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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, MYB24I, and MYB57 Are RGA- and RGL2-Repressible Floral Specific Genes.(A) RT-PCR analysis shows that the expression of the three MYB genes in the young flower buds are greatly reduced in ga1-3 but restored to the WT level in ga1-3 gai-t6 rgat2 rgl1-1 rgl2-1 (penta). (B–C) RT-PCR analysis shows that the repressed expression of the three MYB genes in ga1-3 was restored in ga1-3 gai-t6 rga-t2 rgl2-1 (Q2) and ga1-3 rga-t2 rgl1-1 rgl2-1 (Q4) two quadruple mutants but not in ga1-3 gai-t6 rgl1-1 rgl2-1 (Q1) and ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) two quadruple mutants (B). This restoration of MYB expression nicely correlates with the recovery of fertility in Q2 and Q4 (C). Total RNA used in RT-PCR analysis was extracted from the young flower buds. (D) RT-PCR analysis shows that the three MYB genes are floral specific genes. IF, inflorescence; CL, cauline leaves; RL, rosette leaves; IT, internodes; RT, roots; SL, siliques. (E) Amino acid alignment of MYB21, MYB24 and MYB57 proteins. The conserved R2 and R3 domains and the NYWSV/ME/DDlWP/S motif are highlighted in red, blue and green, respectively.
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pgen-1000440-g002: MYB21, MYB24I, and MYB57 Are RGA- and RGL2-Repressible Floral Specific Genes.(A) RT-PCR analysis shows that the expression of the three MYB genes in the young flower buds are greatly reduced in ga1-3 but restored to the WT level in ga1-3 gai-t6 rgat2 rgl1-1 rgl2-1 (penta). (B–C) RT-PCR analysis shows that the repressed expression of the three MYB genes in ga1-3 was restored in ga1-3 gai-t6 rga-t2 rgl2-1 (Q2) and ga1-3 rga-t2 rgl1-1 rgl2-1 (Q4) two quadruple mutants but not in ga1-3 gai-t6 rgl1-1 rgl2-1 (Q1) and ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) two quadruple mutants (B). This restoration of MYB expression nicely correlates with the recovery of fertility in Q2 and Q4 (C). Total RNA used in RT-PCR analysis was extracted from the young flower buds. (D) RT-PCR analysis shows that the three MYB genes are floral specific genes. IF, inflorescence; CL, cauline leaves; RL, rosette leaves; IT, internodes; RT, roots; SL, siliques. (E) Amino acid alignment of MYB21, MYB24 and MYB57 proteins. The conserved R2 and R3 domains and the NYWSV/ME/DDlWP/S motif are highlighted in red, blue and green, respectively.

Mentions: Three MYB genes, namely MYB21, MYB24 and MYB57, were among the identified DELLA-repressed stamen-enriched genes (Figure 1; Table 1). Based on the phylogenetic tree, MYB24 and MYB21 are classified into the subgroup 19 of R2R3-MYB family [36]. MYB57 shares high similarity with this subfamily and is a close member to this subfamily [37]. Overall, MYB21 shares 61.6% and 51.0% identity with MYB24 and MYB57 at the amino acid level, respectively (Figure S1). The expression of these three MYBs in the young flower buds were reduced to a very low level in ga1-3 but restored to the wild type (WT) level in the ga1-3 gai-t6 rga-t1 rgl1-1 rgl2-1 penta mutant (Figure 2A). In order to find out which DELLA (RGL1, RGL2, RGA and GAI) is more effective in repressing the expression of MYB21, MYB24 and MYB57, transcript levels of each individual MYB gene were studied in four quadruple mutants in which only one of the four DELLA genes remains intact. All three MYB genes were almost undetectable in the Q1 (ga1-3 gai-t6 rgl1-1 rgl2-1, wild type for RGA) and barely detectable in the Q3 (ga1-3 gai-t6 rgl1-1 rga-t2, wild type for RGL2) mutants but were detected at high levels in the Q2 (ga1-3 rga-t2 rgl1-1 rgl2-1, wild type for GAI) and Q4 (ga1-3 gai-t6 rga-t2 rgl2-1, wild type for RGL1) mutants (Figure 2B), suggesting that RGA and RGL2, but not GAI nor RGL1, were the more effective DELLAs in repressing the expression of these three MYB genes. Interestingly, we showed previously that while Q1 and Q3 mutants, as the ga1-3 mutant, were retarded in floral development both Q2 and Q4 mutants produced normal fertile flowers (Figure 2C) [8]. Therefore, it seems there is a nice correlation between normal floral development and the expression of MYB21, MYB24 and MYB57, suggesting that these three MYBs are probably necessary for normal floral development.


