molecular studies demonstrate that GA suppresses DELLAs to mobilize the expression of the key JA biosynthesis gene DAD1, and this is consistent with the observation that the JA content in the young flower buds of the GA-deficient quadruple mutant ga1-3 gai-t6 rga-t2 rgl1-1 is much lower than that in the WT. We conclude that GA promotes JA biosynthesis to control the expression of MYB21, MYB24, and MYB57. Therefore, we have established a hierarchical relationship between GA and JA in that modulation of JA pathway by GA is one of the prerequisites for GA to regulate the normal stamen development in Arabidopsis.

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MYB21, MYB24, and MYB57 Function Redundantly in Regulating the Stamen Filament Development.(A) Schematic diagram shows the respective T-DNA insertions in the three MYB genes. Black box: exon; black line: intron; triangle: T-DNA insertion site. (B) RT-PCR analysis of MYB24 transcripts in myb24-t1 and MYB57 transcripts in myb57-t1 and northern analysis of MYB21 transcripts in myb21-t1. Total RNA for RT-PCR and northern analysis was extracted from the young flower buds. (C) Comparison of main shoots bearing siliques among different mutant lines as indicated. (D) Comparison of the stamen phenotype among different mutant lines as indicated. Genotypes for flowers a-h in (D) corresponds to that showed in (C).
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pgen-1000440-g003: MYB21, MYB24, and MYB57 Function Redundantly in Regulating the Stamen Filament Development.(A) Schematic diagram shows the respective T-DNA insertions in the three MYB genes. Black box: exon; black line: intron; triangle: T-DNA insertion site. (B) RT-PCR analysis of MYB24 transcripts in myb24-t1 and MYB57 transcripts in myb57-t1 and northern analysis of MYB21 transcripts in myb21-t1. Total RNA for RT-PCR and northern analysis was extracted from the young flower buds. (C) Comparison of main shoots bearing siliques among different mutant lines as indicated. (D) Comparison of the stamen phenotype among different mutant lines as indicated. Genotypes for flowers a-h in (D) corresponds to that showed in (C).

Mentions: To investigate their roles in GA-mediated floral organ development, we identified T-DNA insertional mutant lines corresponding to these three MYB genes from the Salk Institute Genomic Arabidopsis Laboratory (SIGnAL) database. Mutant alleles were confirmed (data not shown) and designated as myb21-t1 (SALK_042711) for MYB21, myb24-t1 (SALK_017221) for MYB24, and myb57-t1 (SALK_065776) for MYB57 (Figure 3A). myb24-t1 and myb57-t1 are both likely alleles since MYB24 and MYB57 transcripts were undetectable in myb24-t1 and myb57-t1 mutant flower buds, respectively (Figure 3B). On the other hand, MYB21 transcripts were still detectable in myb21-t1 although its level was greatly reduced in the mutant, suggesting that myb21-t1 is likely a leaky allele (Figure 3B). After two rounds of backcross, we found that myb24-t1 and myb57-t1 mutant plants were phenotypically indistinguishable from the WT control plant (Figure 3C; Table 2). However, in myb21-t1 the early developed flowers (∼the first 10 flowers) bore short stamens (Figure S4) with greatly reduced fertility and only the late developed flowers yielded proper seed settings (Figure 3C; Table 2). A close look at the matured early flowers in myb21-t1 showed that the stamens did produce pollens (Figure 3D, panel d). Cross-pollinating the pollens onto the myb21-t1 stigma yielded seeds that were homozygous for myb21-t1 and onto the WT stigma yielded myb21-t1 heterozygous seeds (data not shown), demonstrating that the short stamen is responsible for the partial sterile phenotype. Although myb21-t1 is likely a leaky allele, the short stamen phenotype conferred by the myb21-t1 mutation is identical to a MYB21 allele we obtained later from Gabi-Kat stock (stock number N311167, data not shown).


Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis.

Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J - PLoS Genet. (2009)

MYB21, MYB24, and MYB57 Function Redundantly in Regulating the Stamen Filament Development.(A) Schematic diagram shows the respective T-DNA insertions in the three MYB genes. Black box: exon; black line: intron; triangle: T-DNA insertion site. (B) RT-PCR analysis of MYB24 transcripts in myb24-t1 and MYB57 transcripts in myb57-t1 and northern analysis of MYB21 transcripts in myb21-t1. Total RNA for RT-PCR and northern analysis was extracted from the young flower buds. (C) Comparison of main shoots bearing siliques among different mutant lines as indicated. (D) Comparison of the stamen phenotype among different mutant lines as indicated. Genotypes for flowers a-h in (D) corresponds to that showed in (C).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2654962&req=5

