BAM3 Is a CLE19 Receptor that Mediates a Distinct Signaling Branch Controlling Tapetum Degeneration and Pollen Wall Formation

Abstract

Pollen wall formation requires precise coordination between tapetum differentiation, metabolism, and programmed cell death. In Arabidopsis, the microspore-derived peptide CLE19 restricts tapetal activity to maintain pollen wall homeostasis, yet how CLE19 signaling achieves developmental specificity and robustness remains unclear. Here, we identify the receptor-like kinase BARELY ANY MERISTEM 3 (BAM3) as an additional receptor for CLE19. Genetic, cytological, biochemical, and transcriptomic analyses showed that disruption of BAM3 signaling impairs tapetum differentiation, secretory homeostasis, and pollen exine patterning, resulting in selective transcriptional reprogramming during anther development. Comparative transcriptomic analyses reveal that BAM3 mediates a distinct subset of CLE19-responsive genes, including both AMS-dependent pathways governing tapetal degeneration and exine biosynthesis, and AMS-independent programs associated with flavonoid metabolism and pollen wall development. Biochemical assays, structure-guided mutagenesis, and AlphaFold3 modeling further support CLE19-dependent assembly of BAM3-SERK1/2 receptor complex, revealing a conserved molecular framework for CLE19 perception that is distinct from, yet complementary to, the previously characterized CLE19–PXL1–SERK1/2 receptor module. Together, these findings establish a dual-receptor architecture for CLE19 signaling in which BAM3 mediates a transcriptionally distinct branch of the CLE19 pathway. More broadly, this work demonstrates how combinatorial peptide-receptor usage expands the signaling capacity of a single developmental peptide to coordinate robust male reproductive development.