Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock in Chlamydomonas triploids

Genome merging is a common phenomenon in many organisms, causing a wide range of consequences on phenotype, adaptation, and gene expression, among other effects, yet its broader implications are not well understood. Two consequences of genome merging on gene expression remain poorly understood: dosage effects and evolution of expression. In this study, we employed Chlamydomonas reinhardtii as a model to investigate the effects of asymmetric genome merging by crossing a diploid with a haploid strain to create a novel triploid line. Five independent clonal lineages derived from this triploid line were evolved for 425 asexual generations in a laboratory natural selection (LNS) experiment. Utilizing fitness assays, qPCR, and RNA-Seq, we assessed the immediate consequences of genome merging and subsequent evolution over time. Our findings reveal substantial alterations in gene expression, protein homeostasis (proteostasis) and cytonuclear stoichiometry. Notably, gene expression exhibited expression level dominance and transgressivity (i.e., expression level higher or lower than either parent). Ongoing expression level dominance and a pattern of “functional dominance” from the haploid parent was observed, alongside remarkable stability in expression patterns across generations. Despite major nucleo-cytoplasmic disruptions, enhanced fitness was detected in the triploid strain. By comparing gene expression across generations, our results indicate that proteostasis restoration is a critical component of rapid adaptation following genome merging in Chlamydomonas reinhardtii and possibly other systems.