pgen-1000440-g003: MYB21, MYB24, and MYB57 Function Redundantly in Regulating the Stamen Filament Development.(A) Schematic diagram shows the respective T-DNA insertions in the three MYB genes. Black box: exon; black line: intron; triangle: T-DNA insertion site. (B) RT-PCR analysis of MYB24 transcripts in myb24-t1 and MYB57 transcripts in myb57-t1 and northern analysis of MYB21 transcripts in myb21-t1. Total RNA for RT-PCR and northern analysis was extracted from the young flower buds. (C) Comparison of main shoots bearing siliques among different mutant lines as indicated. (D) Comparison of the stamen phenotype among different mutant lines as indicated. Genotypes for flowers a-h in (D) corresponds to that showed in (C).
Mentions: To investigate their roles in GA-mediated floral organ development, we identified T-DNA insertional mutant lines corresponding to these three MYB genes from the Salk Institute Genomic Arabidopsis Laboratory (SIGnAL) database. Mutant alleles were confirmed (data not shown) and designated as myb21-t1 (SALK_042711) for MYB21, myb24-t1 (SALK_017221) for MYB24, and myb57-t1 (SALK_065776) for MYB57 (Figure 3A). myb24-t1 and myb57-t1 are both likely alleles since MYB24 and MYB57 transcripts were undetectable in myb24-t1 and myb57-t1 mutant flower buds, respectively (Figure 3B). On the other hand, MYB21 transcripts were still detectable in myb21-t1 although its level was greatly reduced in the mutant, suggesting that myb21-t1 is likely a leaky allele (Figure 3B). After two rounds of backcross, we found that myb24-t1 and myb57-t1 mutant plants were phenotypically indistinguishable from the WT control plant (Figure 3C; Table 2). However, in myb21-t1 the early developed flowers (∼the first 10 flowers) bore short stamens (Figure S4) with greatly reduced fertility and only the late developed flowers yielded proper seed settings (Figure 3C; Table 2). A close look at the matured early flowers in myb21-t1 showed that the stamens did produce pollens (Figure 3D, panel d). Cross-pollinating the pollens onto the myb21-t1 stigma yielded seeds that were homozygous for myb21-t1 and onto the WT stigma yielded myb21-t1 heterozygous seeds (data not shown), demonstrating that the short stamen is responsible for the partial sterile phenotype. Although myb21-t1 is likely a leaky allele, the short stamen phenotype conferred by the myb21-t1 mutation is identical to a MYB21 allele we obtained later from Gabi-Kat stock (stock number N311167, data not shown).

Bottom Line: Further genetic and molecular studies demonstrate that GA suppresses DELLAs to mobilize the expression of the key JA biosynthesis gene DAD1, and this is consistent with the observation that the JA content in the young flower buds of the GA-deficient quadruple mutant ga1-3 gai-t6 rga-t2 rgl1-1 is much lower than that in the WT.We conclude that GA promotes JA biosynthesis to control the expression of MYB21, MYB24, and MYB57.Therefore, we have established a hierarchical relationship between GA and JA in that modulation of JA pathway by GA is one of the prerequisites for GA to regulate the normal stamen development in Arabidopsis.

View Article: PubMed Central - PubMed

Affiliation: Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Proteos, Singapore.

ABSTRACT
Precise coordination between stamen and pistil development is essential to make a fertile flower. Mutations impairing stamen filament elongation, pollen maturation, or anther dehiscence will cause male sterility. Deficiency in plant hormone gibberellin (GA) causes male sterility due to accumulation of DELLA proteins, and GA triggers DELLA degradation to promote stamen development. Deficiency in plant hormone jasmonate (JA) also causes male sterility. However, little is known about the relationship between GA and JA in controlling stamen development. Here, we show that MYB21, MYB24, and MYB57 are GA-dependent stamen-enriched genes. Loss-of-function of two DELLAs RGA and RGL2 restores the expression of these three MYB genes together with restoration of stamen filament growth in GA-deficient plants. Genetic analysis showed that the myb21-t1 myb24-t1 myb57-t1 triple mutant confers a short stamen phenotype leading to male sterility. Further genetic and molecular studies demonstrate that GA suppresses DELLAs to mobilize the expression of the key JA biosynthesis gene DAD1, and this is consistent with the observation that the JA content in the young flower buds of the GA-deficient quadruple mutant ga1-3 gai-t6 rga-t2 rgl1-1 is much lower than that in the WT. We conclude that GA promotes JA biosynthesis to control the expression of MYB21, MYB24, and MYB57. Therefore, we have established a hierarchical relationship between GA and JA in that modulation of JA pathway by GA is one of the prerequisites for GA to regulate the normal stamen development in Arabidopsis.

Show MeSH
Related in: MedlinePlus