1535American Journal of Botany 91(10): 1535–1556. 2004.GREEN ALGAE AND THE ORIGIN OF LAND PLANTS1LOUISEA. LEWIS2,4ANDRICHARDM. MCCOURT3,42Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269 USA; and3Department ofBotany, Academy of Natural Sciences, 1900 Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103 USAOver the past two decades, molecular phylogenetic data have allowed evaluations of hypotheses on the evolution of green algaebased on vegetative morphological and ultrastructural characters. Higher taxa are now generally recognized on the basis of ultrastruc-tural characters. Molecular analyses have mostly employed primarily nuclear small subunit rDNA (18S) and plastid rbcL data, as wellas data on intron gain, complete genome sequencing, and mitochondrial sequences. Molecular-based revisions of classification at nearlyall levels have occurred, from dismemberment of long-established genera and families into multiple classes, to the circumscription oftwo major lineages within the green algae. One lineage, the chlorophyte algae or Chlorophyta sensu stricto, comprises most of whatare commonly called green algae and includes most members of the grade of putatively ancestral scaly flagellates in Prasinophyceaeplus members of Ulvophyceae, Trebouxiophyceae, and Chlorophyceae. The other lineage (charophyte algae and embryophyte landplants), comprises at least five monophyletic groups of green algae, plus embryophytes. A recent multigene analysis corroborates aclose relationship between Mesostigma (formerly in the Prasinophyceae) and the charophyte algae, although sequence data of theMesostigma mitochondrial genome analysis places the genus as sister to charophyte and chlorophyte algae. These studies also supportCharales as sister to land plants. The reorganization of taxa stimulated by molecular analyses is expected to continue as more dataaccumulate and new taxa and habitats are sampled.Key words: Chlorophyta; Charophyta; DNA; Mesostigma; Streptophytina; ultrastructure.Twenty years ago, a relatively slim volume with chaptersby leading chlorophycologists celebrated the systematics ofgreen algae (Irvine and John, 1984), a field that was under-going rapid and fascinating changes, both in content and the-ory. ‘‘The present period may be termed the ‘Age of Ultra-structure’ in green algal systematics,’’ wrote Frank Round(1984, p. 7) in the introductory chapter, which summarized thehistory and state of the art. Round (1984) argued that lightmicroscopy had laid the foundation in the preceding two cen-turies, but that the foundation was largely descriptive—alphataxonomy in the most restricted sense. Ultrastructure, he as-serted, had enlarged and presumably would continue to expandour horizons to unify systematics of green algae and overcomethe fragmented alpha taxonomy that had dominated the field.Little did Round know that this golden age of green algalsystematics was about to go platinum. Molecular systematics,in concert with a rigorous theoretical approach to data analysisand hypothesis testing (Theriot, 1992; Swofford et al., 1996),would at first complement and then transform the age of ul-trastructure and usher in the ‘‘Age of Molecules.’’In this article, we review the major advances in green algalsystematics in the past 20 years, with a focus on well-sup-ported, monophyletic taxa and the larger picture of phylogenyand evolution of green algae. We will review the types of datathat have fueled these advances. As will become obvious, thisperspective entails discussion of some embryophytes as wellas their closest green algal relatives. In addition, we will point1Manuscript received 15 January 2004; revision accepted 15 June 2004.The authors thank F. Zechman, M. Fawley, C. Lemieux, C. Delwiche, E.Harris, and R. Chapman for helpful advice and unpublished data. We aregreatly appreciative of F. Trainor and two anonymous reviewers who providedextensive comments on the manuscript. Kyle Luckenbill did the line drawingartwork, and Ste´phane Marty prepared the color plate and cell images. Theauthors acknowledge support from National Aeronautics and Space Admin-istration to LAL (EXB02–0042–0054) and the National Science Foundationto RMM (DEB 9978117).4Authors contributed equally to this work. E-mail: [email protected] major uncertainties in green algal systematics, which posesome of the most provocative areas for further research.Deconstructing hypotheses of relationships of the greenalgae and land plants—A link between green algae and landplants has been clear to biologists for centuries, since beforeDarwin and the advent of evolutionary thinking and phylo-genetics (Smith, 1950; Prescott, 1951). Recent new data onmorphology, genes, and genomes, as well as new ways ofanalyzing and synthesizing information, are only the most re-cent in a long history of change in our understanding of theseso-called ‘‘primitive’’ plants. This review focuses primarily onresearch that has led to both some radical restructuring of theclassification of algae and some satisfying confirmations of thecareful observations of earlier workers.First and foremost, green algae, the division Chlorophyta ofSmith (1950), are undoubtedly monophyletic with embryo-phyte green plants, although the Chlorophyta in this sense isparaphyletic (Mattox and Stewart, 1984; Mishler and Chur-chill, 1985; McCourt, 1995). Embryophytes (land plants;bryophytes and vascular plants) are clearly descended fromgreen algal-like ancestors, but the sister of the embryophytesincludes only a few green algae. The remainder of Chloro-phyta constitutes a monophyletic group. This major bifurcationin green plant evolution implies a single common ancestor tothe two lineages, but, given the diversity of unicellular greenalgae and our growing understanding of them, there may beadditional lineages outside this major bifurcation.What are green algae?—The term algae is not phyloge-netically meaningful without qualifiers. Algae in general andgreen algae in particular are difficult to define to the exclusionof other phylogenetically related organisms that are not algae.This difficulty is a reflection of recent data on algae as wellas the way phylogenetic thinking has permeated classification.Green algae are photosynthetic eukaryotes bearing doublemembrane-bound plastids containing chlorophyll a and b, ac-cessory pigments found in embryophytes (beta carotene and1536
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