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, MYB24I, and MYB57 Are RGA- and RGL2-Repressible Floral Specific Genes.(A) RT-PCR analysis shows that the expression of the three MYB genes in the young flower buds are greatly reduced in ga1-3 but restored to the WT level in ga1-3 gai-t6 rgat2 rgl1-1 rgl2-1 (penta). (B–C) RT-PCR analysis shows that the repressed expression of the three MYB genes in ga1-3 was restored in ga1-3 gai-t6 rga-t2 rgl2-1 (Q2) and ga1-3 rga-t2 rgl1-1 rgl2-1 (Q4) two quadruple mutants but not in ga1-3 gai-t6 rgl1-1 rgl2-1 (Q1) and ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) two quadruple mutants (B). This restoration of MYB expression nicely correlates with the recovery of fertility in Q2 and Q4 (C). Total RNA used in RT-PCR analysis was extracted from the young flower buds. (D) RT-PCR analysis shows that the three MYB genes are floral specific genes. IF, inflorescence; CL, cauline leaves; RL, rosette leaves; IT, internodes; RT, roots; SL, siliques. (E) Amino acid alignment of MYB21, MYB24 and MYB57 proteins. The conserved R2 and R3 domains and the NYWSV/ME/DDlWP/S motif are highlighted in red, blue and green, respectively.
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Related In: Results  -  Collection

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pgen-1000440-g002: MYB21, MYB24I, and MYB57 Are RGA- and RGL2-Repressible Floral Specific Genes.(A) RT-PCR analysis shows that the expression of the three MYB genes in the young flower buds are greatly reduced in ga1-3 but restored to the WT level in ga1-3 gai-t6 rgat2 rgl1-1 rgl2-1 (penta). (B–C) RT-PCR analysis shows that the repressed expression of the three MYB genes in ga1-3 was restored in ga1-3 gai-t6 rga-t2 rgl2-1 (Q2) and ga1-3 rga-t2 rgl1-1 rgl2-1 (Q4) two quadruple mutants but not in ga1-3 gai-t6 rgl1-1 rgl2-1 (Q1) and ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) two quadruple mutants (B). This restoration of MYB expression nicely correlates with the recovery of fertility in Q2 and Q4 (C). Total RNA used in RT-PCR analysis was extracted from the young flower buds. (D) RT-PCR analysis shows that the three MYB genes are floral specific genes. IF, inflorescence; CL, cauline leaves; RL, rosette leaves; IT, internodes; RT, roots; SL, siliques. (E) Amino acid alignment of MYB21, MYB24 and MYB57 proteins. The conserved R2 and R3 domains and the NYWSV/ME/DDlWP/S motif are highlighted in red, blue and green, respectively.
Mentions: Three MYB genes, namely MYB21, MYB24 and MYB57, were among the identified DELLA-repressed stamen-enriched genes (Figure 1; Table 1). Based on the phylogenetic tree, MYB24 and MYB21 are classified into the subgroup 19 of R2R3-MYB family [36]. MYB57 shares high similarity with this subfamily and is a close member to this subfamily [37]. Overall, MYB21 shares 61.6% and 51.0% identity with MYB24 and MYB57 at the amino acid level, respectively (Figure S1). The expression of these three MYBs in the young flower buds were reduced to a very low level in ga1-3 but restored to the wild type (WT) level in the ga1-3 gai-t6 rga-t1 rgl1-1 rgl2-1 penta mutant (Figure 2A). In order to find out which DELLA (RGL1, RGL2, RGA and GAI) is more effective in repressing the expression of MYB21, MYB24 and MYB57, transcript levels of each individual MYB gene were studied in four quadruple mutants in which only one of the four DELLA genes remains intact. All three MYB genes were almost undetectable in the Q1 (ga1-3 gai-t6 rgl1-1 rgl2-1, wild type for RGA) and barely detectable in the Q3 (ga1-3 gai-t6 rgl1-1 rga-t2, wild type for RGL2) mutants but were detected at high levels in the Q2 (ga1-3 rga-t2 rgl1-1 rgl2-1, wild type for GAI) and Q4 (ga1-3 gai-t6 rga-t2 rgl2-1, wild type for RGL1) mutants (Figure 2B), suggesting that RGA and RGL2, but not GAI nor RGL1, were the more effective DELLAs in repressing the expression of these three MYB genes. Interestingly, we showed previously that while Q1 and Q3 mutants, as the ga1-3 mutant, were retarded in floral development both Q2 and Q4 mutants produced normal fertile flowers (Figure 2C) [8]. Therefore, it seems there is a nice correlation between normal floral development and the expression of MYB21, MYB24 and MYB57, suggesting that these three MYBs are probably necessary for normal floral development.

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