Ascomycete fungal actins differentially support plant spatial cell and organ development

Actin interacts with a wide variety of cytoplasmic and nuclear proteins to support spatial development in nearly all eukaryotes. Null mutations in plant vegetative actins produce dramatically altered cell, tissue, and organ morphologies. Animal cytoplasmic actins (e.g., human HsACTB, HsACTG1) and some ancestral protist actins fully suppress these mutant phenotypes suggesting that some animal, plant, and protist actins share functional competence for spatial development. Considering that fungi have a phylogenetic origin closer to animals than plants, we were interested to explore whether the fungal actins may have this same capacity to function in plants and support development. We ectopically expressed actins from four highly divergent ascomycete fungi in two different Arabidopsis double vegetative actin null mutants. We found that expression of actin from the earliest diverging ascomycete subphyla, the archiascomycete Schizosaccharomyces pombe, qualitatively and quantitatively suppressed the root cell polarity and root organ developmental defects of act8/act7 mutants and the root-hairless cell elongation phenotype of act2/act8 mutants. Interestingly, the actin from the pyrenomycete Neurospora crassa was modestly effective in the suppression of vegetative actin mutant phenotypes. In contrast, actins from the saccharomycetes Saccharomyces cerevisiae and Candida albicans were unable to support any aspect of plant development, and moreover induced severe dwarfism and sterility. These data imply that basal fungi inherited an actin with full competence for spatial development from their protist ancestor and maintained it via non-progressive sequence evolution, while the later more derived fungal species lost these activities.