What contributions have the authors mentioned in the paper "Phylogeny and molecular evolution of the green algae" ?

Leliaert et al. this paper reported that the green lineage diverged early from the remaining Chlorophyta, but the relationships among these lineages remain largely unresolved, mainly because multi-gene data are only available for a limited number of taxa.

Why are the stoneworts well represented in the fossil record?

Because the sporopollenin surrounding the zygotes is highly resistant to degradation and because the shallow freshwater habitats in which they live often create favourable depositional conditions, the stoneworts are well represented in the fossil record (fossilized zygote walls are called gyrogonites).

What is the main problem in multi-gene phylogenetic investigations?

A persistent problem in many of the multi-gene phylogenetic investigations thus far is sparse and incomplete taxon sampling, which may result in systematic errors in phylogenetic reconstruction.

What is the appeal of the organisms as a model system?

Their appeal as a model system stems from the relative simplicity of their development and from the wide range of sizes and degrees of complexity found in extant species.

What are the biochemical innovations that have been identified?

Several biochemical innovations have been identified, including synthesis and accumulation of protective “sunscreens,” plant growth hormones, isoprene, phenolics, heat shock proteins, and enhanced DNA repair mechanisms (Waters, 2003; Rensing et al., 2008).

What is the prominent endosymbiosis in eukaryo?

The two most prominent endosymbioses in eukaryote evolution have involved an alpha-proteobacterial and a cyanobacterial endosymbiont, and have given rise to mitochondria and plastids, respectively (Keeling and Palmer, 2008).

Why is the marine planktonic compartment of picoeukaryotes overlooked?

The marine planktonic compartment of picoeukaryotes has been previously overlooked because of the extremely small size of its constituents (1–3µm).

What is the significance of the phylogenomic analysis of two diatom genomes?

Phylogenomic analyses of two diatom genomes revealed that a considerable proportion of nuclear genes are of green algal origin, which is surprising given that diatom plastids are of red algal origin (Moustafa et al., 2009).

What are the recent advances in high-throughput DNA sequencing?

Recent advances in high-throughput DNA sequencing, including Roche-454 and Illumina-Solexa (Shendure and Ji, 2008; Metzker, 2010) facilitate rapid sequencing of organellar genomes, transcriptomes and entire nuclear genomes.

What are the traits that are unique to the remaining streptophytes?

Additional traits that are uniquely shared by the remaining streptophytes include apical growth (not in the Zygnematophyceae), sexual reproduction, some biochemical features, and similar cellulose-synthesizing rosettes (Tsekos, 1999).

What is the role of cytoplasmic streaming in siphonous algae?

In addition to facilitating transport of transcripts as mentioned above, the evolution of cytoplasmic streaming in siphonous algae also allowed transport of nutrients and organelles throughout the siphonous algal body.

What is the reason for the similar architectures of green algal genomes?

the comparable architectures of green algal plastid and mitochondrial DNAs may be a consequence of these genomes having similar mutation rates, as reflected in their similar rates of silent-site substitution.

What is the function of EF-1 in eukaryotes?

Despite this crucial function, not all eukaryotes have this protein, and it has been shown that an elongation factor-like protein (EF-like) can substitute for EF-1α in these taxa (Keeling and Inagaki, 2004).

what is the phylogenetic position of the klebsormidiophy?

This phylogenetic position is further supported by some chloroplast genomic features, such as the presence of introns in two transfer RNAs which is shared between Klebsormidium and the later-diverging streptophyte lineages, and the presence of functional plastid tufA, which is shared with the early-diverging lineages (Baldauf et al., 1990; Baldauf and Palmer, 1990; Manhart and Palmer, 1990; Turmel et al., 2005; Turmel et al., 2007b) (Figure 4).

(Open Access) Phylogeny and Molecular Evolution of the Green Algae (2012) | Frederik Leliaert

Q: Why were ribosomal sequences chosen at the time?

Ribosomal sequences were chosen at the time because enough RNA could be obtained for direct sequencing and (later) because regions of the gene were conserved enough to make universal primers.

