BES1 is activated by EMS1-TPD1-SERK1/2-mediated signaling to control tapetum development in Arabidopsis thaliana

Weiyue Chen,Xiaoping Gou,Yanze Wang,Jia Li,Yanwei Cui,Minghui Lv,Meizhen Li,Ruoshi Wang,Ping-An Wang

doi:10.1038/s41467-019-12118-4

Weiyue Chen, Xiaoping Gou + Show 7 more

Open Access

https://doi.org/10.1038/s41467-019-12118-4

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Abstract

BES1 and BZR1 were originally identified as two key transcription factors specifically regulating brassinosteroid (BR)-mediated gene expression. They belong to a family consisting of six members, BES1, BZR1, BEH1, BEH2, BEH3, and BEH4. bes1 and bzr1 single mutants do not exhibit any characteristic BR phenotypes, suggesting functional redundancy of these proteins. Here, by generating higher order mutants, we show that a quintuple mutant is male sterile due to defects in tapetum and microsporocyte development in anthers. Our genetic and biochemical analyses demonstrate that BES1 family members also act as downstream transcription factors in the EMS1-TPD1-SERK1/2 pathway. Ectopic expression of both TPD1 and EMS1 in bri1-116, a BR receptor null mutant, leads to the accumulation of non-phosphorylated, active BES1, similar to activation of BES1 by BRI1-BR-BAK1 signaling. These data suggest that two distinctive receptor-like kinase-mediated signaling pathways share BES1 family members as downstream transcription factors to regulate different aspects of plant development.

Highlights

BRASSINOSTEROID INSENSITIVE 1 (BRI1) EMS SUPPRESSOR 1 (BES1) and BRASSINAZOLE RESISTANT 1 (BZR1) were originally identified as two key transcription factors regulating brassinosteroid (BR)-mediated gene expression
Phylogenic analysis indicated that BES1 and BZR1 belong to a six-member family, including BES1, BZR1, BEH1, BEH2, BEH3, and BEH4 (Supplementary Fig. 1)
Genotypic analyses confirmed the true T-DNA insertions for BES1, BZR1, BEH1, BEH3, and BEH4, but not for BEH2. These five T-DNA insertion lines were subsequently named as bes[1], bzr[1], beh[1], beh[], and beh[], respectively (Supplementary Fig. 2a)

Summary

Introduction

BES1 and BZR1 were originally identified as two key transcription factors regulating brassinosteroid (BR)-mediated gene expression. Our genetic and biochemical analyses demonstrate that BES1 family members act as downstream transcription factors in the EMS1-TPD1-SERK1/2 pathway. Ectopic expression of both TPD1 and EMS1 in bri[1-116], a BR receptor null mutant, leads to the accumulation of non-phosphorylated, active BES1, similar to activation of BES1 by BRI1-BR-BAK1 signaling. These data suggest that two distinctive receptor-like kinase-mediated signaling pathways share BES1 family members as downstream transcription factors to regulate different aspects of plant development. Recent studies suggested that carbonic anhydrases act as direct targets of EMS1 in regulating tapetal cell differentiation, how activated TPD1-EMS1/ SERK1/2 complex triggers downstream response gene expression is not fully understood[41]

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