Melkonian and Burkhard Becker. Origin of land plants: Do conjugating green algae hold the key? BMC Evolutionary Biology, (in press) [link]. Plants are thought to have evolved from a class of freshwater green algae called The bryophytes consist of the liverworts, hornworts, and mosses, and as their. Phylogeny and evo-devo approaches to the evolution of plant form are starting to .. Transition to a land flora: phylogenetic relationships of the green algae and.
Phylogeny of the green lineage 1. Chlorophyta and Streptophyta Current hypotheses on green algal evolution posit the early divergence of two discrete lineages: The Chlorophyta includes the majority of described species of green algae. The Streptophyta are comprised of the charophytes, a paraphyletic assemblage of freshwater algae, and the land plants. Overview phylogeny of the green lineage top and spread of green genes in other eukaryotes bottom — Updated Fig.
Marin provided evidence for an independent class Pedinophyceae, sister to all phycoplast-containing core chlorophytes Chlorodendrophyceae, Trebouxiophyceae, Ulvophyceae and Chlorophyceae. Re-analysis of the dataset of Finet et al. They display a number of ultrastructural and biochemical traits that are shared with land plants but not with the Chlorophyta: Members of the Chlorophyta are common inhabitants of marine, freshwater and terrestrial environments and exhibit a remarkable morphological diversity Fig.
When viewed from the anterior flagellar end of the cell, the flagellar basal bodies and rootlets can have a perfect cruciate pattern i. Traditionally, four classes are recognized within the Chlorophyta: Resolution of the earliest green algal divergences often remains elusive because of the antiquity of the green lineage and the rapidity of the early evolutionary radiations McCourt, Figures 2 and 3 illustrate our current understanding of green algal relationships. The topology presented is a somewhat conservative interpretation of available data with polytomies representing uncertainties or conflicts between different studies.
The evidence supporting these relationships is discussed below on a clade-by-clade basis. A consensus reconstruction of green algal relationships, based on molecular data. Details and support for various clades are discussed in the text. Poorly resolved or conflicting relationships are shown as polytomies. Non-monophyletic lineages are indicated by dotted lines.
Branch lengths roughly represent genetic distance deduced from different phylogenetic studies. Multigene analysis strongly support a monophyletic Sphaeropleales, and indicate a possible relationship between Chaetophorales and Oedogoniales Tippery et al.
Molecular data have provided clear evidence that the class forms a paraphyletic assemblage of early diverging lineages Kantz et al. Based on the early diverging nature of the Prasinophyceae, the ancestor of the green lineage is believed to be a flagellate unicell.
However, the nature of this ancestral green flagellate AGF remains tentative. Simple flagellates have been proposed to most closely resemble the AGF Moestrup, Alternatively, the food uptake apparatus of some complex mixotrophic prasinophytes e. Cymbomonas has been interpreted as a feature inherited from a phagotrophic ancestor of the green lineage that was subsequently lost in most green algae Moestrup et al.
The circumscription of the prasinophytes has changed considerably with the discovery of several new taxa and environmental sequencing Hasegawa et al. The prasinophytes, as presently conceived, include a heterogeneous assemblage of scaled e. In addition, several coccoid forms have been found, which are distributed among at least four clades Fawley et al.
Although sexual reproduction has rarely been documented in prasinophytes but see Suda et al. Sexual reproduction has also been implied in Micromonas and Ostreococcus based on the presence of meiosis-specific and sex-related genes in the four sequenced genomes see below Derelle et al. The paraphyletic nature of prasinophytes has important consequences for understanding early green algal evolution, and a well-resolved phylogeny has the potential to shed light on the nature of the common ancestor of the Chlorophyta and on the origin of the core chlorophytes Turmel et al.
Development and genetics in the evolution of land plant body plans
Multi-gene phylogenetic analyses are just beginning to shed light on these early divergences. To date five chloroplast genomes from prasinophyte representatives of four clades Mamiellophyceae, Nephroselmidophyceae, Pycnococcaceae and Pyramimonadales have been sequenced, in addition to Mesostigma, a former member of the prasinophytes that is now known to be an early-branching streptophyte Turmel et al. The Mamiellales includes marine and freshwater flagellates with one or two laterally inserted flagella, as well as coccoid forms, with or without body scales.
