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

Shota Yamashita,Shigekatsu Suzuki,Yohei Minakuchi,Masanobu Kawachi,Shunsuke Hirooka,Kayoko Yamamoto,Ryo Matsuzaki,Haruyo Yamaguchi,Atsushi Toyoda,Hisayoshi Nozaki,Shin-Ya Miyagishima

doi:10.1038/s41598-021-01521-x

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.

Highlights

The evolution from unicellular to multicellular organisms is one of the major transitions in evolution, during which individual lower-level units are integrated into a higher-level u nit[1,2]
Among the multicellular traits observed in the volvocine green algae, differentiation between somatic cells and reproductive cells has been a central topic of evolutionary biology for more than a century, since Weismann pointed out the germ-soma differentiation of Volvox in his Germ-plasm t heory[17]
Germ-soma differentiation is a pivotal trait in convergent evolution, as it has occurred in many multicellular lineages and contributed to the evolution of multicellular c omplexity[3,22]

Summary

Introduction

The evolution from unicellular to multicellular organisms is one of the major transitions in evolution, during which individual lower-level units are integrated into a higher-level u nit[1,2]. One of the best model groups for examining the initial evolution of multicellularity is volvocine green algae[5] (Fig. 1a). This group, which consists of Volvox and its closely related genera, includes organisms of various intermediate stages of multicellular complexity, ranging from unicellular Chlamydomonas to multicellular Volvox with germ-soma division of labor in the expanded multicellular body (spheroid). Diverse molecular biology tools are available in Chlamydomonas reinhardtii and Volvox carteri[12,13] and are potentially applicable to other volvocine s pecies[14,15,16] This group is a suitable model for the stepwise evolution of multicellular complexity at both the genetic and genomic level. Previous studies of V. carteri have revealed specialization of somatic cells for flagellar motility and ECM biosynthesis and the specialization of reproductive cells for photosynthesis and anabolism, at the transcriptomic level[30,31,32]

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