Critical Reviews in Plant Sciences, 31:1–46, 2012



Taylor & Francis Group, LLC

ISSN: 0735-2689 print / 1549-7836 online

DOI: 10.1080/07352689.2011.615705

Phylogeny and Molecular Evolution of the Green Algae

Frederik Leliaert,

David R. Smith,

Herv

eMoreau,

Matthew D. Herron,

Heroen Verbruggen,

Charles F. Delwiche,

and Olivier De Clerck

Phycology Research Group, Biology Department, Ghent University 9000, Ghent, Belgium

Canadian Institute for Advanced Research, Evolutionary Biology Program, Department of Botany,

University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

Observatoire Oc

eanologique, CNRS–Universit

e Pierre et Marie Curie 66651, Banyuls sur Mer, France

Department of Zoology, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada

Department of Cell Biology and Molecular Genetics and the Maryland Agricultural Experiment Station,

University of Maryland, College Park, MD 20742, USA

Table of Contents

I. THE NATURE AND ORIGINS OF GREEN ALGAE AND LAND PLANTS

.............................................................................2

II. GREEN LINEAGE RELATIONSHIPS

..........................................................................................................................................................5

A. Morphology, Ultrastructure and Molecules

...............................................................................................................................................5

B. Phylogeny of the Green Lineage

...................................................................................................................................................................6

1. Two Main Lineages: Chlorophyta and Streptophyta

........................................................................................................................6

2. Early Diverging Chlorophyta: The Prasinophytes

.............................................................................................................................6

3. The Core Chlorophyta: Ecological and Morphological Diversiﬁcation

....................................................................................9

4. Streptophyta: Charophyte Green Algae and the Origin of Land Plants

.................................................................................. 15

III. SPREAD OF GREEN GENES IN OTHER EUKARYOTES

............................................................................................................ 17

IV. GREEN ALGAL EVOLUTION: INSIGHTS FROM GENES AND GENOMES

................................................................... 19

A. Organelle Genome Evolution

...................................................................................................................................................................... 20

B. Ecology and Molecular Evolution of Oceanic Picoplanktonic Prasinophytes

........................................................................... 25

C. Genomic Insights into the Evolution of Complexity in Volvocine Green Algae

...................................................................... 26

D. Genetic Codes and the Translational Apparatus in Green Seaweeds ............................................................................................ 29

E. Molecular Evolution in the Streptophyta and the Origin of Land Plants

..................................................................................... 30

V. CONCLUSIONS AND PERSPECTIVES

................................................................................................................................................... 31

ACKNOWLEDGMENTS

................................................................................................................................................................................................ 32

REFERENCES

..................................................................................................................................................................................................................... 32

Address correspondence to Frederik Leliaert, Phycology Research Group, Biology Department, Ghent University, 9000, Ghent, Belgium.

E-mail: frederik.leliaert@gmail.com

Downloaded by [University of Gent] at 07:28 14 February 2012

2 F. LELIAERT ET AL.

The green lineage (Viridiplantae) comprises the green algae and

their descendants the land plants, and is one of the major groups of

oxygenic photosynthetic eukaryotes. Current hypotheses posit the

early divergence of two discrete clades from an ancestral green ﬂag-

ellate. One clade, the Chlorophyta, comprises the early diverging

prasinophytes, which gave rise to the core chlorophytes. The other

clade, the Streptophyta, includes the charophyte green algae from

which the land plants evolved. Multi-marker and genome scale

phylogenetic studies have greatly improved our understanding of

broad-scale relationships of the green lineage, yet many questions

persist, including the branching orders of the prasinophyte lin-

eages, the relationships among core chlorophyte clades (Chloroden-

drophyceae, Ulvophyceae, Trebouxiophyceae and Chlorophyceae),

and the relationships among the streptophytes. Current phyloge-

netic hypotheses provide an evolutionary framework for molecular

evolutionary studies and comparative genomics. This review sum-

marizes our current understanding of organelle genome evolution

in the green algae, genomic insights into the ecology of oceanic

picoplanktonic prasinophytes, molecular mechanisms underlying

the evolution of complexity in volvocine green algae, and the evo-

lution of genetic codes and the translational apparatus in green

seaweeds. Finally, we discuss molecular evolution in the strepto-

phyte lineage, emphasizing the genetic facilitation of land plant

origins.

