American Journal of Botany 91 10 1535 1556 2004 GREEN ALGAE AND THE ORIGIN OF LAND PLANTS1 LOUISE A LEWIS2 4 AND RICHARD M MCCOURT3 4 Department of Ecology and Evolutionary Biology University of Connecticut Storrs Connecticut 06269 USA and 3Department of Botany Academy of Natural Sciences 1900 Benjamin Franklin Parkway Philadelphia Pennsylvania 19103 USA 2 Over the past two decades molecular phylogenetic data have allowed evaluations of hypotheses on the evolution of green algae based on vegetative morphological and ultrastructural characters Higher taxa are now generally recognized on the basis of ultrastructural characters Molecular analyses have mostly employed primarily nuclear small subunit rDNA 18S and plastid rbcL data as well as data on intron gain complete genome sequencing and mitochondrial sequences Molecular based revisions of classification at nearly all levels have occurred from dismemberment of long established genera and families into multiple classes to the circumscription of two major lineages within the green algae One lineage the chlorophyte algae or Chlorophyta sensu stricto comprises most of what are commonly called green algae and includes most members of the grade of putatively ancestral scaly flagellates in Prasinophyceae plus members of Ulvophyceae Trebouxiophyceae and Chlorophyceae The other lineage charophyte algae and embryophyte land plants comprises at least five monophyletic groups of green algae plus embryophytes A recent multigene analysis corroborates a close relationship between Mesostigma formerly in the Prasinophyceae and the charophyte algae although sequence data of the Mesostigma mitochondrial genome analysis places the genus as sister to charophyte and chlorophyte algae These studies also support Charales as sister to land plants The reorganization of taxa stimulated by molecular analyses is expected to continue as more data accumulate and new taxa and habitats are sampled Key words Chlorophyta Charophyta DNA Mesostigma Streptophytina ultrastructure Twenty years ago a relatively slim volume with chapters by leading chlorophycologists celebrated the systematics of green algae Irvine and John 1984 a field that was undergoing rapid and fascinating changes both in content and theory The present period may be termed the Age of Ultrastructure in green algal systematics wrote Frank Round 1984 p 7 in the introductory chapter which summarized the history and state of the art Round 1984 argued that light microscopy had laid the foundation in the preceding two centuries but that the foundation was largely descriptive alpha taxonomy in the most restricted sense Ultrastructure he asserted had enlarged and presumably would continue to expand our horizons to unify systematics of green algae and overcome the fragmented alpha taxonomy that had dominated the field Little did Round know that this golden age of green algal systematics was about to go platinum Molecular systematics in concert with a rigorous theoretical approach to data analysis and hypothesis testing Theriot 1992 Swofford et al 1996 would at first complement and then transform the age of ultrastructure and usher in the Age of Molecules In this article we review the major advances in green algal systematics in the past 20 years with a focus on well supported monophyletic taxa and the larger picture of phylogeny and evolution of green algae We will review the types of data that have fueled these advances As will become obvious this perspective entails discussion of some embryophytes as well as their closest green algal relatives In addition we will point Manuscript 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 are greatly appreciative of F Trainor and two anonymous reviewers who provided extensive comments on the manuscript Kyle Luckenbill did the line drawing artwork and Ste phane Marty prepared the color plate and cell images The authors acknowledge support from National Aeronautics and Space Administration to LAL EXB02 0042 0054 and the National Science Foundation to RMM DEB 9978117 4 Authors contributed equally to this work E mail louise lewis uconn edu out major uncertainties in green algal systematics which pose some of the most provocative areas for further research Deconstructing hypotheses of relationships of the green algae and land plants A link between green algae and land plants has been clear to biologists for centuries since before Darwin and the advent of evolutionary thinking and phylogenetics Smith 1950 Prescott 1951 Recent new data on morphology genes and genomes as well as new ways of analyzing and synthesizing information are only the most recent in a long history of change in our understanding of these so called primitive plants This review focuses primarily on research that has led to both some radical restructuring of the classification of algae and some satisfying confirmations of the careful observations of earlier workers First and foremost green algae the division Chlorophyta of Smith 1950 are undoubtedly monophyletic with embryophyte green plants although the Chlorophyta in this sense is paraphyletic Mattox and Stewart 1984 Mishler and Churchill 1985 McCourt 1995 Embryophytes land plants bryophytes and vascular plants are clearly descended from green algal like ancestors but the sister of the embryophytes includes only a few green algae The remainder of Chlorophyta constitutes a monophyletic group This major bifurcation in green plant evolution implies a single common ancestor to the two lineages but given the diversity of unicellular green algae and our growing understanding of them there may be additional lineages outside this major bifurcation 1 What are green algae The term algae is not phylogenetically meaningful without qualifiers Algae in general and green algae in particular are difficult to define to the exclusion of other phylogenetically related organisms that are not algae This difficulty is a reflection of recent data on algae as well as the way phylogenetic thinking has permeated classification Green algae are photosynthetic eukaryotes bearing double membrane bound plastids containing chlorophyll a and b accessory pigments found in embryophytes beta carotene and 1535 1536 AMERICAN JOURNAL xanthophylls and a unique stellate structure linking nine pairs of microtubules in the flagellar base Mattox and Stewart 1984
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