Brassinosteroid and TPD1 signaling pathways redundantly control anther lobe formation in Arabidopsis thaliana.

Abstract

Sharing the most recent common ancestor, receptor-like kinases EXCESS MICROSPOROCYTES1 (EMS1) and BRASSINOSTEROID INSENSITIVE1 (BRI1) family members respectively perceive the peptide ligand TAPETUM DETERMINANT1 (TPD1) and the phytohormone brassinosteroids (BRs) to activate the same downstream BRI1 EMS SUPPRESSOR1 (BES1)/BRASSINAZOLE RESISTANT1 (BZR1) transcription factor family. Yet only their distinct canonical functions have been revealed. TPD1 specifically sustains tapetum development but is dispensable for global plant growth, whereas BRs regulate overall plant growth without impacting tapetum development. This generates a fundamental evolutionary conflict: gradual biochemical divergence with saltational biological diversification. Here, we identify an unrecognized redundant role of TPD1 and BR signaling in controlling early anther lobe formation. Simultaneous disruption of both pathways causes a lobeless anther defect, phenocopying the loss of the entire BES1/BZR1 family. Single-pathway disruption produces no such defect. Interestingly, we found that pathway specificity during tapetum development is caused by spatiotemporal ligand dynamics. The expression of DWF4 (encoding a rate-limiting BR biosynthetic enzyme) decreases sharply at the onset of tapetum development, while TPD1 expression remains stable. Consistently, exogenous BR application or the introduction of an active, ligand-independent BRI1 rescues tapetum defects in either the ems1 mutant or the dual-pathway-deficient mutant background. Our findings reconcile biochemical divergence and biological diversification with gradual evolution, likely stimulating study of the functional divergence of numerous other receptor-like kinases at multiple levels.