Keywords Chlorophyta, Charophyta, endosymbiosis, molecular evo-

lution, origin of embryophytes, Prasinophyceae, phy-

logeny, Streptophyta

I. THE NATURE AND ORIGINS OF GREEN ALGAE

AND LAND PLANTS

The green lineage or Viridiplantae

includes the green algae

and land plants, and is one of the major groups of oxygenic pho-

tosynthetic eukaryotes. Green algae are diverse and ubiquitous

in aquatic and some terrestrial habitats, and they have played

a crucial role in the global ecosystem for hundreds of millions

of years (Falkowski et al., 2004; O’Kelly, 2007; Leliaert et al.,

2011). The evolution of land plants from a green algal ancestor

was a key event in the history of life and has led to dramatic

changes in the earth’s environment, initiating the development

of the entire terrestrial ecosystem (Kenrick and Crane, 1997).

The green lineage originated following an endosymbiotic

event in which a heterotrophic eukaryotic host cell captured a

cyanobacterium that became stably integrated and ultimately

turned into a plastid (Archibald, 2009; Keeling, 2010). This

primary endosymbiosis, which likely happened between 1 and

1.5 billion years ago (Hedges et al., 2004; Yoon et al., 2004),

marked the origin of the earliest oxygenic photosynthetic eu-

karyotes. The subsequent diversiﬁcation of this primary plastid-

Various names have been proposed for the lineage comprising the green

algae and land plants: “Viridiplantae” or “Viridaeplantae” (Cavalier-Smith,

1981, 1998), “Chlorobiota” or “Chlorobionta” (Jeffrey, 1971, 1982), “Chloro-

plastida” (Adl et al. 2005), or simply “green plants” (Sluiman et al., 1983) or

“green lineage.”

containing eukaryote gave rise to the green lineage, as well as

the red algae and the glaucophytes. From this starting point, pho-

tosynthesis spread widely among diverse eukaryotic protists via

secondary and tertiary endosymbioses, which involved captures

of either green or red algae by non-photosynthetic protists (Keel-

ing, 2010). Secondary endosymbioses involving green algae as

the autotrophic partner have given rise to three groups of algae:

the chlorarachniophytes, the photosynthetic euglenids and the

“green” dinoﬂagellates (see section III. Spread of green genes in

other eukaryotes). The other eukaryotic algal groups, the cryp-

tophytes, haptophytes, photosynthetic stramenopiles (e.g., di-

atoms, chrysophytes and brown seaweeds) and dinoﬂagellates,

have acquired plastids from a red algal ancestor, either by a sin-

gle or multiple endosymbiotic events (Archibald, 2009; Bodyl

et al., 2009; Baurain et al., 2010).

The green lineage is ancient, and dating its origin has been

a difﬁcult task because of the sparse fossil record of the group.

The earliest fossils attributed to green algae date from the Pre-

cambrian (ca. 1200 mya) (Tappan, 1980; Knoll, 2003). The na-

ture of these early fossils, however, remains controversial (e.g.,

Cavalier-Smith, 2006). The resistant outer walls of prasinophyte

cysts (phycomata) are well preserved in fossil deposits and es-

pecially abundant and diverse in the Paleozoic era (ca. 250–

540 mya) (Parke et al., 1978; Tappan, 1980; Colbath,

1983). A ﬁlamentous fossil (Proterocladus) from middle

Neoproterozoic deposits (ca. 750 mya) has been attributed

to siphonocladous green algae (Cladophorales) (Butterﬁeld

et al., 1994; Butterﬁeld, 2009), while the oldest reli-

able records of the siphonous seaweeds (Bryopsidales,

Dasycladales) and stoneworts (Charophyceae) are from

the Paleozoic (Hall and Delwiche, 2007; Verbruggen et

al., 2009a). The earliest land plant fossils are Mid-

Ordovician in age (ca. 460 mya) (Kenrick and Crane, 1997;

Steemans et al., 2009). Molecular clock analyses have esti-

mated the origin of the green lineage between 700 and 1500

mya (Douzery et al., 2004; Hedges et al., 2004; Berney and

Pawlowski, 2006; Roger and Hug, 2006; Herron et al., 2009).

