Evolution of osmosensing OSCA1 Ca2+ channel family coincident with plant transition from water to land

Abstract

Water is crucial to plant growth, development, and environmental adaptation. Water stress triggers cytosolic Ca²⁺ ([Ca²⁺ ]_i ) increases, and the osmosensor OSCA1 (REDUCED-HYPEROSMOLALITY-INDUCED-[Ca²⁺ ]_i -INCREASE 1), a member of the OSCA family, perceives the initial water stress and governs its downstream responses. OSCA homologs exist in eukaryotes and largely radiate in higher plants. However, it is enigmatic whether the OSCA family is crucial for plant evolution from aqueous to terrestrial environments and for the subsequent adaptation on land. Here, we carried out the first phylogenetic and molecular evolutionary analyses of the OSCA family. The family originated and diversified during the early evolution of protists, and three more lineages were established (a) in plants, (b) in fungi, and (c) in a complex clade of several major eukaryotic lineages. The chlorophyte algal cluster is directly basal to streptophyte-specific Clades 1-3, consistent with plant transition from water to land. The Clades 1-3 present different gene expansion pattern and together with previous functional analysis of OSCAs reveal that they probably have evolved diverse functions in respond to various mechanical stresses during the independent evolution of land plant clades. Moreover, variable selection pressures on different land plant lineages were explored. OSCAs in early land plants (mosses and lycophytes) were under decelerated evolution, whereas OSCAs in seed plants showed accelerated evolution. Together, we hypothesize OSCAs have evolved to sense water stress in the ancestor of euphyllophytes, which occupies typical leaves, typical roots, and phloem tissues, all of which require osmosensors to maintain water balance and food conduction through plant bodies.