Molecular and functional adaption of Arabidopsis villins.

Abstract

Villins are versatile, multifunctional actin regulatory proteins. They promote actin stabilization and remodeling mainly via their actin bundling and Ca²⁺-dependent severing activities, respectively. Arabidopsis subclass II and III villins normally coexist in cells, but the biological significance of their coexistence remains unknown. Here we demonstrate that subclass II villin binds to Ca²⁺ with high affinity and exhibits strong severing but weak bundling activity compared to subclass III villin. Subclass II villin plays a dominant role in promoting actin remodeling, which requires its Ca²⁺-dependent severing activity. Subclass II villin is also strictly required for physiological processes including oriented organ growth and stress tolerance. By comparison, subclass III villin binds to Ca²⁺ with low affinity and exhibits weak severing but strong bundling activity, and acts as the major player in controlling actin stabilization and organization. Thus, we demonstrate that multifunctional villin isovariants have diverged biochemically to ensure exquisite control of the actin cytoskeleton to meet different cellular needs in plants. This study provides new insights into the role of villins in fine-tuning actin dynamics and plant development.