Early Sexual Origins of Homeoprotein Heterodimerization and Evolution of the Plant KNOX/BELL Family

Abstract

Developmental mechanisms that yield multicellular diversity are proving to be well conserved within lineages, generating interest in their origins in unicellular ancestors. We report that molecular regulation of the haploid-diploid transition in Chlamydomonas, a unicellular green soil alga, shares common ancestry with differentiation pathways in land plants. Two homeoproteins, Gsp1 and Gsm1, contributed by gametes of plus and minus mating types respectively, physically interact and translocate from the cytosol to the nucleus upon gametic fusion, initiating zygote development. Their ectopic expression activates zygote development in vegetative cells and, in a diploid background, the resulting zygotes undergo a normal meiosis. Gsm1/Gsp1 dyads share sequence homology with and are functionally related to KNOX/BELL dyads regulating stem-cell (meristem) specification in land plants. We propose that combinatorial homeoprotein-based transcriptional control, a core feature of the fungal/animal radiation, may have originated in a sexual context and enabled the evolution of land-plant body plans.

Seaweed reproductive biology: environmental and genetic controls

“…Regarding the genetic mechanism underlying the full program of zygote development, GSP1 originating from plus gametes and GSM1 originating from minus gametes both contribute to zygote development, including the resorption of flagella, fusion of nuclei and chloroplasts, destruction of minus gamete G-chloroplast DNA, and secretion of a resistant cell wall (Wilson et al 1999). Earlier studies showed that the ectopic expression of GSP1 in minus gametes or of GSM1 in plus gametes can switch the zygotic differentiation programme on, and the resulting zygotes could undergo a normal meiosis (Zhao et al 2001, Lee et al 2008. Further research has uncovered the functional homology between GSP1/GSM1 and KNOX/BELL, which regulate stem-cell specification in land plants (Lee et al 2008).…”

“…Earlier studies showed that the ectopic expression of GSP1 in minus gametes or of GSM1 in plus gametes can switch the zygotic differentiation programme on, and the resulting zygotes could undergo a normal meiosis (Zhao et al 2001, Lee et al 2008. Further research has uncovered the functional homology between GSP1/GSM1 and KNOX/BELL, which regulate stem-cell specification in land plants (Lee et al 2008). Both genes are conserved among algae, although they appear to be lost in some lineages (Trebouxiophyceae, Gonium, Chondrus and Saccharina, see Supplemental Table S1).…”

Green Algae and the Origins of Multicellularity in the Plant Kingdom

“…Interestingly, the genetic program that directs sporophyte development in the bryophyte moss Physcomitrella is directed by a KNOX family homeodomain transcription factor whose homologs in the chlorophyte alga C. reinhardtii direct development of the dormant diploid zygospore formed after fertilization (Lee et al 2008;Nishimura et al 2012;Sakakibara et al 2013). The role of these homeodomain proteins in charophyte algae has not been examined, but they are predicted to participate in zygote development.…”

The evolutionary development of plant body plans

“…Indeed, combinatorial homeodomainbased transcriptional control of reproduction has deep phylogenetic roots. Ectopic expression of the homeoproteins Gsp1 and Gsm1 in the plus and minus strains of the unicellular green alga Chlamydomonas activates vegetative cells to form zygote-like structures (Lee et al 2008). Gsp1 and Gsp2 are members of the TALE (three amino acid loop extension) homeodomain containing transcription factors, which includes the class 1 KNOX and class 2 KNOX proteins.…”