These estimates are sensitive to differences in methodology and

interpretation of fossils and tend to yield older dates than are

well supported by the fossil record. This could be attributable

to miscalibration of the molecular clock estimates or to tapho-

nomic bias and the difﬁculty of interpreting fossils with no

modern exemplars. Molecular phylogenetic evidence has pro-

vided a substantially improved understanding of the relation-

ships among major lineages. Reconstruction of ancestral char-

acter states could assist in the reinterpretation of known spec-

imens of uncertain afﬁnity, and this, combined with continued

paleontological investigation, holds out hope for reconciliation

of molecular and fossil evidence.

Green algae are characterized by a number of distinct fea-

tures, many of which are also shared with the land plants (van

den Hoek et al., 1995; Graham et al., 2009). The chloroplasts

are enclosed by a double membrane with thylakoids grouped

in lamellae, and contain chlorophyll a and b along with a

Downloaded by [University of Gent] at 07:28 14 February 2012

MOLECULAR EVOLUTION OF GREEN ALGAE 3

set of accessory pigments such as carotenes and xanthophylls.

Pyrenoids, when present, are embedded within the chloroplast

and are surrounded by starch, which is the main reserve polysac-

charide. Most green algae have ﬁrm cell walls with a ﬁber matrix

generally composed of cellulose. The ﬂagellate cells are isokont,

which means that the two ﬂagella are similar in structure, al-

though they may differ in length. The ﬂagellar transition zone

(i.e., the region between the ﬂagellum and its basal body) is

typically characterized by a stellate structure, which is a nine-

pointed star, visible in cross section using an electron micro-

scope, linking nine pairs of microtubules (Melkonian, 1984).

Despite their many unifying features, green algae exhibit

a remarkable variation in morphology and ecology reﬂect-

ing their evolutionary diversiﬁcation. Morphological diversity

ranges from the smallest known free-living eukaryote, Ostreo-

coccus tauri, to large, multicellular life forms (Figure 1). Green

algae are especially abundant and diverse in freshwater envi-

ronments, including lakes, ponds, streams and wetlands (John

et al., 2002; Wehr and Sheath, 2003), where they may form

nuisance blooms under conditions of nutrient pollution (Malkin

et al., 2010). Only two green algal groups are well represented

in marine environments. The green seaweeds (Ulvophyceae)

abound in coastal habitats. Some green seaweeds (mainly Ulva)

can form extensive, free-ﬂoating coastal blooms, called ‘green

tides’ (Leliaert et al., 2009c); others, like Caulerpa and Codium

are notorious for their invasive nature (Meinesz and Hesse, 1991;

Jousson et al., 2000; Lapointe et al., 2005). The prasinophytes

are planktonic green algae that occur mainly in oceanic environ-

ments and are especially abundant in more eutrophic, near-shore

waters, where they can form monospeciﬁc blooms (O’Kelly

et al., 2003; Not et al., 2004). Embryophytes have dominated

the terrestrial environment since the late Ordovician, and some

have become secondarily adapted to aquatic environments, in-

cluding holoaquatic marine species that form extensive beds of

seagrass. Several green algae have adapted to highly specialised

or extreme environments, such as hot or cold deserts (Lewis

and Lewis, 2005; De Wever et al., 2009; Schmidt et al., 2011),

hypersaline habitats (Vinogradova and Darienko, 2008), acidic

waters with extreme concentrations of heavy metals (Zettler

et al., 2002), marine deep waters (Zechman et al., 2010) and

deep-sea hydrothermal vents (Edgcomb et al., 2002). Some

green algal groups, i.e., Trentepohliales, are exclusively terres-

trial and never found in aquatic environments (L

opez-Bautista

et al., 2006). Several lineages have engaged in symbiosis with a

diverse range of eukaryotes, including fungi to form lichens, cil-

iates, foraminifers, cnidarians, molluscs (nudibranchs and giant

clams) and vertebrates (Friedl and Bhattacharya, 2002; Lewis

and Muller-Parker, 2004; Kovacevic et al., 2010; Kerney et al.,

2011). Others have evolved an obligate heterotrophic life style as

parasites or free-living species (Joubert and Rijkenberg, 1971;

