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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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GA Induces DAD1 Expression Prior To Induction of Expression of MYB21, MYB24, and MYB 57.(A–B) Semi-quantitative analysis of LOX2, GA2ox1, GA3ox1 and GA20ox2 (A), DAD1 (in red line), MYB21, MYB24 and MYB57 (B) expression in the ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) mutant flowers at 18, 48, 72 and 96 hrs after GA treatment. Data were averaged from 2–4 batches of independently treated samples and ACTII was used as the normalization control. The graph was drawn based on Log10 scale of the ratio of the expression levels of GA treated versus untreated samples.
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pgen-1000440-g007: GA Induces DAD1 Expression Prior To Induction of Expression of MYB21, MYB24, and MYB 57.(A–B) Semi-quantitative analysis of LOX2, GA2ox1, GA3ox1 and GA20ox2 (A), DAD1 (in red line), MYB21, MYB24 and MYB57 (B) expression in the ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) mutant flowers at 18, 48, 72 and 96 hrs after GA treatment. Data were averaged from 2–4 batches of independently treated samples and ACTII was used as the normalization control. The graph was drawn based on Log10 scale of the ratio of the expression levels of GA treated versus untreated samples.

Mentions: DAD1 is a stamen specific gene encoding chloroplastic phospholipase A1 protein that catalyzes the first step of JA biosynthesis. Mutation in DAD1 resulted in a typical JA-deficient phenotype in stamen development [40], a phenotype similar to that of myb21-t1 myb24-t1 double mutant. As mentioned earlier, JA likely acts downstream of GA to regulate the expression of MYB21, MYB24 and MYB57. To study whether there is a correlation between GA-regulated DAD1 expression and MYB21, MYB24 and MYB57 expression, we treated the ga1-3 gai-t6 rga-t2 rgl1-1 quadruple mutant with GA. We first confirmed the GA-responsiveness in the quadruple mutant plants by examining the expression of known GA-response genes GA3ox1, GA20ox2 and GA2ox1 (Figure 7A). Then we examined the expression of DAD1 and the three MYB genes MYB21, MYB24 and MYB57. Surprisingly, compared to the induction of MYB21 and MYB24 expression by JA treatment which is detectable at 18 hrs post treatment (Figure 5D), GA induction of the expression of these two MYB genes in ga1-3 gai-t6 rga-t2 rgl1-1 happens much later and only became detectable at 72 hrs (Figure 7B). More interestingly, GA induction of the expression of DAD1 is obviously detectable at 48 hrs which is prior to GA-induced expression of MYB21 and MYB24 in the ga1-3 gai-t6 rga-t2 rgl1-1 quadruple mutant (Figure 7B). Our data suggest that GA might first induce the expression of DAD1 to promoter JA production then via JA signaling to regulate the expression of MYB21 and MYB24.


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)

GA Induces DAD1 Expression Prior To Induction of Expression of MYB21, MYB24, and MYB 57.(A–B) Semi-quantitative analysis of LOX2, GA2ox1, GA3ox1 and GA20ox2 (A), DAD1 (in red line), MYB21, MYB24 and MYB57 (B) expression in the ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) mutant flowers at 18, 48, 72 and 96 hrs after GA treatment. Data were averaged from 2–4 batches of independently treated samples and ACTII was used as the normalization control. The graph was drawn based on Log10 scale of the ratio of the expression levels of GA treated versus untreated samples.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2654962&req=5

pgen-1000440-g007: GA Induces DAD1 Expression Prior To Induction of Expression of MYB21, MYB24, and MYB 57.(A–B) Semi-quantitative analysis of LOX2, GA2ox1, GA3ox1 and GA20ox2 (A), DAD1 (in red line), MYB21, MYB24 and MYB57 (B) expression in the ga1-3 gai-t6 rga-t2 rgl1-1 (Q3) mutant flowers at 18, 48, 72 and 96 hrs after GA treatment. Data were averaged from 2–4 batches of independently treated samples and ACTII was used as the normalization control. The graph was drawn based on Log10 scale of the ratio of the expression levels of GA treated versus untreated samples.
Mentions: DAD1 is a stamen specific gene encoding chloroplastic phospholipase A1 protein that catalyzes the first step of JA biosynthesis. Mutation in DAD1 resulted in a typical JA-deficient phenotype in stamen development [40], a phenotype similar to that of myb21-t1 myb24-t1 double mutant. As mentioned earlier, JA likely acts downstream of GA to regulate the expression of MYB21, MYB24 and MYB57. To study whether there is a correlation between GA-regulated DAD1 expression and MYB21, MYB24 and MYB57 expression, we treated the ga1-3 gai-t6 rga-t2 rgl1-1 quadruple mutant with GA. We first confirmed the GA-responsiveness in the quadruple mutant plants by examining the expression of known GA-response genes GA3ox1, GA20ox2 and GA2ox1 (Figure 7A). Then we examined the expression of DAD1 and the three MYB genes MYB21, MYB24 and MYB57. Surprisingly, compared to the induction of MYB21 and MYB24 expression by JA treatment which is detectable at 18 hrs post treatment (Figure 5D), GA induction of the expression of these two MYB genes in ga1-3 gai-t6 rga-t2 rgl1-1 happens much later and only became detectable at 72 hrs (Figure 7B). More interestingly, GA induction of the expression of DAD1 is obviously detectable at 48 hrs which is prior to GA-induced expression of MYB21 and MYB24 in the ga1-3 gai-t6 rga-t2 rgl1-1 quadruple mutant (Figure 7B). Our data suggest that GA might first induce the expression of DAD1 to promoter JA production then via JA signaling to regulate the expression of MYB21 and MYB24.

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