Significance Cytoskeletal actin microfilaments have roles in cell-shape determination, motility, membrane trafficking, and cell division. Actin filaments respond dynamically to environmental changes and shifting cellular needs, and functionally different actin subtypes may play important roles in such responses. The alga Chlamydomonas has two actins: IDA5, an actin of conventional sequence that is expressed in normal growing cells, and NAP1, a divergent actin that is normally not expressed. Disruption of IDA5 filaments results in rapid transcriptional induction of NAP1 and hundreds of other genes, rapidly replacing all IDA5 filaments with NAP1 filaments, in part by proteasome-mediated degradation of IDA5. This system allows resistance of Chlamydomonas to actin-depolymerizing drugs and probably also compensates for other, diverse actin cytoskeletal perturbations, whether intrinsic or induced.