Gibberellin Acts through Jasmonate to Control the Expression of MYB21, MYB24, and MYB57 to Promote Stamen Filament Growth in Arabidopsis

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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. Gibberellin and jasmonate are plant hormones that mediate diverse plant developmental processes and responses to the environment. Deficiency in either gibberellin or jasmonate causes male sterility, in part due to the short stamen filament conferred. In this report, we sought to study the interaction between gibberellin and jasmonate during stamen filament development. We focused on three MYB genes, namely MYB21, MYB24, and MYB57, which have been proven to be essential for stamen filament development in Arabidopsis. These three MYB genes are regulated by both gibberellin and jasmonate. We performed various molecular analyses and found that GA activates the expression of DAD1 and LOX1, two genes essential for jasmonate biosynthesis. The hypothesis of GA regulating JA biosynthesis is proved by the fact that the JA content in the young flower buds of the ga1-3 gai-t6 rga-t2 rgl1-1 quadruple mutant is much lower than that in the WT. This evidence demonstrates that GA promotes the production of jasmonate and high level of jasmonate will induce the expression of MYB21, MYB24, and MYB57 to promote stamen filament development. This is most likely the first molecular and genetic evidence to show how gibberellin and jasmonate interact to control stamen filament development.