Broad Phylogenomic Sampling and the Sister Lineage of Land Plants

Tsvetan R. Bachvaroff,Ruth E. Timme,Charles F. Delwiche,Simon Joly

doi:10.1371/journal.pone.0029696

Tsvetan R. Bachvaroff, Ruth E. Timme + Show 2 more

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https://doi.org/10.1371/journal.pone.0029696

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Abstract

The tremendous diversity of land plants all descended from a single charophyte green alga that colonized the land somewhere between 430 and 470 million years ago. Six orders of charophyte green algae, in addition to embryophytes, comprise the Streptophyta s.l. Previous studies have focused on reconstructing the phylogeny of organisms tied to this key colonization event, but wildly conflicting results have sparked a contentious debate over which lineage gave rise to land plants. The dominant view has been that ‘stoneworts,’ or Charales, are the sister lineage, but an alternative hypothesis supports the Zygnematales (often referred to as “pond scum”) as the sister lineage. In this paper, we provide a well-supported, 160-nuclear-gene phylogenomic analysis supporting the Zygnematales as the closest living relative to land plants. Our study makes two key contributions to the field: 1) the use of an unbiased method to collect a large set of orthologs from deeply diverging species and 2) the use of these data in determining the sister lineage to land plants. We anticipate this updated phylogeny not only will hugely impact lesson plans in introductory biology courses, but also will provide a solid phylogenetic tree for future green-lineage research, whether it be related to plants or green algae.

Highlights

It is hard to imagine what the planet looked like 500 million years ago, before green algae first colonized the terrestrial habitat
We included published Sanger sequences from a Mesostigma viride EST library [12] and analyzed them alongside our in-house transcriptomes. From these data we identified a set of orthologs common across the green lineage (Chlorophyta+Streptophyta) using an unbiased approach
We believe our results warrant serious reconsideration of charophyte evolution given that the phylogenomic approach of our study confirms the plastid-encoded analyses of Turmel et al [9] and the recent nuclear-genomic study of Wodniok et al [10]

Summary

Introduction

It is hard to imagine what the planet looked like 500 million years ago, before green algae first colonized the terrestrial habitat. Microfossils and fragments of plant tissue from the middle Ordovician (458–470 mya) reveal evidence of the first plant colonizers [1,2], but these pioneering species and their green-algal progenitors have long since disappeared Descendants of these early pioneers are widespread, which begs the question: Which extant green algal group is the closest living relative of land plants?. It was nearly a decade ago that Karol et al [3] concluded after a four-gene, three genome analysis that, of the charophytes, the Charales constitute the closest living relative to land plants Another combined data analysis [4] supported the same topology and, for a time, this appeared to be a settled matter. Sexual reproduction evolves from isogamy in the ancestral lineages to oogamy into the more derived charophyte lineages

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