Rumpf et al., 1996; Huss et al., 1999; Nedelcu, 2001). The

heterotrophic green alga Prototheca, which grows in sewage

and soil, can cause infections in humans and animals known as

protothecosis (Sudman, 1974).

Several green algae serve as model systems or are of eco-

nomic importance. Melvin Calvin used cultures of Chlorella

to elucidate the light-independent reactions of photosynthesis.

Now known as the Calvin cycle (Calvin and Benson, 1948).

Transplant experiments with the giant-celled Acetabularia, con-

ducted by Joachim H

ammerling, demonstrated that the nucleus

of a cell contains the genetic information that directs cellular

development, and postulated the existence of messenger RNA

before its structure was determined (H

ammerling, 1953). Ac-

etabularia, along with other giant-celled green algae (Valonia,

Chara and Nitella), has also served as an experimental organism

for electro-physiological research and studies of cell morpho-

genesis (Menzel, 1994; Mandoli, 1998; Shepherd et al., 2004;

Bisson et al., 2006; Mine et al., 2008). The charophyte Mougeo-

tia played a key role in outlining the role of phytochrome in

plant development (Winands and Wagner, 1996). The biochem-

istry and physiology of the unicellular, halophilic Dunaliella

salina have been studied in great detail. This alga is among the

most industrially important microalgae because it can produce

massive amounts of β-carotene that can be collected for com-

mercial purposes, and because of its potential as a feedstock for

biofuels production (Oren, 2005; Gouveia and Oliveira, 2009;

Tafresh and Shariati, 2009). The unicellular ﬂagellate Chlamy-

domonas reinhardtii has long been used as a model system

for studying photosynthesis, chloroplast biogenesis, ﬂagellar

assembly and function, cell-cell recognition, circadian rhythm

and cell cycle control because of its well-deﬁned genetics, and

the development of efﬁcient methods for nuclear and chloroplast

transformation (Rochaix, 1995; Harris, 2001; Grossman et al.,

2003; Breton and Kay, 2006). The colonial green alga Volvox

has served as a model for the evolution of multicellularity, cell

differentiation, and colony motility (Kirk, 1998; Kirk, 2003;

Herron and Michod, 2008; Herron et al., 2009).

Analysis of the complete nuclear genome sequence of C.

reinhardtii greatly advanced our understanding of ancient eu-

karyotic features such as the function and biogenesis of chloro-

plasts, ﬂagella and eyespots, and regulation of photosynthe-

sis (Merchant et al., 2007; Kreimer, 2009; Peers et al., 2009).

Genome data are rapidly accumulating and to date seven com-

plete green algal genomes have been sequenced: the prasino-

phytes Ostreococcus tauri (Derelle et al., 2006), O. lucimarinus

(Palenik et al., 2007) and two isolates of Micromonas pusilla

(Worden et al., 2009), the chlorophytes C. reinhardtii (Merchant

et al., 2007) and Volvox carteri (Prochnik et al., 2010), and the

trebouxiophyte Chlorella variabilis (Blanc et al., 2010). Several

other genome projects are ongoing, including the complete se-

quencing of Coccomyxa, Dunaliella, Bathycoccus, Botryococ-

cus and additional Ostreococcus and Micromonas strains (Tiri-

chine and Bowler, 2011). These data provide a great resource for

in-depth analysis of genome organization and the processes of

eukaryotic genome evolution. In addition, green algal genomes

are important sources of information for the evolutionary ori-

gins of plant traits because of their evolutionary relationship to

land plants.