They include some of the smallest eukaryotes known e.
- Development and genetics in the evolution of land plant body plans
- Phylogeny and molecular evolution of the green algae
The clade is further characterized by prasinoxanthin, a pigment that is also found in some other clades, such as the Pycnococcaceae Zingone et al. Analyses of 18S sequence and chloroplast genome data clearly show that Monomastix is sister to the Mamiellales Turmel et al. The biflagellate Dolichomastigales are also morphologically distinct: Dolichomastix has atypical scales and Crustomastix has a specialized cell covering rather than the more typical body scales Nakayama et al.
Their phylogenetic placement in Mamiellophyceae has been demonstrated by 18S data Zingone et al. The relationships among the Mamiellales, Monomastigales and Dolichomastigales, however, have not been resolved.
Chloroplast phylogenomic analyses resolved a sister relationship between the Mamiellophyceae and the Pyramimonadales Turmel et al. As mentioned above, some Pyramimonadales e. Cymbomonas are unique among green algae in possessing a food uptake apparatus Moestrup et al.
The Pycnococcaceae is a small clade containing the marine biflagellate Pseudoscourfieldia and the naked coccoid Pycnococcus. Some 18S studies have related this clade with the Nephroselmidophyceae although never with strong support; Fawley et al. However, chloroplast multi-gene analyses do not support a relationship between the two clades and have identified the Nephroselmidophyceae as an early diverging prasinophyte lineage, while the phylogenetic position of the Pycnococcaceae remains equivocal Turmel et al.
However, the nature and phylogenetic affinities of these clades remain elusive. Palmophyllales feature a unique type of multicellularity, forming firm, well-defined macroscopic thalli composed of isolated spherical cells in a gelatinous matrix Pueschel et al.
Analysis of two plastid genes atpB and rbcL placed the Palmophyllales as the sister clade to all other Chlorophyta while 18S phylogenetic analysis allied the Palmophyllales with the Prasinococcales clade. This clade includes the coccoid prasinophytes Prasinococcus and Prasinoderma, and it has also been shown to form an early diverging prasinophyte clade based on 18S data Guillou et al.
Sequencing of environmental samples and cultures has identified a clade of coccoid prasinophytes CCMP clade that, together with the saline lake dwelling coccoid Picocystis, emerges as a sister lineage to the core chlorophytes, although strong support for this relationship is still lacking Guillou et al.
This group includes the early diverging Chlorodendrophyceae, and three major classes: The core chlorophytes are characterized by a new mode of cell division that is mediated by a phycoplast i. The Chlorodendrophyceae is a small clade uniting the marine or freshwater scaly quadriflagellates Tetraselmis and Scherffelia Guillou et al.
The close relationship with the UTC classes has been confirmed by 18S and multi-gene phylogenetic data Massjuk, ; Cocquyt et al. Radiation of the Ulvophyceae, Trebouxiophyceae and Chlorophyceae The UTC classes are species-rich and morphologically and ecologically diverse.
Ecophysiological adaptations have likely led to the success of the Chlorophyceae and Trebouxiophyceae in freshwater and terrestrial environments, while the Ulvophyceae mainly diversified in coastal ecosystems. Marine versus freshwater lifestyles also coincide with differentiations in life histories. Whereas the marine Ulvophyceae mainly have life cycles involving an alternation between a free-living haploid, gametophytic and a free-living diploid, sporophytic multicellular generation, most freshwater green algae have a haploid vegetative phase and a single-celled, often dormant zygote as the diploid stage.
In terrestrial members of the core chlorophytes, sexual reproduction has rarely been documented Rindi, Resolving the phylogenetic relationships among and within the UTC classes can provide important insights into the evolution of these ecophysiological, life history and morphological traits.
