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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-t1 myb24-t1 Is Epistatic to ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 in Controlling Stamen Filament Elongation.(A) Comparison of the stamen phenotype among ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1(penta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 myb24-t1 (hepta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 (hexa1) and ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb24-t1 (hexa2). (B) SEM of stamen filament epidermal cells in the penta, hepta, hexa1 and hexa2 mutants. Segments shown were all from the middle part of the filament. Some individual cells were outlined with black lines for easy visualization. (C) Comparison of stamen and pistil lengths among different genotypes. Filament and pistil lengths were measured from SEM pictures (n = 30). (D) Average number of epidermal cells per stamen filament in penta, hepta, hexa1 and hexa2. n: number of stamens used in counting.
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pgen-1000440-g004: myb21-t1 myb24-t1 Is Epistatic to ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 in Controlling Stamen Filament Elongation.(A) Comparison of the stamen phenotype among ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1(penta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 myb24-t1 (hepta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 (hexa1) and ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb24-t1 (hexa2). (B) SEM of stamen filament epidermal cells in the penta, hepta, hexa1 and hexa2 mutants. Segments shown were all from the middle part of the filament. Some individual cells were outlined with black lines for easy visualization. (C) Comparison of stamen and pistil lengths among different genotypes. Filament and pistil lengths were measured from SEM pictures (n = 30). (D) Average number of epidermal cells per stamen filament in penta, hepta, hexa1 and hexa2. n: number of stamens used in counting.

Mentions: MYB21 and MYB24 were repressed in ga1-3 but their expressions were restored to the WT level in the ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 penta mutant, suggesting that GA regulates MYB21 and MYB24 through inactivating DELLA proteins. Application of exogenous GA could not rescue the stamen development in myb21 myb24 mutant (data not shown), suggesting that MYB21 and MYB24 are needed in GA-mediated stamen development. To further confirm this hypothesis, we crossed myb21 myb24 with ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 to generate two hexa mutants (hexa1: ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1; hexa2: ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb24-t1) and one hepta mutant (ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 myb24-t1). The two hexa mutants overall appeared similar to each other and had wildtype-like stamens and were largely fertile (Figure 4A; Figure S5). The hepta mutant plant displayed no difference from the penta mutant plant in its vegetative growth. However, its mature flowers showed a short filament phenotype identical to that in the myb21-t1 myb24-t1 double mutant (Figure 4A; Figure S5). This observation demonstrated that myb21-t1 myb24-t1 double mutations are epistatic to DELLA mutations. SEM analysis showed that the short stamen phenotype in the hepta mutant was due to reduced cell length (Figure 4B and 4C), rather than to a reduction in cell number (Figure 4D). Therefore, MYB21 and MYB24 act downstream of DELLAs in GA signaling pathway to control the stamen filament 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-t1 myb24-t1 Is Epistatic to ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 in Controlling Stamen Filament Elongation.(A) Comparison of the stamen phenotype among ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1(penta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 myb24-t1 (hepta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 (hexa1) and ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb24-t1 (hexa2). (B) SEM of stamen filament epidermal cells in the penta, hepta, hexa1 and hexa2 mutants. Segments shown were all from the middle part of the filament. Some individual cells were outlined with black lines for easy visualization. (C) Comparison of stamen and pistil lengths among different genotypes. Filament and pistil lengths were measured from SEM pictures (n = 30). (D) Average number of epidermal cells per stamen filament in penta, hepta, hexa1 and hexa2. n: number of stamens used in counting.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2654962&req=5

pgen-1000440-g004: myb21-t1 myb24-t1 Is Epistatic to ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 in Controlling Stamen Filament Elongation.(A) Comparison of the stamen phenotype among ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1(penta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 myb24-t1 (hepta), ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 (hexa1) and ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb24-t1 (hexa2). (B) SEM of stamen filament epidermal cells in the penta, hepta, hexa1 and hexa2 mutants. Segments shown were all from the middle part of the filament. Some individual cells were outlined with black lines for easy visualization. (C) Comparison of stamen and pistil lengths among different genotypes. Filament and pistil lengths were measured from SEM pictures (n = 30). (D) Average number of epidermal cells per stamen filament in penta, hepta, hexa1 and hexa2. n: number of stamens used in counting.
Mentions: MYB21 and MYB24 were repressed in ga1-3 but their expressions were restored to the WT level in the ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 penta mutant, suggesting that GA regulates MYB21 and MYB24 through inactivating DELLA proteins. Application of exogenous GA could not rescue the stamen development in myb21 myb24 mutant (data not shown), suggesting that MYB21 and MYB24 are needed in GA-mediated stamen development. To further confirm this hypothesis, we crossed myb21 myb24 with ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 to generate two hexa mutants (hexa1: ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1; hexa2: ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb24-t1) and one hepta mutant (ga1-3 gai-t6 rga-t2 rgl1-1 rgl2-1 myb21-t1 myb24-t1). The two hexa mutants overall appeared similar to each other and had wildtype-like stamens and were largely fertile (Figure 4A; Figure S5). The hepta mutant plant displayed no difference from the penta mutant plant in its vegetative growth. However, its mature flowers showed a short filament phenotype identical to that in the myb21-t1 myb24-t1 double mutant (Figure 4A; Figure S5). This observation demonstrated that myb21-t1 myb24-t1 double mutations are epistatic to DELLA mutations. SEM analysis showed that the short stamen phenotype in the hepta mutant was due to reduced cell length (Figure 4B and 4C), rather than to a reduction in cell number (Figure 4D). Therefore, MYB21 and MYB24 act downstream of DELLAs in GA signaling pathway to control the stamen filament 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