Elsevier

Gene

Volume 769, 15 February 2021, 145203
Gene

Review
Tracking the evolutionary innovations of plant terrestrialization

https://doi.org/10.1016/j.gene.2020.145203Get rights and content

Highlights

  • The mechanism of plant terrestrialization is crucial for understanding plant evolution.

  • The recent report of high-quality reference genomes of six species sheds light on this question.

  • Early diverging plants could have gained new genes through horizontal gene transfer.

  • Horizontal gene transfer is vital for adapting new environment during plant terrestrialization.

Abstract

The gradual transition of the algal ancestor from the freshwater to land has always attracted evolutionary biologists. The recent report of high-quality reference genomes of five Charophyta algae (Spirogloea muscicola, Mesotaenium endlicherianum, Mesostigma viride, Chlorokybus atmophyticus and Penium margaritaceum) and one hornwort (Anthoceros angustus) species sheds light on this fascinating transition. These early diverging plants and algae could have gained new genes from soil bacteria and fungi through horizontal gene transfer (HGT), which was so common during plant terrestrialization and may outrun our expectations. Through reviewing and critical thinking about the advancements on these plant genomes, here, I propose three prospective research directions that need to address in the future: (i) due to the ubiquitous nature of viruses that is similar to soil bacteria and fungi, there is less attention to viruses that probably also play an important role in the genome evolution of plants via HGT; (ii) multicellularity has occurred many times independently, but we still know a little about the biological and ecological mechanisms leading to multi-cellularity in Streptophyta; (iii) and most importantly, the quantitative relationships between genetic innovations and environmental variables such as temperature, precipitation and solar radiation, need pioneering research collaborated by biological evolutionists, computer scientists, and ecologists, which are crucial for understanding the macroevolution of plants and could also be used to simulate the evolution of plants under future climate change.

Introduction

Our diverse plant world might have originated from a subaerial/terrestrial unicellular alga. Today's >380,000 of land plant species (Embryophyta) with morphological and functional diversities are mainly attributed to two major evolutionary events (Bowles et al., 2020). The first is the evolution of life from single-cell to multi-cells; the second is the gradual transition to land from the aquatic and survive in the more variable terrestrial environment. Compared with the aquatic environment, the terrestrial environment is characterized by reduced moisture, enhanced ultraviolet radiation, sudden changes in temperature, and increased damage by herbivores/pathogens (de Vries and Archibald, 2018). For centuries, the gradual transition of the algal ancestor from the freshwater to the terrestrial environment has always attracted biologists, ecologists, and geneticists (Bowles et al., 2020, Zhang, 1998).

Plant genome contains the most critical information of plant evolution, physiological functions and genetic variations. With the advancement of sequencing technology and the sharp drop in sequencing costs, more and more plant genomes have been sequenced and released during these years. By comparing plant genomes of different lineages, the derived conclusions could help us explore the evolutionary route of multicellularity in algae (Hanschen et al., 2016), the evolutionary innovations of plant terrestrialization (Bowles et al., 2020, de Vries et al., 2018, Delaux et al., 2015, Radhakrishnan et al., 2020), the development of stomata, and the genetic basis for angiosperms to become the most successful plant lineage on Earth (Chen et al., 2020, Twyford, 2018). For example, the gradual transition of the algal ancestor and the underlying mechanisms from the freshwater to land is an old question in evolutionary biology.

Section snippets

Horizontal gene transfer

For centuries, people are curious about which plant species (or lineage) might be the common ancestor of extant land plants and how did the first land plants evolve step by step from aquatic to terrestrial successfully. Recently, Cheng et al. (2019) found that Zygnematophyceae algae (Spirogloea muscicola and Mesotaenium endlicherianum) had a large number of core gene families previously thought to be unique to land plants, such as genes involved in plant hormones, symbiosis with bacteria and

Pre-adaptation of terrestrialization

The transition from freshwater to land is a big leap in plant evolution and lots of morphological and molecular changes are needed for this adaption. Wang et al. (2020) sequenced the genomes of two Charophyta Mesostigma viride, a unicellular green algae in freshwater (Liang et al., 2020) and Chlorokybus atmophyticus, a multicellular algae living in subaerial/terrestrial, both are members of the earliest lineages of Streptophyta. These ancient Charophyta algae are ideal model to study earliest

Jigsaw of the bryophytes’ genomes

The bryophytes originated ~500 Mya and have been an intriguing plant lineage to study the evolution of land plants (Lang et al., 2018). While the Embryophyta (land plants) could be dated back to ~580 Mya (Morris et al., 2018), the divergences between bryophytes and other tracheophytes (vascular plants) probably dated back to ~470 Mya, suggesting bryophytes might be listed as monophyletic and a sister group to tracheophytes (Puttick et al., 2018). Bryophytes are relatively primitive land plants

Conclusions and future perspectives

These studies on early diverging plants are encouraging and have extraordinary significance, especially the single-celled S. muscicola (or P. margaritaceum) that dated back to Precambrian terrestrial that might be the candidate common ancestor of land plants (Cheng et al., 2019, Jiao et al., 2020), which probably can be used to explain the “Cambrian Explosion” that perplexed Charles Darwin. The “Cambrian Explosion” was an event ~540 Mya in the Cambrian period when almost all present (including

Declaration of Competing Interest

The author declares that there are no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

I am grateful to five anonymous reviewers for constructive suggestions on this manuscript. I would like to acknowledge Professor Shu-Nong Bai (Peking University) and Zhong-Jian Liu (Fujian Agriculture and Forestry University) for their critical comments on this manuscript. I would also like to thank Professor Pamela Diggle (University of Connecticut) for critical reading of this article.

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