Downloaded by [University of Gent] at 07:28 14 February 2012

4 F. LELIAERT ET AL.

FIG. 1. Taxonomical, morphological and ecological diversity among green algae. A: Pterosperma (Pyramimonadales), a marine prasinophyte characterized by

quadriﬂagellate unicells (photo by Bob Andersen, reproduced under license from microscope.mbl.edu). B: Nephroselmis (Nephroselmidophyceae), a prasinophyte

with bean-shaped cells and two unequal ﬂagella occuring in marine or freshwater environments. C: Palmophyllum (Palmophyllales) forming lobed crusts composed

of coccoid cells embedded in a gelatinous matrix, growing in deep-water marine habitats (photo by Jordi Regas). D: Tetraselmis (Chlorodendrophyceae),

quadriﬂagellate unicells from marine or freshwater habitats. E: Chlorella (Trebouxiophyceae, Chlorellales), coccoid cells, endosymbiontic inside the single-celled

protozoan Paramecium (photo by Antonio Guill

en). F: Oocystis (Trebouxiophyceae, Oocystaceae), small colonies of coccoid cells within a thin mucilaginous

envelope from freshwater habitats (image copyright Microbial Culture Collection, NIES). G: Haematococcus (Chlorophyceae, Chlamydomonadales), a freshwater

biﬂagellate unicell (photo by William Bourland, reproduced under license from microscope.mbl.edu). H: Pediastrum (Chlorophyceae, Sphaeropleales), a coenobial

colony of non-motile cells arranged in a circular plate, occuring in freshwater habitats. I: Bulbochaete (Chlorophyceae, Oedogoniales), branched ﬁlaments with

terminal hair-cells. J: Chaetophora (Chlorophyceae, Chaetophorales), highly branched ﬁlaments, occuring in freshwater habitats (H–J: photos by Jason Oyadomari).

K: Ulothrix (Ulvophyceae, Ulotrichales), unbranched ﬁlaments from marine or brackish areas (photo by Giuseppe Vago). L: Ulva (Ulvophyceae, Ulvales), sheet-

like plants, mainly from marine habitats (photo by Tom Schils). M: Cladophora (Ulvophyceae, Cladophorales), branched ﬁlament with cells containing numerous

chloroplasts and nuclei (photo by Antonio Guill

en). N: Boergesenia (Ulvophyceae, Cladophorales), plants composed of giant, multinucleate cells, from tropical

marine habitats (photo by HV). O: Acetabularia (Ulvophyceae, Dasycladales), siphonous plants (i.e. single-celled) differentiated into a stalk and a ﬂattened

cap, with a single giant nucleus situated at the base of the stalk; typically found in subtropical marine habitats (photo by Antoni L

opez-Arenas). P: Caulerpa

(Ulvophyceae, Bryopsidophyceae), siphonous plant differentiated into creeping stolons anchored by rhizoids and erect photosynthetic fronds, containing millions

of nuclei; occuring in (sub)tropical marine waters (photo by FL). Q: Klebsormidium (Klebsormidiophyceae), unbranched ﬁlamentous charophyte, mainly from

moist terrestrial habits (photo by Jason Oyadomari). R: Spirotaenia, a unicellular charophyte with typical spiral chloroplast; generally growing in acidic freshwater

habitats (photo by Antonio Guill

en). S: Nitella (Charophyceae), morphologically complex charophyte from freshwater habitats, consisting of a central stalk

and whorls of branches radiating from nodes that bear oogonia and antheridia (photo by Nadia Abdelahad). T: Micrasterias (Zygnematophyceae, Desmidiales),

characterized by non-motile unicells constricted in two parts with ornamented cell wall; generally found in acidic, oligotrophic freshwater habitats (photo by

Antonio Guill

en). U: Coleochaete (Coleochaetophyceae), branched ﬁlaments adherent to form a disc-like, parenchymatous thallus; found in freshwater habitats,

often as epiphytes on submerged vascular plants (photo by CFD). (Color ﬁgure available online.)

