Genome sequencing of the multicellular alga Astrephomene provides insights into convergent evolution of germ-soma differentiation

Abstract

Germ-soma differentiation evolved independently in many eukaryotic lineages and contributed to complex multicellular organizations. However, the molecular genetic bases of such convergent evolution remain unresolved. Two multicellular volvocine green algae, Volvox and Astrephomene, exhibit convergent evolution of germ-soma differentiation. The complete genome sequence is now available for Volvox, while genome information is scarce for Astrephomene. Here, we generated the de novo whole genome sequence of Astrephomene gubernaculifera and conducted RNA-seq analysis of isolated somatic and reproductive cells. In Volvox, tandem duplication and neofunctionalization of the ancestral transcription factor gene (RLS1/rlsD) might have led to the evolution of regA, the master regulator for Volvox germ-soma differentiation. However, our genome data demonstrated that Astrephomene has not undergone tandem duplication of the RLS1/rlsD homolog or acquisition of a regA-like gene. Our RNA-seq analysis revealed the downregulation of photosynthetic and anabolic gene expression in Astrephomene somatic cells, as in Volvox. Among genes with high expression in somatic cells of Astrephomene, we identified three genes encoding putative transcription factors, which may regulate somatic cell differentiation. Thus, the convergent evolution of germ-soma differentiation in the volvocine algae may have occurred by the acquisition of different regulatory circuits that generate a similar division of labor.

The Genetics of Fitness Reorganization During the Transition to Multicellularity: The Volvocine regA-Like Family as a Model

“…Gonium species have 8 -16 Chlamydomonas-like cells arranged as a flat plate. Whereas Astrephomene species are 32 or 64-celled spheroidal colonies with 2 to 4 sterile somatic cells in the posterior of the colony (Coleman, 2012;Hanschen et al, 2016;Yamashita et al, 2021). The Volvocaceae is the largest and most diverse family of volvocine green algae with many polyphyletic genera.…”

“…Based on currently available whole genome sequence data, the VARL gene family contains 12 members in C. reinhardtii (Duncan et al, 2007), 8 in Gonium pectorale (Hanschen et al, 2016) and Tetrabaena socialis (Featherston et al, 2018), 6 in Astrephomene gubernaculifera (Yamashita et al, 2021), and 14 in V. carteri (Duncan et al, 2007). With the exception of regA orthologs (when present), all other regA homologs are known as regA-like sequences: annotated as RLS1-12 in Chlamydomonas and Goniaceae or rlsA-O in Volvocaceae.…”

“…To date, regA orthologs have been found in every member of the Volvocaceae family that was investigated (including species without somatic cells) but appear to be absent in volvocine species outside of the Volvocaceae (Duncan et al, 2007;Featherston et al, 2018;Grochau-Wright et al, 2017Hanschen et al, 2014Hanschen et al, , 2016Yamashita et al, 2021). In all species with a regA ortholog for which complete genome sequence is available, the gene is found in a syntenic gene cluster of 4 -5 paralogs of closely related VARL genes called the regA cluster (Figures 2 & 5).…”

“…Astrephomene species are the only volvocine algae outside of the Volvocaceae that have cellular differentiation, but unlike Volvox and Pleodorina species the somatic cells of Astrephomene are located in the posterior of the colony due to the lack of an inversion process during development (Yamashita et al, 2016). In addition, Astrephomene does not possess the regA gene and evolved somatic cells independently of other volvocine algae (Grochau-Wright et al, 2017;Lindsey et al, 2021;Yamashita et al, 2021)(Figure 2).…”

Cryopreservation of two species of the multicellular volvocine green algal genus Astrephomene

“…S1) [5][6][7]. Whole-genome sequencing of A. gubernaculifera provided insight into the molecular-genetic basis of such convergent evolution [8]. Thus, Astrephomene represents a hopeful key organism for studies of multicellularity and germ-soma differentiation.…”