Polygalacturonase45 cleaves pectin and links cell proliferation and morphogenesis to leaf curvature in Arabidopsis thaliana

Regulating plant architecture is a major goal in current breeding programs. Previous studies have increased our understanding of the genetic regulation of plant architecture, but it is also essential to understand how organ morphology is controlled at the cellular level. In the cell wall, pectin modification and degradation are required for organ morphogenesis, and these processes involve a series of pectin-modifying enzymes. Polygalacturonases (PGs) are a major group of pectin-hydrolyzing enzymes that cleave pectin backbones and release oligogalacturonides (OGs). PG genes function in cell expansion and separation, and contribute to organ expansion, separation and dehiscence in plants. However, whether and how they influence other cellular processes and organ morphogenesis are poorly understood. Here, we characterized the functions of Arabidopsis PG45 (PG45) in organ morphogenesis using genetic, developmental, cell biological and biochemical analyses. A heterologously expressed portion of PG45 cleaves pectic homogalacturonan in vitro, indicating that PG45 is a bona fide PG. PG45 functions in leaf and flower structure, branch formation and organ growth. Undulation in pg45 knockout and PG45 overexpression leaves is accompanied by impaired adaxial–abaxial polarity, and loss of PG45 shortens the duration of cell proliferation in the adaxial epidermis of developing leaves. Abnormal leaf curvature is coupled with altered pectin metabolism and autogenous OG profiles in pg45 knockout and PG45 overexpression leaves. Together, these results highlight a previously underappreciated function for PGs in determining tissue polarity and regulating cell proliferation, and imply the existence of OG-based signaling pathways that modulate plant development.