Phylogeny and Molecular Evolution of the Green Algae - Phycology ...

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30 F. LELIAERT ET AL.is a crucial protein in the translation process. Despite this crucialfunction, not all eukaryotes have this protein, and it hasbeen shown that an elongation factor-like protein (EF-like) cansubstitute for EF-1α in these taxa (Keeling and Inagaki, 2004).Interestingly, most eukaryote genomes contain either EF-1α orEF-like, although a few have both (Kamikawa et al., 2008). Ingreen algae, these elongation factors show a mutually exclusivebut scattered distribution (Noble et al., 2007; Cocquyt etal., 2009; Gile et al., 2009). Whereas the streptophytes haveEF-1α, with the exception of Mesostigma, the chlorophytes encodeEF-like with the exception of certain ulvophytes. Like theprasinophytes and most core chlorophytes, the early-branchingulvophytes have the EF-like gene whereas the clade comprisingIgnatius, the Trentepohliales, Dasycladales, Bryopsidales andCladophorales have EF-1α (Figure 6). Regrettably, phylogenyexplicitmodels of gene gain and loss were unable to determinethe presence of either one or both of the genes in the genome ofthe ancestor of the green lineage and the Ulvophyceae (Cocquytet al., 2009). Nevertheless, the alternative elongation factorsused in different lineages of the green seaweeds can be taken tomark a second considerable alteration of the translation pathwaythat occurred during the evolution of the Ulvophyceae.In addition to the changes in genetic code and elongationfactors mentioned above, two other sources of evidence pointto changes in the translational apparatus of the Ulvophyceae(Cocquyt, 2009). First, patterns of codon usage of eight nuclearhousekeeping genes differ considerably between the prasinophytesand Ulvophyceae. Second, the rates of molecular evolutionof the 18S ribosomal RNA molecule are considerably elevatedin the ulvophycean orders Cladophorales, Dasycladalesand Bryopsidales. All this evidence taken together points toprofound changes in the translational apparatus of the Ulvophyceae,but this hypothesis awaits confirmation from moredetailed studies of the translational pathway.E. Molecular Evolution in the Streptophyta and theOrigin of Land PlantsThe origin of embryophytic land plants from a green algal ancestorwas a major event in the history of life, which influencedthe establishment of the entire terrestrial ecosystem and had farreachingeffects on atmospheric chemistry and climate (Berner,1997; Kenrick and Crane, 1997; Steemans et al., 2009). As notedabove (Section II.B.4), although the Streptophyta are not particularlydiverse (outside of the land plants) in terms of numberof described species, they represent the full range of structuraldiversity, from scaly unicellular flagellates through unbranchedand branched filaments, to the complex three-dimensionally organizedtissues of plants. There is little doubt, however, of thephylogenetic placement of embryophytes among the other streptophytes.The structurally simple streptophytes retain a numberof ancestral features that can shed light on the factors that led tothe success of embryophytes in the terrestrial environment.The colonization of dry land involved adaptation to new andharsh environmental conditions such as desiccation, temperaturefluctuations, the need for support in the absence of a buoyantmedium, and UV radiation (Raven, 2000; Waters, 2003;Floyd and Bowman, 2007; Lang et al., 2008). Ecophysiologicaladaptations of the first land plants included enhanced osmoregulationand osmoprotection, desiccation and freezing tolerance,and heat resistance (Rensing et al., 2008). Several biochemicalinnovations have been identified, including synthesis and accumulationof protective “sunscreens,” plant growth hormones,isoprene, phenolics, heat shock proteins, and enhanced DNArepair mechanisms (Waters, 2003; Rensing et al., 2008). In addition,several morphological innovations are believed to haveallowed successful adaption to life on land and radiation intonew niches (Graham et al., 2000). Some of these are found inone or more algal relatives of embryophytes, including productionof extracellular matrices such as sporopollenin and perhapslignin, the development of differentiated cells and tissues, dorsiventraldevelopment (which is important in the developmentof structures such as leaves), the establishment of intercellularcommunication networks (plasmodesmata, plant hormones, receptorsand their ligands), and the perception of environmentalcues (light and gravity), while others, such as life cycle involvingalternation of two distinct multicellular generations (a haploidsporophyte and diploid gametophyte), protected embryos,and gas-filled spaces within the plant body appear to be uniqueto embryophytes (Delwiche et al., 1989; Graham et al., 2000;Bowman et al., 2007; Ligrone et al., 2008). The success of landplants has further been linked to symbiotic associations withmycorrhizal fungi (Simon et al., 1993; Heckman et al., 2001;McCourt et al., 2004).Important evolutionary transitions and adaptive radiations,such as the origin and diversification of land plants, have been associatedwith gene family expansions resulting from large-scalegene duplication or whole-genome duplication events (Ohno,1970; De Bodt et al., 2005; Flagel and Wendel, 2009). The variousphysiological and morphological adaptations to land werelikely associated with expansion of gene families involved in signallingpathways, such as those for auxin, ABA and cytokinin(Lang et al., 2008; Rensing et al., 2008; Timme and Delwiche,2010; De Smet et al., 2011). Morphological innovations and theevolution of morphological complexity in land plants have beenlinked with increased gene family complexity of several genesincluding actin (An et al., 1999), MADS box genes (Henschelet al., 2002; Tanabe et al., 2005), homeobox genes (Mukherjeeet al., 2009) and OPR genes (Li et al., 2009). Expansion ofthe glutaredoxins gene family (enzymes implicated in oxidativestress response) in land plants likely resulted in genes withnovel functions in development and pathogenesis response (Ziemannet al., 2009). The unique sexual life cycle of land plantslikely evolved through expansion of homeodomain gene networks(e.g. MADS-box genes) (Tanabe et al., 2005; Niklas andKutschera, 2010). Ca 2+ -dependent signalling processes, whichare important in the response to many developmental and environmentalstimuli, have been found to be very different in greenalgae and land plants, with several Ca 2+ signalling mechanisms
MOLECULAR EVOLUTION OF GREEN ALGAE 31having apparently been lost in land plants after their divergencefrom charophyte algae (Wheeler and Brownlee, 2008).Although there is still uncertainty concerning the precise relationshipsbetween land plants and their green algal relatives(see Section II.B.4) it is clear that several fundamental landplant features were inherited from their charophyte green algalprogenitors, including cellulosic cell walls, multicellularity,cytokinetic phragmoplast, plasmodesmata, apical meristematiccells (although the meristematic regions in the Charophyceae,Coleochaetophyceae and Zygnematophyceae are very differentfrom that in the embryophytes), asymmetrical cell division,cell specialization, branching, three-dimensional organization,zygote retention, and placenta (Graham et al., 2000). It hasbeen hypothesized that charophyte green algae were physiologicallypre-adapted to life on land by their primarily freshwaterlife style, which exposed them to periodic exposure and desiccation,and allowed a gradual shift towards moist terrestrialhabitats, and ultimately the colonization of dry land (Beckerand Marin, 2009). It is striking that several streptophyte lineagesother than embryophytes are found in terrestrial habitats(i.e., Chlorokybus atmosphyticus, many species of Klebsormidium,and several Zygnematales), which emphasizes the closerelationship between freshwater and moist terrestrial habitats.A growing body of evidence indicates that the molecularbases of many morphological, life-history, cytological, biochemicaland physiological features of embryophytes lie inan era prior to the colonization of land (Becker and Marin,2009). This has been shown by several studies elucidating theevolution of land plant genes in the green lineage, includingactin (An et al., 1999), cellulose synthase (Roberts and Roberts,2004; Yin et al., 2009), class III homeodomain–leucine zippergenes (Floyd et al., 2006), MADS-box genes (Tanabe et al.,2005), vacuolar sorting receptors (Becker and