Abstract

The Streptophyta include unicellular and multicellular charophyte green algae and land plants. Colonization of the terrestrial habitat by land plants is a major evolutionary event that has transformed the planet. So far, lack of genome information on unicellular charophyte algae hinders the understanding of the origin and the evolution from unicellular to multicellular life in Streptophyta. This work reports the high‐quality reference genome and transcriptome of Mesostigma viride, a single‐celled charophyte alga with a position at the base of Streptophyta. There are abundant segmental duplications and transposable elements in M. viride, which contribute to a relatively large genome with high gene content compared to other algae and early diverging land plants. This work identifies the origin of genetic tools that multicellular Streptophyta have inherited and key genetic innovations required for the evolution of land plants from unicellular aquatic ancestors. The findings shed light on the age‐old questions of the evolution of multicellularity and the origin of land plants.

Highlights

  • One of the most important evolutionary innovations in the history of life is multicellularity, which contains simple and complex forms with elaborate cell–cell communication and network of genetic interactions for co­ordinated cell division and differentiation.[1]

  • We performed RNA sequencing (RNA-seq) on small RNAs, long noncoding RNAs and mRNAs isolated from M. viride using a combination of Illumina and Pacific Biosciences (PacBio) sequencing technologies (Table S1D, Supporting Information)

  • We report the high-quality genome of M. viride, which is the first sequenced unicellular genome in the Streptophyta division, which include land plants that colonized and transformed the terrestrial habitat of our planet

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Summary

Introduction

One of the most important evolutionary innovations in the history of life is multicellularity, which contains simple (colonial, filamentous) and complex forms with elaborate cell–cell communication and network of genetic interactions for co­ordinated cell division and differentiation.[1]. Demko Department of Plant Physiology Faculty of Natural Sciences Comenius University in Bratislava Bratislava 84215, Slovakia. Mesostigma viride is an extant unicellular biflagellate freshwater charophyte algae covered by an outer layer of basket-like scales instead of cell wall (Figure 1A,B; Figure S1, Supporting Information). It is the only known flagellate charophyte algae with a multilayered structure,[8] and is one of the earliest diverging members of streptophytes.[6,9] This crucial phylogenetic position in the evolution of green plants makes M. viride an essential model for understanding the evolution of multicellularity and the origin of land plants. Comparative analyses of its genome and transcriptome with those of other green algae and early diverging land plants allow us to identify the origin of key genetic tools that multicellular charophyte algae and land plants have either inherited or created during the evolution from unicellular to multicellular green plants for colonization of the terrestrial habitat in our planet

Mesostigma viride Genome Assembly and Annotation
Gene and Genome Evolution
Duplication and Repetitive Sequences
Evolutionary Novelties of Multicellularity and Land Plant Heritage Genes
The Split of Charophyta and Chlorophyta
Cell Division and Cell Wall Synthesis
Transcriptional Regulation
Phytohormones
Epigenetic Regulation
Small RNA
RNA Methylation
Sexual Reproduction
Stress Response to Environmental Conditions
Conclusion
Experimental Section
Conflict of Interest
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