Molecular phylogenetic studies based on 18S sequences Zechman et al. All possible relationships have been hypothesized, depending on interpretation of ultrastructural characters, gene and taxon sampling, and phylogenetic methods used. The fossil record indicates the presence of the classes in the mid-Neoproterozoic and molecular clock estimates situate the UTC divergence in the early Neoproterozoic Butterfield et al.
Some early 18S phylogenies showed a sister relationship between Chlorophyceae and Trebouxiophyceae e. Chloroplast multi-gene phylogenetic analyses have generally supported a sister relationship between Ulvophyceae and Trebouxiophyceae Pombert et al. The latter topology is also supported by a mitochondrial multi-gene analysis Pombert et al.
Phylogeny and molecular evolution of the green algae | Frederik Leliaert
Ultrastructural data have been interpreted as either providing supports for a sister relationship between Chlorophyceae and Trebouxiophyceae or between Trebouxiophyceae and Ulvophyceae. A relationship between Trebouxiophyceae and Ulvophyceae was proposed based on a counter-clockwise orientation of the flagellar apparatus Sluiman, In contrast, molecular data generally support an early diverging Trebouxiophyceae.
This would imply the ancestral status of a CCW orientation of the flagellar basal bodies, which evolved to a DO and CW orientation in the Chlorophyceae.
This interpretation is congruent with a CCW flagellar root system in the Chlorodendrophyceae. Similarly, species of the coccoid genus Chlorococcum and the filamentous genus Uronema were present in the Chlorophyceae as well as the Ulvophyceae Watanabe et al. As presently conceived, the class encompasses motile and non-motile unicells, colonies and multicellular filaments or blades from freshwater or terrestrial habitats, with some species penetrating in brackish or marine waters.
A number of trebouxiophytes have lost photosynthetic capacity and have evolved heterotrophic free-living or highly adapted parasitic lifestyles e.
Several distinct lineages within the Trebouxiophyceae have been recovered by molecular data, including the Chlorellales, Trebouxiales, Microthamniales, Prasiola-clade and several clades that have not yet received a formal name Katana et al. Resolving the branching patterns among these lineages can provide important insights into morphological and ecological evolution, and provide clues about the origins and adaptations of symbiotic and parasitic lifestyles, ultimately leading to obligate heterotrophic lifestyles.
Knowledge of trebouxiophyte interrelationships, however, is limited. Single gene mostly 18S analyses were not able to resolve the relationships among the main lineages, and some analyses even cast doubt on the monophyly of the group Krienitz et al.
Molecular data have revealed extreme polyphyly of morphologically simple genera indicating convergent evolution toward reduced morphology. In addition, polyphyly has been demonstrated in genera with more complex colonial forms e. The Chlorellales mainly includes freshwater and terrestrial coccoid forms and a few marine members Aslam et al.
Although plastids are not apparent in Helicosporidium cells, molecular evidence indicates that it maintains a functional plastid genome Tartar et al. Diversity and phylogenetic relationships within the Chlorellales have been well studied Huss et al. The enigmatic Pedinomonas is likely related to the Chlorellales. This tiny naked uniflagellate has traditionally been placed in a separate order Pedinomonadales or class Pedinophyceae based on some unusual ultrastructural features Melkonian, a; Moestrup, However, chloroplast multi-gene analyses and gene linkage data place Pedinomonas firmly within the Chlorellales Turmel et al.
This placement is supported by the CCW orientation of the flagellar apparatus but the persistent telophase spindle in Pedinomonas is atypical for the Trebouxiophyceae. It should also be noted that phylogenetic analyses of seven mitochondrial genes have placed Pedinomonas sister to the Chlorophyceae on a long branch, but these analyses may suffer from low taxon sampling and systematic errors in phylogeny reconstruction Turmel et al.
Analysis of complete nuclear and plastid-encoded rRNA operon sequences resolved the Pedinophyceae as a sister clade to all phycoplast-containing core chlorophytes Chlorodendrophyceae, Trebouxiophyceae, Ulvophyceae and Chlorophyceaesupporting the recognition of a separate class Marin see updated Figs 2 and 3 ] The Prasiola-clade is the morphologically and ecologically most diverse trebouxiophyte lineage, including unicellular e.