Downloaded by [University of Gent] at 07:28 14 February 2012

MOLECULAR EVOLUTION OF GREEN ALGAE 5

Reconstruction of the phylogenetic relationships among

green plants is essential to identifying the innovations under-

lying the diversity of green algae and land plants. Molecular

phylogenetics has dramatically reshaped our views of green al-

gal relationships and evolution. This review summarizes the cur-

rent understanding of green algal phylogeny, focusing primarily

on relationships among the major lineages of green algae, which

are usually classiﬁed as divisions, classes and orders. Current

phylogenetic hypotheses have provided an evolutionary frame-

work for molecular evolutionary studies and comparative ge-

nomics. In this review, we highlight a number of topics, includ-

ing the evolution of organellar genomes, ecology and molecular

evolution of marine picoplanktonic prasinophytes, genomic in-

sights into the evolution of complexity in volvocine green algae,

molecular evolution in the green seaweeds, and molecular evo-

lution in the streptophyte green algae and the origin of land

plants.

II. GREEN LINEAGE RELATIONSHIPS

A. Morphology, Ultrastructure and Molecules

Early hypotheses of green algal phylogeny were based on the

concept that evolution follows trends in levels of morphological

complexity (Fritsch, 1935; Fott, 1971). Unicellular ﬂagellates

were believed to have initially evolved into non-motile unicells

(coccoid) and loose packets of cells (sarcinoid), followed by

various multicellular forms and siphonous algae. This hierarchy

reﬂected the view that the morphologies that are organized in

two- and three-dimensional space require more elaborate devel-

opmental controls, and hence would be expected to appear later

in an evolutionary sequence. In this view the land plants were de-

rived from more complex, ﬁlamentous green algae (Blackman,

1900; Pascher, 1914).

A large amount of new information was gathered in the 1970s

and 1980s, mainly from investigations of the ﬁne structures of

green algal cells and life cycles (Round, 1984). These data led

to a thorough reevaluation of evolutionary relationships and a

revised classiﬁcation of green algae, primarily based on ﬂag-

ellar ultrastructure and processes of mitosis and cell division

(Picket-Heaps and Marchant, 1972; Melkonian, 1982; Mattox

and Stewart, 1984; Melkonian, 1984; O’Kelly and Floyd, 1984a;

O’Kelly and Floyd, 1984b; van den Hoek et al., 1988). These

features, which apply to most (but not all) green algae, were be-

lieved to accurately reﬂect phylogenetic relationships because

of their involvement in fundamental processes of cell replication

and cell motility, and thus to be less liable to convergent evolu-

tion than gross morphological traits. Ultrastructure-based phylo-

genetic hypotheses posited an early diversiﬁcation of ﬂagellate

unicells, resulting in a multitude of ancient lineages of ﬂag-

ellates, some of which then evolved into more complex green

algae. Although ultrastructural data have laid the foundations

for a natural classiﬁcation of the green algae, analyses of these

data have not resolved the phylogenetic relationships among the

main green algal lineages.

The introduction of molecular phylogenetic methods pro-

vided a new framework for reconstructing the evolutionary his-

tory of the green lineage. Analyses of DNA sequence data took

a start in the mid 1980s with the ﬁrst phylogenies of green plants

inferred from 5.8S nrDNA sequences (Hori et al., 1985; Hori

and Osawa, 1987), soon followed by 18S and 28S nrDNA se-

quence analyses (Gunderson et al., 1987; Perasso et al., 1989;

Buchheim et al., 1990; Zechman et al., 1990; Chapman et al.,

1991; Mishler et al., 1992; Chapman et al., 1998). Riboso-

mal sequences were chosen at the time because enough RNA

could be obtained for direct sequencing and (later) because re-

gions of the gene were conserved enough to make universal

primers. Ribosomal RNA is also found in all known living cells,

and although it is typically present in multiple copies in the

genome, concerted evolution homogenizes sequence diversity,

and consequently is assumed to reduce the risk of sequencing

paralogs. Early molecular studies were pre-PCR and hence in-

volved laboratory cloning and generally few taxa. Since 1990

rapid advancements in techniques in molecular biology (e.g.,

the utilization of PCR) and bioinformatics made it possible

to generate and analyze larger datasets. Nuclear-encoded 18S

rDNA sequences have been, until recently, the primary source

of data for inferring phylogenetic relationships among green al-

gae (Pr

oschold and Leliaert, 2007), supplemented by 28S rDNA

(e.g., Buchheim et al., 2001; Shoup and Lewis, 2003), actin (An

et al., 1999) and the chloroplast genes rbcL, tuf A and atpB

(e.g., Daugbjerg et al., 1994; Daugbjerg et al., 1995; McCourt

et al., 2000; Hayden and Waaland, 2002; Nozaki et al.

, 2003;

Zechman, 2003; Rindi et al., 2007).

These initial molecular phylogenetic investigations have gen-

erally corroborated the ultrastructure-based higher-level classi-

ﬁcation of the green algae, but have also revised the circumscrip-

tions of several lineages (McCourt, 1995). However, analyses

of individual genes have only partly resolved the relationships

among the main green algal lineages. It is now clear that a large

number of genes from many species must be analysed to arrive

at a reliable phylogenetic resolution for an ancient group such

as the green algae (Philippe and Telford, 2006). These datasets

have mainly involved concatenated sequences of protein-coding

genes that are shared among green algal chloroplast genomes.

To date, 26 complete green algal plastid genomes have been

sequenced and assembled (Wakasugi et al., 1997; Turmel et

al., 1999b; Lemieux et al., 2000; Maul et al., 2002; Turmel et

al., 2002b; Pombert et al., 2005; Turmel et al., 2005; B

elanger

et al., 2006; de Cambiaire et al., 2006; Pombert et al., 2006;

Turmel et al., 2006; de Cambiaire et al., 2007; Lemieux et al.,

2007; Robbens et al., 2007a; Brouard et al., 2008; Turmel et

al., 2008; Turmel et al., 2009a; Turmel et al., 2009b; Zuccarello

et al., 2009; Brouard et al., 2010; Brouard et al., 2011), in

addition to more than 30 angiosperm plastid genomes (Soltis

et al., 2009). Chloroplast genomes are particularly useful for

phylogenetic reconstruction because of their relatively high and

condensed gene content, in comparison to nuclear genomes. Fur-

thermore, in contrast to many nuclear genes that are multi-copy

Downloaded by [University of Gent] at 07:28 14 February 2012

Phylogeny and Molecular Evolution of the Green Algae

Figures

Citations

多様性--The Diversity

Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation

From algae to angiosperms–inferring the phylogeny of green plants ( Viridiplantae ) from 360 plastid genomes

The cell walls of green algae: a journey through evolution and diversity

Microalgae for High-Value Products Towards Human Health and Nutrition.

References

Sequencing technologies-the next generation

Evolution by gene duplication

Next-generation DNA sequencing.

Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit.

The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions

Related Papers (5)

Phylotranscriptomic analysis of the origin and early diversification of land plants

MUSCLE: multiple sequence alignment with high accuracy and high throughput

RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.

The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions

MrBayes 3: Bayesian phylogenetic inference under mixed models

Frequently Asked Questions (16)

Q1. What contributions have the authors mentioned in the paper "Phylogeny and molecular evolution of the green algae" ?

Q2. Why were ribosomal sequences chosen at the time?

Q3. Why are the stoneworts well represented in the fossil record?

Q4. What is the main problem in multi-gene phylogenetic investigations?

Q5. What made it possible to generate and analyze larger datasets?

Q6. What is the appeal of the organisms as a model system?

Q7. What are the biochemical innovations that have been identified?

Q8. What is the prominent endosymbiosis in eukaryo?

Q9. Why is the marine planktonic compartment of picoeukaryotes overlooked?

Q10. What is the significance of the phylogenomic analysis of two diatom genomes?

Q11. What are the recent advances in high-throughput DNA sequencing?

Q12. What are the traits that are unique to the remaining streptophytes?

Q13. What is the role of cytoplasmic streaming in siphonous algae?

Q14. What is the reason for the similar architectures of green algal genomes?

Q15. What is the function of EF-1 in eukaryotes?

Q16. what is the phylogenetic position of the klebsormidiophy?