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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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Overexpression of MYB21 Rescues the Stamen Filament Growth and Fertility to the opr3 Mutant.(A) RT-PCR analysis of MYB21 and OPR3 gene expression in WT, opr3 and opr3 MYB21OE-1. Total RNA was extracted from the young flower buds. ACTIN was used as the normalization control. (B) Comparison of the flowers at stage 14 in different genotypes. The flower in opr3 MYB21OE-1 shows elongated filament than that in opr3. (C and D) Comparison of seed set in different genotypes as shown (C) and of plant growth of WT (Col-0) (50 days old), opr3 (50 days old) and opr3 MYB21OE-1. The third plant from left was an opr3 MYB21OE-1 plant with primary shoot (50 days old) whereas the last plant was a 60-day-old opr3 MYB21OE-1 with axillary shoots after its primary influence has been removed earlier. White arrows highlight siliques with seed set, red arrows highlight sterile siliques.
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pgen-1000440-g009: Overexpression of MYB21 Rescues the Stamen Filament Growth and Fertility to the opr3 Mutant.(A) RT-PCR analysis of MYB21 and OPR3 gene expression in WT, opr3 and opr3 MYB21OE-1. Total RNA was extracted from the young flower buds. ACTIN was used as the normalization control. (B) Comparison of the flowers at stage 14 in different genotypes. The flower in opr3 MYB21OE-1 shows elongated filament than that in opr3. (C and D) Comparison of seed set in different genotypes as shown (C) and of plant growth of WT (Col-0) (50 days old), opr3 (50 days old) and opr3 MYB21OE-1. The third plant from left was an opr3 MYB21OE-1 plant with primary shoot (50 days old) whereas the last plant was a 60-day-old opr3 MYB21OE-1 with axillary shoots after its primary influence has been removed earlier. White arrows highlight siliques with seed set, red arrows highlight sterile siliques.

Mentions: To test our hypothesis that GA acts through JA to control expression of the MYB genes to promote filament elongation, we fused MYB21 gene with the CaMV35S promoter (pCAMBIA1301 vector) and this construct was used to generate transgenic plants in the opr3 mutant background. Semi-quantitative RT-PCR showed that MYB21 was overexpressed in the transgenic plants in the opr3 background (Figure 9A). We found that overexpression of MYB21 could restore the stamen filament growth (Figure 9B) and restore the fertility (Figure 9C and 9D) to the opr3 mutant partially. Together with the fact that loss of function of four DELLA (GAI, RGA, RGL1 and RGL2) could not restore the fertility and filament elongation to the coil1 mutant (Figure S6), we have now provided strong evidence to show that GAs act through JA to control expression of the MYBs and promote stamen filament elongation.


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)

Overexpression of MYB21 Rescues the Stamen Filament Growth and Fertility to the opr3 Mutant.(A) RT-PCR analysis of MYB21 and OPR3 gene expression in WT, opr3 and opr3 MYB21OE-1. Total RNA was extracted from the young flower buds. ACTIN was used as the normalization control. (B) Comparison of the flowers at stage 14 in different genotypes. The flower in opr3 MYB21OE-1 shows elongated filament than that in opr3. (C and D) Comparison of seed set in different genotypes as shown (C) and of plant growth of WT (Col-0) (50 days old), opr3 (50 days old) and opr3 MYB21OE-1. The third plant from left was an opr3 MYB21OE-1 plant with primary shoot (50 days old) whereas the last plant was a 60-day-old opr3 MYB21OE-1 with axillary shoots after its primary influence has been removed earlier. White arrows highlight siliques with seed set, red arrows highlight sterile siliques.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000440-g009: Overexpression of MYB21 Rescues the Stamen Filament Growth and Fertility to the opr3 Mutant.(A) RT-PCR analysis of MYB21 and OPR3 gene expression in WT, opr3 and opr3 MYB21OE-1. Total RNA was extracted from the young flower buds. ACTIN was used as the normalization control. (B) Comparison of the flowers at stage 14 in different genotypes. The flower in opr3 MYB21OE-1 shows elongated filament than that in opr3. (C and D) Comparison of seed set in different genotypes as shown (C) and of plant growth of WT (Col-0) (50 days old), opr3 (50 days old) and opr3 MYB21OE-1. The third plant from left was an opr3 MYB21OE-1 plant with primary shoot (50 days old) whereas the last plant was a 60-day-old opr3 MYB21OE-1 with axillary shoots after its primary influence has been removed earlier. White arrows highlight siliques with seed set, red arrows highlight sterile siliques.
Mentions: To test our hypothesis that GA acts through JA to control expression of the MYB genes to promote filament elongation, we fused MYB21 gene with the CaMV35S promoter (pCAMBIA1301 vector) and this construct was used to generate transgenic plants in the opr3 mutant background. Semi-quantitative RT-PCR showed that MYB21 was overexpressed in the transgenic plants in the opr3 background (Figure 9A). We found that overexpression of MYB21 could restore the stamen filament growth (Figure 9B) and restore the fertility (Figure 9C and 9D) to the opr3 mutant partially. Together with the fact that loss of function of four DELLA (GAI, RGA, RGL1 and RGL2) could not restore the fertility and filament elongation to the coil1 mutant (Figure S6), we have now provided strong evidence to show that GAs act through JA to control expression of the MYBs and promote stamen filament elongation.

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