TALE homeobox heterodimer GSM1/GSP1 is a molecular switch that prevents unwarranted genetic recombination in Chlamydomonas

Abstract

Eukaryotic sexual life cycles alternate between haploid and diploid stages, the transitions between which are delineated by cell fusion and meiotic division. Transcription factors in the TALE-class homeobox family, GSM1 and GSP1, predominantly control gene expression for the haploid-to-diploid transition during sexual reproduction in the unicellular green alga, Chlamydomonas reinhardtii. To understand the roles that GSM1 and GSP1 play in zygote development, we used gsm1 and gsp1 mutants and examined fused gametes that normally undergo the multiple organellar fusions required for the genetic unity of the zygotes. In gsm1 and gsp1 zygotes, no fusion was observed for the nucleus and chloroplast. Surprisingly, mitochondria and endoplasmic reticulum, which undergo dynamic autologous fusion/fission, did not undergo heterologous fusions in gsm1 or gsp1 zygotes. Furthermore, the mutants failed to resorb their flagella, an event that normally renders the zygotes immotile. When gsm1 and gsp1 zygotes resumed the mitotic cycle, their two nuclei fused prior to mitosis, but neither chloroplastic nor mitochondrial fusion took place, suggesting that these fusions are specifically turned on by GSM1/GSP1. Taken together, this study shows that organellar restructuring during zygotic diploidization does not occur by default but is triggered by a combinatorial switch, the GSM1/GSP1 dyad. This switch may represent an ancient mechanism that evolved to restrict genetic recombination during sexual development.