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.

Deep evolutionary origin of gamete-directed zygote activation by KNOX/BELL transcription factors in green plants

“…KNOX proteins heterodimerize with BELL proteins to regulate gene transcription (Hay and Tsiantis, 2010). In C. reinhardtii , a minus gamete-derived KNOX protein (GSM1) heterodimerizes with a plus gamete-derived BELL protein (GSP1) upon fertilization and activates the majority of early zygote-specific genes (Joo et al, 2017, Kariyawasam et al, 2019, Lee et al, 2008, Lopez et al, 2015, Nishimura et al, 2012). Loss of GSM1 and/or GSP1 results in delayed pronuclear fusion, a phenotype similar to that of Mp knox1 mutants.…”

“…Upon fertilization, the two proteins heterodimerize and translocate to both male and female pronuclei to activate the expression of early zygote-specific genes. Loss-of-function mutations in either GSP1 or GSM1 result in pleiotropic phenotypes involving cellular rearrangements in zygotes, such as the loss of nuclear and mitochondrial fusion, lack of selective degradation of minus -derived chloroplast DNA and chloroplast membrane fusion, and defects in flagella resorption (Joo et al, 2017, Kariyawasam et al, 2019, Lee et al, 2008, Lopez et al, 2015, Nishimura et al, 2012).…”

Homeoprotein transduction in neurodevelopment and physiopathology

“…GSM1 and GSP1 belong to the Knotted and Bell family of homeoproteins, respectively, raising the possibility that they can transfer between gametes before fusion (63). Accordingly, de novo protein synthesis, which is required to maintain flagellar adhesion during gamete activation (90), would depend on GSM1 and/or GSP1 transfer before cell fusion (91,92).…”

Gamete-specific expression of TALE class HD genes activates the diploid sporophyte program inMarchantia polymorpha

“…This maternal zygotically produced MpBELL34 could then heterodimerize with MpKNOX1 and initiate the embryo genetic program. Such a scenario is reminiscent of Chlamydomonas where, in the absence of GSM1 (KNOX), GSP1 (BELL) can induce diploid gene expression(Kariyawasam et al, 2019). It was proposed that in wt(+) x gsm1(-) zygotes GSM1 may be activated by its upstream regulator MID supplied by the (-) gamete(Kariyawasam et al, 2019).…”

“…Such a scenario is reminiscent of Chlamydomonas where, in the absence of GSM1 (KNOX), GSP1 (BELL) can induce diploid gene expression(Kariyawasam et al, 2019). It was proposed that in wt(+) x gsm1(-) zygotes GSM1 may be activated by its upstream regulator MID supplied by the (-) gamete(Kariyawasam et al, 2019). Fourth, maternal expression of MpBELL5 could play a role, perhaps by forming heterodimers, with MpKNOX1 upon a fertilization stimulus, able to initiate, but not sustain, embryo development.Given the phylogenetic affinity of mosses as a sister group to liverworts(Renzaglia et al, 2018), we suggest that expression of PpBELL1 in the sperm as observed by Ortiz-Ramírez et al(Ortiz-Ramírez et al, 2017) is genuine and that the earlier reported lack of male expression(Horst et al, 2016) may be related to sterility in the particular Physcomitrella strain (Meyberg…”