The order also includes several free-living soil algae e. Several other distinct clades of trebouxiophytes, composed of taxa with diverse morphologies and ecologies, have been characterized but their phylogenetic affinities to the better-studied lineages remain uncertain. These clades include the Choricystis lineage, comprising Choricystis, Botryococcus and Coccomyxa Karsten et al.
Given the fact that Leptosira was the only trebouxiophycean representative outside the Chlorellales in these analyses, this relationship may be the result of systematic error in phylogenetic reconstruction Turmel et al. Chlorophyceae The Chlorophyceae are a large and morphologically diverse group, including non-motile and motile unicells, colonies, branched and unbranched filaments, and blade-like thalli.
Reproduction is equally diverse, including various asexual and sexual modes van den Hoek et al. Chlorophycean algae are especially abundant in freshwater but also occur in terrestrial habitats. The class is characterized by closed mitosis during cell division, phycoplast-mediated cytokinesis, and diverse configurations of the flagellar apparatus of motile cells.
Molecular phylogenetic analyses have drastically reshaped the classification of the class. Traditional orders and genera were found to be polyphyletic while others were moved to other classes e.
Molecular and ultrastructural data have identified five major clades Booton et al. The Chlamydomonadales is characterized by a CW flagellar apparatus orientation in biflagellate members, but quadriflagellate representatives may display various other orientations Nakayama et al. The Sphaeropleales include nonmotile unicells or colonies that produce biflagellate zoospores with a DO basal body configuration Deason et al. The Chaetophorales and Chaetopeltidales are both characterized by quadriflagellate motile cells.
The Oedogoniales are characterized by zoospores with an anterior ring of numerous flagella stephanokont Pickett-Heaps, The atypical flagellar apparatus in the Chaetopeltidales, Oedogoniales and Sphaeropleales has hampered homology assessment with flagellar characters occurring in the other two clades Turmel et al. The phylogenetic relationships among the five main clades of Chlorophyceae have proven difficult to resolve.
Phylogenetic analyses of nuclear rDNA data have suggested a sister relationship between the Chlamydomonadales and Sphaeropleales, with the Chaetophorales, Oedogoniales, and Chaetopeltidales forming early diverging clades with uncertain interrelationships Booton et al. Chloroplast multi-gene analyses identified two main lineages within the Chlorophyceae: This dichotomy was independently supported by molecular signatures in chloroplast genes, such as presence of indels and transspliced introns.
The Chlamydomonadales forms the largest group of Chlorophyceae and has a complex taxonomic history. Molecular phylogenetic analyses of nuclear ribosomal DNA and chloroplast sequences have profoundly changed the concept of the class, which now includes a diverse range of taxa formally placed in the Dunaliellales, Chlorococcales, Tetrasporales, Chlorosarcinales, Volvocales and Chaetophorales Lewis et al.
As presently conceived, the class includes non-motile or motile unicells with two or four flagella, biflagellate colonies, filaments and cells that are imbedded in a mucilage envelope Nakazawa et al. A few species have evolved an obligate heterotrophic life style e. Several genera are polyphyletic, with the most extreme example being the large genus Chlamydomonas, which is distributed in at least five distinct lineages within the Chlamydomonadales Buchheim et al.
Phylogenetic analyses based on chloroplast genes and 18S sequences showed that quadriflagellate members with CCW or CW basal body orientation Golenkinia, Carteria, Pseudocarteria, Hafniomonas, Trochiscia, Treubaria and Cylindrocapsa form early diverging lineages, suggesting that the CW orientation of most chlamydomonadalean genera may have evolved from the CCW orientation in ancestral quadriflagellate members Nozaki et al.
The early diverging position of the quadriflagellate Tetraflagellochloris further supports this hypothesis Barsanti et al. Because the Chlamydomonadales include unicellular flagellates e. The Sphaeropleales form another large group of Chlorophyceae, including some of the most common freshwater phytoplankters such as Scenedesmus, Desmodesmus and Pediastrum, as well as picoplanktonic members Wolf et al.
