eXtra Botany
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Algal models in plant biology
J. Mark Cock1,2,* and Susana M. Coelho1,2
1
UPMC Univ. Paris 06, The Marine Plants and Biomolecules
Laboratory, UMR 7139, Station Biologique de Roscoff, Place
Georges Teissier, F-29682 Roscoff, France
2
CNRS, UMR 7139, Laboratoire International Associé Dispersal
and Adaptation in Marine Species, Station Biologique de Roscoff,
Place Georges Teissier, F-29682 Roscoff, France
* To whom correspondence should be addressed. E-mail: cock@
sb-roscoff.fr
Journal of Experimental Botany, Vol. 62, No. 8, pp. 2425–2430,
2011
doi:10.1093/jxb/err117
During the last three decades, plant science has focused on
model organism-based approaches, particularly on exploiting the powerful system represented by Arabidopsis
thaliana, for which there are a wide range of genetic and
genomic resources available. Increasingly, however, there
is a tendency to broaden analyses to include multiple study
organisms in an attempt to understand biological processes
from an evolutionary perspective. An additional advantage
of this multi-organism approach is that it has the potential
to capture functional variations on a central theme as
particular biological processes are likely to have been
adapted to the needs of each organism. The exact nature
of the organisms selected for such studies depends on the
objectives of the study. For recently evolved systems, such
as the regulatory processes controlling flowering, for
example, the group of organisms will usually need to be
quite closely related. By contrast, for ancient, more basic
cellular processes such as photosynthesis or primary cell
metabolism, for example, it may be of interest to compare
much more widely diverged organisms. The objective of
this article is to underline the potential of the diverse
spectrum of eukaryote species that are grouped under the
definition ‘algae’ as study organisms for the latter type of
approach.
The term ‘algae’ refers to all photosynthetic eukaryotes
apart from land plants. Algae is a polyphyletic grouping
and includes taxons in five of the eight major eukaryotic
groups (Fig. 1). This very broad phylogenetic distribution
of photosynthetic organisms in the eukaryotic tree is due to
a combination of two factors: (i) the very ancient nature of
the initial primary endosymbiotic event that occurred in the
green lineage (in which a cyanobacterium was captured and
enslaved to become a plastid) and (ii) the subsequent
occurrence of multiple secondary and tertiary endosymbiotic events in which a photosynthetic alga was, in turn,
captured by a phylogenetically unrelated heterotrophic
eukaryote and itself enslaved to become a plastid within the
predator cell (Armbrust, 2009; Keeling, 2010). These
secondary and tertiary endosymbiotic events are particularly interesting because they have led to plastids being
resident in a very diverse range of cellular contexts and
because the reiterative ‘Russian doll’ capture process
resulted in novel combinations of genomes due to gene
transfer processes that occurred during the enslavement.
Most of the key endosymbiotic events are very ancient,
having occurred before the colonization of the land by
photosynthetic organisms (Keeling, 2010) and many of the
taxonomic groups that include algal species have no
terrestrial members. The marine environment is, therefore,
a potentially rich source of novel model photosynthetic
organisms.
Photosynthesis: variations on a theme in
algae
Recent work on microalgae illustrates how these organisms
are contributing to our understanding of the evolution and
diversification of one key cellular process, photosynthesis.
Prasinophyte algae, which are major constituents of many
marine phytoplankton ecosystems, exhibit many primitive
features and are therefore considered to be a basal group
for the green lineage (Melkonian, 2001). The identification
of a photosynthesis antenna protein that appeared to be
associated with both photosystem I (PSI) and PSII initially
suggested that this may have been the ancestral situation
but genomic analyses showed that these organisms also
possess proteins that are incorporated specifically into either
PSI or PSII (Six et al., 2005). Interestingly, the PSI
antennae system of red algae represents an evolutionary
intermediate between the antenna system of prokaryotic
cyanobacteria and those of other eukaryotes in the green
lineage (Busch et al., 2010). Other intriguing photosynthesis-related phenomena that have been observed in marine
phytoplankton algae include evidence for C4 photosynthesis
(Reinfelder et al., 2000; Roberts et al., 2007; McGinn and
Morel, 2008) and alternative carbon-concentrating mechanisms based, for example, on carbonic anhydrase, which is
widespread in marine algae (Kroth et al., 2008).
Along with the obvious benefits of photosynthesis as
a source of energy for cellular processes, photosynthetic
cells have to cope with the risks associated with the
absorption of excess light, which can cause oxidative
ª The Author [2011]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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Fig. 1. Simplified schema representing the eukaryotic tree (adapted from Baldauf, 2008, with permission from the Editorial Office of the
Journal of Systematics and Evolution). Groups that include photosynthetic organisms are indicated by green lettering. A single primary
endosymbiotic event was at the origin of the plastids of all the members of the archaeplastida. Photosynthetic species within the
stramenopiles, alveolates, haptophytes, cryptophytes, chlorarachnia, and euglenids obtained their plastids through multiple secondary or
tertiary endosymbiotic events.
damage to the cell. Work carried out on algae in this
domain have identified a remarkable diversity of responses
to this problem. Despite being a member of the green
lineage, the photosynthetic system of the chlorophyte alga
Chlamydomonas differs in several respects from that of land
plants (Finazzi et al., 2010). Recent genetic analysis has
demonstrated the implication of a light-induced lightharvesting protein, LHCSR (previously called LI818), in the
non-photochemical quenching (NPQ) of chlorophyll fluorescence, a mechanism that involves de-excitation of chlorophyll molecules in photosystem II (qE) (Peers et al., 2009).