Hoef-Emden,2009), arabinogalactan-like proteins and hemicelluloses (e.g.endotransglucosylase, responsible for cell wall loosening andcell expansion) (Van Sandt et al., 2007; Eder et al., 2008; Fryet al., 2008).Expressed sequence tag (EST) sequencing of various charophytesand land plants has been used in comparative plant genomicsstudies to uncover the origins of land plant genes andtheir associated molecular pathways (Nedelcu et al., 2006; Simonet al., 2006; Timme and Delwiche, 2010). Overall, thesestudies indicate that several land plant characteristics evolvedbefore the transition to land. For example, EST analysis ofMesostigma (Mesostigmatophyceae) suggests that importantphysiological changes involving regulation of photosynthesisand photorespiration took place early in the evolution of theStreptophyta (Simon et al., 2006). Similarly, putative homologsof genes involved in the development of three-dimensional tissuesthrough asymmetrically dividing apical meristematic cells(BIB gene family) have been identified in Mesostigma (Nedelcuet al., 2006). Several other genes that have been hypothesized tobe important in the colonization of land plants (Graham et al.,2000) may have true orthologs in Coleochaete (Coleochaetophyceae)and Spirogyra (Zygnematophyceae) but are apparentlyabsent in the ESTs of the earlier diverging Mesostigma(Timme and Delwiche, 2010). These include genes involvedin cellulose synthesis (RSW1), phragmoplast mediated cytokinetic(GEM1/MOR1), formation of plasmodesmata (CRT1)and development of a multicellular sporophyte (MERISTEMLAYER1). Two genes associated with asymmetric cell division(WUSCHEL and GNOM) were only found in Coleochaete,while the plant cell wall loosening expansin genes (EXP) wereonly present in Spirogyra. In addition, several ethylene pathwaygenes, long thought to be unique to land plants, have beenidentified in Coleochaete and Spirogyra.Cell walls are believed to have played crucial roles in thecolonization of land by plants (Sorensen et al., 2010). Althoughsome cell wall components do appear to be land plant innovations,cell wall evolution after the colonization of land appearsto be characterized mostly by the elaboration of a pre-existingset of cell wall polysaccharides and the enzymes that synthesizethem (e.g., cellulose synthase and wall-remodelling enzymes),rather than substantial innovation (Roberts and Roberts, 2004;Domozych et al., 2007; Van Sandt et al., 2007; Eder et al., 2008;Fry et al., 2008; Domozych et al., 2009; Yin et al., 2009; Popperand Tuohy, 2010; Popper et al., 2011).There are several other examples where the genetic potentialfor plant specific features has been suggested in green algae.For example, genes involved in auxin signalling (central to landplant growth and development) have been detected in variousmembers of Chlorophyta and Streptophyta, indicating that auxinresponse and transport mechanisms were likely present beforethe evolution of land plants (De Smet et al., 2011). Similarly,the B3 DNA Binding superfamily, including genes mainly involvedin hormone signaling pathways such as those for auxin,abscisic acid, brassinosteroid and gibberellins, are also presentin Chlorophyta but have undergone extensive duplication eventsduring land plant evolution (Romanel et al., 2009).V. CONCLUSIONS AND PERSPECTIVES20 years ago, a review article in this journal reported on thestate of knowledge on green algal relationships, gathered fromthe few pioneering years of ribosomal DNA-based phylogeneticresearch (Chapman et al., 1991). The past two decades have witnessedprofound changes in our understanding of the evolutionof green algae. 18S phylogenies have made way for multi-geneand genome scale analyses. These studies have greatly improvedour understanding of the deepest relationships of the green lineage(Figure 3); however, many questions remain.A large body of molecular evidence has confirmed theultrastructural-based hypothesis that the green lineage divergedinto two discrete clades: the Chlorophyta, which includes themajority of described species of green algae, and the Streptophyta,which is comprised of the charophytes, a paraphyleticassemblage of freshwater algae from which the land plantshave evolved. The prasinophytes take up a critical position,
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