Representatives are non-motile unicells, colonies or filaments, which produce biflagellate zoospores zoosporic or non-motile spores autosporic. Diversity and phylogenetic relationships within the Sphaeropleales have been studied by LewisKrienitz et al. The Chaetophorales of about 10 genera include unbranched e.
The Oedogoniales includes the filamentous genera Oedogonium, Oedocladium and Bulbochaete. They share a unique form of cytokinesis and a specialized form of oogamous sexual reproduction involving the production of stephanokont motile cells Pickett-Heaps, Phylogenetic relationships within the order have been studied by Alberghina et al.
The class is best known for its macroscopic marine representatives the green seaweedsbut several members also occur in freshwater or damp subaerial habitats such as soil, rocks, tree bark and leaves Chihara et al.
In terms of diversity in thallus complexity and cellular sophistication, the Ulvophyceae far exceed the other chlorophytan classes. Their morphologies range from microscopic unicells to macroscopic multicellular plants, and giant-celled organisms with unique cellular and physiological characteristics Mine et al. Four main cytomorphological types can be distinguished Cocquyt et al. The first type comprises non-motile uninucleate unicells, and is present in some Ulotrichales Chihara et al.
The second type consists of multicellular filaments or blades composed of uninucleate cells; it characterizes most Ulvales, Ulotrichales and Trentepohliales.
This is known as the siphonocladous type and characterizes the Cladophorales and Blastophysa and some members of the Ulotrichales e.
The fourth type is better known as siphonous type and is characterized by plants consisting of a single giant tubular cell.
Evolution of Plants
It is present in the orders Bryopsidales and Dasycladales. Siphonous cells generally contain thousands to millions of nuclei. In contrast to the siphonocladous type, the cytoplasm of siphonous algae exhibits vigorous streaming, enabling transportation of transcripts across the plant Menzel, ; Menzel, ; Mine et al.
Although some siphonous algae are tiny microscopic siphons, many form large and complex seaweeds that exhibit morphological differentiation into structures that resemble the roots, stems, and leaves of land plants and even have similar functions Chisholm et al.
The evolution of siphonocladous and siphonous architectures coincided with several cytological and cytoskeletal specializations such as unique mechanisms of wounding response Menzel, ; La Claire, ; Kim et al. 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. In combination with morphological changes, this allows nutrient uptake from marine sediments Chisholm et al.
Understanding the phylogenetic relationships among the ulvophycean orders can provide important insights into the diversification of cytological types and evolution of morphological complexity in the class. These, along with the cyanobacteria often misleadingly called blue-green algaeform the phytoplankton of aquatic ecosystems. Others, including all brown algae Phaeophytamost red algae Rhodophytaand many green algae are multicellular.
The large marine forms of these phyla are usually called seaweeds. Plants are thought to have evolved from a class of freshwater green algae called the charophytes.
Two particular groups of charophyte, the Coleochaetales and the Charales, resemble the earliest land plants bryophytes in a variety of ways, including the structure of their chloroplasts and sperm cells, and the way their cells divide during mitosis.
The Importance of Vascular Tissue Plants are classified into two main groups: Both groups have multicellular embryos, which indicates that they are closely related to each another and distinguishes them from the green algae. Indeed, true plants are often referred to as embryophytes because of this feature. The bryophytes consist of the liverworts, hornworts, and mosses, and as their name implies none of these plants possess vascular tissues. All other plants, including the ferns, gymnosperms, and angiosperms, are classified as tracheophytes.
These possess specialized vascular tissues— phloem and xylem —to transport sugars, water, and minerals throughout their bodies. The oldest known vascular plants appeared in the middle Silurian period — million years ago ; the oldest known bryophytes appeared later, in the Devonian — million years ago.
Despite this, most scientists believe that bryophytes evolved before vascular plants, and that the earliest bryophytes have not been found because they fossilize poorly. This belief is supported by a variety of evidence, including morphological traits, ultrastructural features visible under the electron microscope, and molecular information obtained from gene sequencing.
Bryophytes Since bryophytes are land plants, they need to support themselves in air. However, because they lack lignified vascular tissues, this support must be provided largely by the turgor pressure of their cells. Consequently, they cannot grow to be very tall, and most bryophytes are small and rather inconspicuous.
