Charophyte algae and land plant origins

doi:10.1016/j.tree.2004.09.013

Trends in Ecology & Evolution

Volume 19, Issue 12, December 2004, Pages 661-666

https://doi.org/10.1016/j.tree.2004.09.013 Get rights and content

The charophyte algae are six distinct groups of mostly freshwater green algae that are related to modern land plants. Charophyte algae exhibit diverse morphologies and reproductive strategies, from unicells to branching erect forms, and from swimming asexual spores to sex involving eggs and sperm, respectively. The green algae known as stoneworts (Charales) are suggested to be the extant sister group to all land plants, although the phylogeny is not conclusive. Here we review recent molecular phylogenetic work on the charophyte algae and its implications for our understanding of the origins of land plants and of characters in their aquatic ancestors that might have played a role in the explosive diversification of plants on land.

Section snippets

Chlorophyte and charophyte algae

The close evolutionary relationship of green plants to green algae (Chlorophyta sensu lato) has been long accepted, but the diversity of form (unicells to multicellular) and life cycles (with one or two free-living stages in the life cycle) among green algae led to diverse hypotheses about which taxa gave rise to land-dwelling descendants. Frederick O. Bower's [3] early 20th-century book about the evolution of land plants and their life cycles framed the debate about the origin of a land flora

Genes and genomes unravel charophyte algal phylogeny

Recent molecular phylogenetic studies support the monophyly of individual charophyte algal groups and of most of the charophyte algal groups plus land plants (the exception being Mesostigma, which is discussed in detail below). However, the branching order of groups within the phylogeny has been uncertain 13, 14, 15, 16, 17, 18, 19, 20, 21. Hypotheses of relationships among charophyte algae have developed in a piecemeal fashion, as subsets of taxa from several groups were sampled one gene at a

From simple to complex?

Despite the uncertainty of some of the branches in Figure 1, some inferences can be drawn about the derivation of characters that might have played a role in the morphological elaboration of embryophytes. Groups near the base of the tree are either unicellular (e.g. Mesostigmatales) or consist of packets of a few cells (e.g. Chlorokybus). Later diverging groups are multicellular and exhibit various types of branching through cell division (Box 1). Similarly, sexual reproduction is absent or

The fossil record and timing of divergence

The fossil record of most charophyte algae is scarce and provides few clues to phylogeny, and minimum dates for some groups might be greatly underestimated [37]. However, fossils are abundant for Charales and several related extinct groups. Calcified oogonia of these algae (gyrogonites) first occur in deposits of the lower Silurian [425 million years ago (Mya)] and extinct taxa are more diverse than extant forms 24, 38. Fossils of other charophyte algal groups are known only from rocks younger

The enigma of Mesostigma

The placement of the unicellular Mesostigma viride, the sole known member of Mesostigmatales, has been the focus of several studies that have yielded conflicting results. This scaly flagellate unicell was initially classified in a paraphyletic assemblage of unicellular algae (Class Prasinophyceae) [5]. Later study of ultrastructural features led to its placement in the lineage of charophyte algae and land plants [51], which meant it might resemble the unicellular ancestor of the group.

Acknowledgements

We thank Kyle Luckenbill for the artwork and preparation of Figure 1, Scott Kroken for advice on identifying the moss photograph, and several anonymous reviewers for criticisms of the article. This material is based upon work supported by the National Science Foundation under Grant No. DEB 9978117.

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View full text

Trends in Ecology & Evolution

Charophyte algae and land plant origins

Section snippets

Chlorophyte and charophyte algae

Genes and genomes unravel charophyte algal phylogeny

From simple to complex?

The fossil record and timing of divergence

The enigma of Mesostigma

Acknowledgements

Trends Ecol. Evol.

Mol. Phylog. Evol.

Protist

Mol. Phylog. Evol.

Origin of Land Plants

Algae

The Origin of a Land Flora: A Theory Based on the Facts of Alternation

The Origin and Early Diversification of Land Plants: A Cladistic Study

Classification of the green algae: a concept based on comparative cytology

Introduction to the Algae. Structure and Reproduction

The closest living relatives of land plants

Science

Algal evolution and the early radiation of green plants

The association of rosette and globule terminal complexes with cellulose microfibril assembly in Nitella translucens var. axillaris (Charophyceae)

J. Phycol.

Evolution of the cellulosic cell wall in the Charophyceae

A new putative cellulose-synthesizing complex of Coleochaete scutata

Protoplasma

Algal phylogeny and the origin of land plants

Plant Physiol.

Molecular systematics of the green algae

Phylogeny of the genus Coleochaete (Coleochaetales, Charophyta) and related taxa inferred by analysis of the chloroplast gene rbcL

J. Phycol.

Charophyte evolution and the origin of land plants

Plant Syst. Evol.

The origin of land plants: phylogenetic relationships among charophytes, bryophytes, and vascular plants inferred from complete small-subunit ribosomal RNA gene sequences

J. Mol. Evol.

Phylogeny of the Chlorophyta – congruence between ultrastructural and molecular evidence

Bull. Soc. Zool. France Evol. Zool.

Group I introns are inherited through common ancestry in the nuclear-encoded rRNA of Zygnematales (Charophyceae)

Proc. Natl. Acad. Sci. U. S. A.

Phylogeny of the conjugating green algae (Zygnemophyceae) based on rbcL sequences

J. Phycol.

Phylogeny of extant genera in the family Characeae (Charales, Charophyceae) based on rbcL sequences and morphology

Am. J. Bot.

Bayesian inference of phylogeny and its impact on evolutionary biology

Science

Phylogenetic inference

Origin, evolution, and metabolic role of a novel glycolytic GAPDH enzyme recruited by land plant plastids

J. Mol. Evol.