LHCSR proteins are absent from vascular plants, where
the PsbS protein plays a major role in qE. Chlamydomonas
possesses PsbS genes but the corresponding proteins have
not been detected. Moreover, more distantly related algae,
such as the diatoms in the chromalveolate group, appear
to lack PsbS genes altogether, despite the presence of an
unusual xanthophyll-based energy-dissipation system (Lohr
and Wilhelm, 1999), which confers a high capacity for
NPQ. LHCSR genes have, however, been found in both
diatoms and in prymnesiophytes (Peers et al., 2009),
although these proteins appear to function slightly differently, at least in diatoms. The Phaeodactylum tricornutum
LHCSR, LHCX1, is present under non-stress conditions
and modulates NPQ capacity both under stress conditions
and during normal light/dark cycles (Bailleul et al., 2010).
State transitions, which may provide additional photoprotection in terrestrial plants, have not been observed in
diatoms (Owens, 1986). Interestingly, in at least one strain
of the prasinophyte alga Ostreococcus a considerable proportion of photosynthetic electron flow is diverted through
the chlororespiratory enzyme plastoquinol terminal oxidase
(PTOX) (Cardol et al., 2008). It has been suggested that
this innovation may allow ATP production under iron
starvation conditions, although this idea has recently been
contested (Rusch et al., 2010).
The red algae also exhibit some unusual features
related to photosynthesis. Work on the unicellular species
Cyanidioschyzon merolae indicates that, in contrast to green
algae and land plants, gene expression in red algal
chloroplasts is controlled mainly at the transcriptional level
(Apt and Grossman, 1993; Minoda et al., 2005) and that the
Rubisco operon is regulated in a nucleus-independent
manner in these organelles (Minoda et al., 2010). This latter
feature is probably ancient, reflecting the situation at the
time that the primary endosymbiosis occurred.
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Evolutionary origins of other metabolic
pathways
Algae that are very distantly related to land plants, such as
members of the chromalveolate lineage (which includes
stramenopiles and alveolates; Fig. 1), can exhibit unusual
metabolic systems due to their having retained different sets
of metabolic genes during the long periods for which they
have been evolving independently of their green cousins.
One interesting example was the discovery of a urea cycle in
diatoms (Armbrust et al., 2004), a metabolic pathway that
is found in animals but has been lost from green plants and
algae. The diatom urea cycle is unlikely to be involved in
the production of urea as a waste molecule but is probably
integrated into metabolic pathways that produce molecules
such as spermine and spermidine and possibly additional
long-chain polyamines involved in the precipitation of the
silica that makes up the diatoms protective frustule.
The recent sequencing of the complete genome of the
filamentous brown alga Ectocarpus siliculosus has allowed
comparative approaches to be extended to this group of
algae and has provided several insights into processes
that have played a key role in eukaryotic evolution. For
example, inclusion of the Ectocarpus genome data in a broad
comparative analysis of genome data has allowed evolutionary scenarios to be proposed for two important
metabolic processes, carbon storage and cell wall biosynthesis (Michel et al., 2010a, b). In both cases, there appear to
have been major changes in the metabolic pathways present
in the cells of different groups of organisms across the
eukaryotic tree over evolutionary time. The recent discovery
of starch in cyanobacteria indicates that starch metabolism
was probably acquired by the green lineage as a result of the
primary endosymbiosis (Deschamps et al., 2008a). Several
lines of evidence, including data based on genome comparisons, indicate that starch metabolism was rapidly
transferred to the cytoplasm following the primary endosymbiotic event in the ancestor of the three major lines of
the archaeplastida: the glaucophytes, the rhodophytes (red
algae), and the chloroplastida (the green lineage). Starch
metabolism was then relocated to the plastid at a later
stage, but only in the chloroplastida lineage (Deschamps
et al., 2008b). However, starch metabolism is completely
absent from the stramenopile lineage, despite the secondary
endosymbiotic capture of a red alga. The presence of
different carbon storage pathways in stramenopiles and
alveolates suggests that they are derived from different
secondary endosymbiotic events (Michel et al., 2010a), and
not from the single endosymbiotic event proposed by the
chromalveolate hypothesis (Cavalier-Smith, 1999). Similar
results were obtained with the analysis of cell wall
metabolism. The cell walls of photosynthetic eukaryotes are
highly diverse, reflecting both their evolutionary history and
the constraints imposed by the environments in which they
live (Michel et al., 2010b). For example b-1,3-glucan
polymers were probably present in the common eukaryotic
ancestor, whereas cellulose would have been acquired from
a cyanobacterium during the primary endosymbiosis, and
the alginates of brown algae via horizontal transfer from an
actinobacterium. As an example of an environmental
constraint, sulphated polysaccharides tend to be found
predominantly in marine organisms.
The presence of a flavonoid pathway in both green plants
and in Ectocarpus indicates that this metabolic system
evolved in their common ancestor and is, therefore, very
ancient. This is not consistent with the proposition that
much of the complexity of phenylpropanoid metabolism
evolved in land plants after the horizontal transfer of
a phenylalanine ammonia lyase gene from a bacterial
genome (Emiliani et al., 2009), suggesting rather that this
enzyme was integrated into a pre-existing pathway (Cock
et al., 2010).
Ectocarpus and the evolution of complex
multicellularity
The brown algae include organisms that can be considered
to have evolved complex, multicellular bodyplans. This is
a rare feature amongst the eukaryotes, with only a small
number of eukaryote groups exhibiting complex multicellularity (Cock et al., 2010). The Ectocarpus genome was
therefore of particular interest as a means to investigate the
molecular basis of this phenomenon. Moreover, as complex
multicellularity evolved independently in the brown algae,
compared with other groups such as the green plants and
animals, comparative analyses could potentially distinguish
fundamental features associated with the transition to
complex multicellularity from features that were contingent
on the evolutionary history of each group. Three types of
feature were identified that could have been associated with
the evolution of complex multicellularity in the brown algae
(Cock et al., 2010). The first was the retention of key genes
during evolution. Three integrin-like genes and several
classes of ion channel were found in the Ectocarpus genome
but not in the genomes of other stramenopiles, such as the
unicellular diatoms and the oomycetes, which exhibit
a primative form of multicellularity. Both of these classes
of gene could play important roles in functions linked to
multicellularity, the integrin-like genes because of a potential
role in cell–cell communication and the ion channels as
components of signalling networks, which are thought to be
more complex in multicellular organisms. The second type
of feature that was identified was a tendency for complexity
to be conserved with respect to several key gene families,
including transcription factors, small GTPases, and the
Rad51 gene family, which is involved in DNA repair and
meiosis. This latter observation is consistent with a previous
report that the Rad51 family tends to be more complete in
multicellular organisms (Lin et al., 2006). Finally, evolution
of novel gene families may also have played an important
role in the transition to multicellularity. One of the gene
families that is predicted to have evolved since the divergence from the diatoms encodes membrane-spanning
receptor kinases. These are particularly interesting because
the independent emergence of analogous families in the
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animal and green plant lineages has been associated with
the transitions to complex multicellularity in these two
lineages (Shui and Bleecker, 2001; Cock et al., 2002).
Deep sequencing of small RNA sequences allowed the
identification of 26 microRNA genes in the Ectocarpus
genome. A large proportion of the putative target genes of
these microRNAs encode proteins with leucine-rich repeats,
many of which were predicted to have evolved since the
divergence of the brown algal and diatom lineages. This is
interesting because it has been suggested that the expansion
of small-RNA-based gene regulatory processes may have
played an important role in the evolution of complex
multicellularity in animals (Peterson et al., 2009).
New algal model organisms
The examples given above illustrate the potential of algae as
tools to investigate the biology of photosynthetic organisms. The emergence of new algal model organisms in recent
years, particularly among marine algae, is an important
development that should greatly facilitate the exploitation
of algal diversity for plant research. Within the green algae,
complete genome sequences of two strains of the picoeukaryote Ostreococcus (Derelle et al., 2006; Palenik et al., 2007)
have revealed very compact genomes with a very low level
of functional redundancy, the majority of protein functions
being encoded by a single gene. This feature, together with
the availability of an efficient transformation protocol,
makes this organism an attractive candidate for the analysis
of cellular processes such as the control of circadian
rhythms (Moulager et al., 2010). A complete genome
sequence is available for the red alga C. merolae (Matsuzaki
et al., 2004), and this organism has proved to be a powerful
system for studying several aspects of cell biology including
organelle division (Fujiwara et al., 2009; Yoshida et al.,
2010), organelle inheritance (Fujiwara et al., 2010) and the
mechanisms that co-ordinate organelle and nuclear DNA
replication (Kobayashi et al., 2009). Within the stramenopiles, the diatom Phaeodactylum tricornutum is emerging as
a useful cellular model, again with a complete genome
sequence available (Bowler et al., 2008), several molecular
tools (Siaut et al., 2007) and, more recently, the development of an RNA interference-base method for gene
knockdown (De Riso et al., 2009). The brown macroalga
Ectocarpus is also being developed as a model organism
(Peters et al., 2004; Coelho et al., 2007) providing a novel
system to study developmental processes such as the
regulatory mechanisms that control the life cycle (Peters
et al., 2008). As the collections of tools available for these
new model organisms are gradually enlarged in the coming
years, we can expect them to make many more contributions to our understanding of plant biology.
Acknowledgements
We would like to thank Frédéric Partensky for critically
reading the manuscript. Work on Ectocarpus in Roscoff
has been supported by the Centre National de Recherche
Scientifique, the French GIS ‘Institut de la Génomique
Marine’, the European Union network of excellence
Marine Genomics Europe, the GIS Europôle Mer, and
the University Pierre and Marie Curie.
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