An additional important feature of their lifestyle is their reproductive system. The male gametesproduced by reproductive structures called antheridia, are free-swimming sperm cells that need water to transport them to the female gametes, which are enclosed within structures called archegonia.
Because of the need for water, bryophytes are especially common in wet habitats such as bogs, streambanks, and in moist forests. However, they are not restricted to these habitats, and some mosses thrive in deserts, above the treeline, and in the Arctic tundra.
Among the living bryophytes, liverworts are probably most closely related to the earliest land plants, since unlike hornworts, mosses, and all vascular plants they do not possess stomata. Indeed, the fact that stomata first appeared in hornworts and mosses is evidence that vascular plants evolved from one of these two groups.
Vascular plants appear to be more closely related to mosses than to hornworts, because some mosses possess food-conducting cells leptoids and water-conducting cells hydroids that resemble the phloem and xylem of vascular plants.
Early Vascular Plants The first detailed vascular plant fossils appear in rocks from middle Silurian, about million years ago. The oldest of these, including a plant called Aglaophyton, appear to have possessed conducting cells similar to the hydroids of mosses.
These ancient plants, which are sometimes called prototracheophytes, may have been an evolutionary link between the bryophytes and the true tracheophytes. Early vascular plants possessed two features that made them especially well adapted to life on land. First, their vascular tissues transported sugars, nutrients, and water far more efficiently than the conducting cells of mosses. Second, they evolved the ability to synthesize ligninwhich made the cell walls of their vascular tissues rigid and supportive.
Taken together, these features allowed them to grow much larger than their bryophyte ancestors and considerably reduced their dependence on moist habitats. There are three major groups of tracheophytes: Since the first appearance of tracheophytes in the Silurian, the fossil record shows three major evolutionary transitions, in each of which a group of plants that were predominant before the transition is largely replaced by a different group that becomes predominant afterward.
The first such transition occurred in the late Devonian, approximately million years ago. Prior to this time the most common plants were simple, seedless vascular plants in various phyla, several of which are now extinct.
However, one phylum from this time, the Psilophyta, still has two living genera, including a greenhouse weed called Psilotum. From the late Devonian until the end of the Carboniferous period million years ago larger, more complex seedless plants were predominant. The main phyla were the Lycophyta, the Sphenophyta, and the Pterophyta.
All three groups contain living relatives, including club mosses Lycopodiaceae in the Lycophyta, Equisetum the only living genus of sphenophytesand ferns, which are pterophytes. Only the ferns, which have about 11, living species, are common today, but in the Carboniferous these three phyla comprised a large fraction of the vegetation on the planet.
Many grew to the size of trees and dominated the tropical and subtropical swamps that covered much of the globe at this time. The second major transition was the decline of the lycophytes, sphenophytes, and pterophytes at the end of the Carboniferous and their replacement by gymnosperms in the early Permian. Gymnosperms dominated the vegetation of the land for the next million years until they themselves began to decline and were replaced by angiosperms in the middle of the Cretaceous.
Although one group of gymnosperms the conifers is still abundant, the angiosperms have been the most diverse and widespread group of plants on Earth for the last million years. Gymnosperms The gymnosperms probably evolved from an extinct phylum of seedless vascular plants, the progymnosperms, that appeared about million years ago. The fossils of these plants, some of which were large trees, appear to form a link between the trimerophytes another extinct phylum of seedless vascular plants and true gymnosperms.
Progymnosperms reproduced by means of spores like the former, but their vascular tissues were very similar to those of living conifers. The oldest true gymnosperms, which produce seeds rather than spores, first appeared about million years ago.
The evolution of seeds, with their hard, resilient coats, was almost certainly a key factor in the success of the group. A second factor was the evolution of pollen grains to protect and transport the male gametes. As a consequence of this, gymnosperms, unlike seedless vascular plants, were no longer dependent on water for successful fertilization and could broadcast their male gametes on the wind. Several early gymnosperm groups are now extinct, but there are four phyla with living representatives: