Brief History Of Green Plant Evolution

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Recent data have provided evidence for an unrecognized ancient lineage of green plants, which persists in marine deep-water environments. The green plants are a major group of photosynthetic eukaryotes that have played a prominent role in the global ecosystem for millions of years. A schism early in their evolution gave rise to two major lineages, one of which diversified in the world's oceans and gave rise to a large diversity of marine and freshwater green algae (Chlorophyta) while the other gave rise to a diverse array of freshwater green algae and the land plants (Streptophyta). It is generally believed that the earliest-diverging Chlorophyta were motile planktonic unicells, but the discovery of an ancient group of deep-water seaweeds shakes up our understanding of the basal branches of the green plant phylogeny. In this review, we discuss current insights into the origin and diversification of the green lineage.

A brief history of green plant evolution

The green plants are one of the most dominant groups of primary producers on earth. They include the green algae and the embryophytes, which are generally known as the land plants. While the green algae are ubiquitous in the world's oceans and freshwater ecosystems, the land plants are major structural components of terrestrial ecosystems [1,2]. The green plant lineage is ancient, probably over a billion years old [3,4], and intricate evolutionary trajectories underlie its present taxonomic and ecological diversity.

The green plants originated following a primary endosymbiotic event in which a heterotrophic eukaryotic host cell engulfed a photosynthetic cyanobacterium-like prokaryote that became stably integrated and ultimately turned into a plastid [5,6]. This single event marked the origin of oxygenic photosynthesis in eukaryotes and gave rise to three autotrophic lineages with primary plastids: the green plants, the red algae and the glaucophytes. From this starting point, photosynthesis spread widely among the eukaryotes via secondary endosymbiotic events that involved the capture of either green or red algae by diverse non-photosynthetic eukaryotes, thus transferring the captured cyanobacterial endosymbionts (i.e., the plastids) laterally among eukaryotes [5]. Some of these secondary endosymbiotic partnerships have in their turn been captured by other eukaryotes, known as tertiary endosymbiosis, resulting in an intricate history of plastid acquisition [reviewed in 5,6,7]. Three groups of photosynthetic eukaryotes now have plastids derived from a green algal endosymbiont: the chlorarachniophytes, a small group of mixotrophic algae from tropical seas, the euglenophytes, which are especially common in freshwater, and some green dinoflagellates. A much wider diversity of photosynthetic eukaryotes, including the cryptophytes, haptophytes, diatoms, chrysophytes, brown seaweeds and dinoflagellates, have acquired plastids from a red algal ancestor, either by a single or by repeated endosymbiotic events [6,8].

An early split in the evolution of the green plants gave rise to its two principal lineages that have subsequently followed radically different evolutionary trajectories (Fig. 1) [1,9,10]. One lineage, the Chlorophyta, diversified as plankton in the oceans and gave rise to the modern prasinophytes and the core chlorophytes that radiated in marine coastal and freshwater environments. The Chlorophyta now encompass a large diversity of green algae with a bewildering variety of body forms, eco-physiological traits and life cycle strategies [1]. The second lineage, the Streptophyta, evolved in freshwater and damp terrestrial habitats and colonized dry land approximately 476-432 million years ago, giving rise to the land plants [11]. Contemporary streptophytes comprise a diverse array of mainly freshwater algae (collectively termed the charophytes) and the vastly species-rich land plants [11].

The early evolutionary history of the Chlorophyta in the oceans of the Meso- and Neoproterozoic (between 700 and 1500 million year ago) is marked by a radiation of planktonic unicells [2]. These ancestral green algae were of fundamental importance to the eukaryotic greening that shaped the geochemistry of our planet [12]. Although the fossil record is clearly incomplete, analysis of microfossils suggests that green algae were prevalent in the eukaryotic oceanic phytoplankton of the Paleozoic Era [2,13,14]. Subsequently, the red plastid-containing dinoflagellates, coccolithophores and diatoms increased in abundance to largely displace the green algae in the phytoplankton from the end-Permian extinction to the present. This evolutionary transition has been related to a long-term change in the chemistry of the ocean during the Mesozoic combined with specific eco-physiological traits of the red plastid-containing lineages [15]. Trace element usage in algae with a red-type plastid differs from that of the green algae, which may have been advantageous following a shift in the redox conditions of the oceans [16]. The pigment sets of red plastids provide for higher underwater photosynthetic efficiency compared to green plastids, and may be another explanation for the red dominance in the seas [2,17]. In addition, the success of lineages with red-type plastids has been explained by better portability of red-type plastids via secondary endosymbiosis to diverse eukaryotic hosts [16], but this hypothesis has been questioned [18].

Despite this red dominance in the phytoplankton, green algae continue to play prominent roles in contemporary marine environments. Prasinophytic picoplanktonic species (i.e., with cells smaller than 3 µm) can dominate both photosynthetic biomass and production in open oceans and coastal systems [19]. In addition, the green seaweeds of the class Ulvophyceae, which radiated in marine benthic habitats in the Neoproterozoic [20-22] (Fig. 1), form key components in many contemporary coastal environments.

The first eukaryotic algae in freshwater environments were probably unicellular streptophytes, which prevailed in these ecosystems in the Proterozoic [23]. During the Paleozoic, the two principal multicellular groups of charophytes, the conjugating green algae (Zygnematophyceae) and stoneworts (Charophyceae) radiated, and the latter dominated freshwater macrophytic communities between the Permian and Early Cretaceous [24]. In the Late Cretaceous and Tertiary, they were largely replaced by freshwater angiosperms. Two classes of the Chlorophyta, the Chlorophyceae and Trebouxiophyceae, adapted to freshwater environments during the Neoproterozioc [4] (Fig. 1) and have dominated freshwater planktonic assemblages during the Paleozoic and Mesozoic Eras while the diversity and abundance of charophytes gradually decreased [23,24]. The fall of the green dominance of freshwater phytoplankton started with the appearance of freshwater dinoflagellates in the Early Cretaceous, and the radiation of diatoms and chrysophytes during the Cenozoic.

The dominance of algae with red-type plastids in the seas (and to a lesser extent in freshwater environments) is in sharp contrast to the situation on land where photosynthesis has been dominated by the green land plants ever since they colonized the land in the Ordovician [25].

Deep branches of the Chlorophyta

Molecular phylogenetic, ultrastructural and biochemical studies have identified the prasinophytes as a paraphyletic assemblage of unicells with a wide variety of cell shapes (Fig. 1), flagellar numbers and behaviour, body scale shapes, mitotic processes, biochemical features and photosynthetic pigment signatures [26-30].

The critical phylogenetic position of the prasinophytes, diverging early from the remaining Chlorophyta (Fig. 1), reinforced the notion that the ancestral chlorophytes were marine planktonic unicellular flagellates with characters typical of extant prasinophytes such as the presence of organic body scales [31,32]. The nature of this hypothetical ancestral green flagellate (AGF, Fig. 1), however, still remains uncertain. Moestrup [33] proposed that small, simple flagellate cells most closely resemble the AGF. Alternatively, the food uptake apparatus of some complex mixotrophic flagellates has been interpreted as a feature inherited from a phagotrophic ancestor of the green plants that was subsequently lost in most green algae [2,34,35].

A better understanding of prasinophytic diversity and relationships has the potential to shed light on the nature of the common ancestor of the green plants. Originally, only flagellate unicells covered by organic body scales were classified in the prasinophytes [31]. The discovery of several new species and the application of environmental sequencing have revealed a greater morphological and ecological diversity [28,36,37]. Non-motile (coccoid) forms have been identified in several of the major prasinophytic lineages and many members lack scales or have other types of specialized cell coverings (Table 1). Prasinophytes are primarily marine but several representatives have adapted to freshwater environments (Table 1).

Although there is little doubt that sex predates diversification of extant eukaryotes [38,39], it has rarely been observed in prasinophytes. A notable exception is Nephroselmis, where sexual reproduction has been detected in cultures [40,41]. However, circumstantial evidence points toward a much wider occurrence of sex among prasinophytes. For example, members of the Pyramimonadales produce resistant cysts (phycomata) containing two chloroplasts, indicative of sexual reproduction [34]. In addition, sexual reproduction has been suggested in Micromonas and Ostreococcus based on the presence of meiosis-specific and sex-related genes in their genomes [12,42].

Several studies have aimed at resolving the relationships among the prasinophytic lineages, which has proven to be a difficult task due to the antiquity of these divergences. Small subunit nuclear ribosomal DNA (18S rDNA) sequences have been, until recently, the primary source of data for inferring phylogenetic relationships among green plants [43]. Although 18S data have been useful in delineating the main prasinophytic lineages [27,30,36], analyses of these single gene datasets have not resolved the relationships among them. A reliable phylogenetic resolution for an ancient group like the green plants requires analysis of a large number of genes and species.

Multi-gene data derived from chloroplast genomes, which are presently available for five prasinophytes, are just beginning to shed light on the ancient divergences of the Chlorophyta. A recent chloroplast phylogenomic analysis identified Nephroselmis (Nephroselmidophyceae) as the earliest-branching chlorophytic lineage [35] (Fig. 1). This flagellate with a complex covering of scales and two unequal flagella (Fig. 2A,B, Table 1) might thus represents our best guess of what the AGF might have looked like. Interestingly, Nephroselmis is one of the few prasinophytes where sexual reproduction has been well documented [41].

The close relationship between the Pyramimonadales and the Mamiellophyceae was an unexpected result from chloroplast phylogenomic studies [35] (Fig. 1). The Pyramimonadales are relatively large flagellates with complex body scale coverings (Fig. 2C-D), and, as mentioned above, some of its members are unique among green plants in possessing a food uptake apparatus [34]. The Mamiellophyceae is a large group comprising the morphologically and ecologically diverse Mamiellales and two smaller clades, the Monomastigales and Dolichomastidales [36]. The phylogenetic affinity of the latter two has long been uncertain because several of their members lack scales and have atypical surface structures (Table 1). The Mamiellales are probably the largest and most diverse group of prasinophytes (Table 1). Several members (e.g., Ostreococcus and Micromonas) may form major components of marine picoeukaryotic communities [19,44,45]. These algae have cell sizes smaller than those of many bacteria and show highly reduced cellular complexity and unusually compact genomes [12,42,46]. Their small cellular sizes and reduced genome have led to the hypothesis that they may represent “the bare limits of life as a free-living photosynthetic eukaryote” [42]. These simplifications in body form and genome compaction have been interpreted as being derived from the more complex organization seen in the Pyramimonadales and other prasinophytes [35].

There are several other groups of early-branching prasinophytes that we cannot place in the tree with great precision, either because only single-gene data are available or because genome-scale phylogenetic analyses provide equivocal results.

1. The Pycnococcaceae is a small clade of marine flagellates and coccoids (Fig. 1, Table 1). Some studies based on 18S rDNA sequences have related this clade with the Nephroselmidophyceae [27,30] but this relationship has not been supported by chloroplast multi-gene analyses [35].

2. The Prasinococcales includes a few marine coccoid prasinophytes [47,48] (Fig. 2E, Table 1) and has been suggested to form an early-diverging clade based on 18S data [30] (Fig. 1). Multi-gene data has not yet been generated for this group.

3. The Picocystis clade has been identified by environmental and culture-based sequencing. It includes a number of undescribed coccoid prasinophytes along with the saline lake-dwelling coccoid Picocystis (Table 1). This clade emerges as a sister lineage to the core chlorophytes based on 18S and multi-gene data (Fig. 1) but strong support for this relationship is lacking [30,36,49].

4. Environmental sequencing of photosynthetic picoeukaryotic communities has identified two additional prasinophytic clades (termed clades VIII and IX) [50-52]. The nature and phylogenetic affinities of these clades remain elusive.

The prasinophytes have given rise to the morphologically and ecologically diverse core chlorophytes (Fig. 1). This group includes the early-diverging Chlorodendrophyceae, a clade uniting the marine or freshwater quadriflagellates Tetraselmis and Scherffelia [30]. These unicells were traditionally regarded as members of the prasinophytes but they share several ultrastructural features with the three major core chlorophytic clades Ulvophyceae, Trebouxiophyceae and Chlorophyceae [1]. The core chlorophytes are characterized by a new mode of cell division that is mediated by a phycoplast, which was subsequently lost in the Ulvophyceae. Several eco-physiological adaptations have likely led to the success of the Chlorophyceae and Trebouxiophyceae in freshwater and soil environments. The Ulvophyceae have mainly diversified along marine shorelines and have evolved an unrivalled diversity of body forms, ranging from microscopic unicells to macroscopic plants, and giant-celled organisms with unique cellular and physiological characteristics [22]. They are best known as the green seaweeds that frequently dominate rocky shores and tropical lagoons. Several members of the core chlorophytes have engaged in symbioses with a diverse range of eukaryotes, including fungi to form lichens, ciliates, foraminifera, cnidarians and vertebrates [53-55], or have evolved an obligate heterotrophic life style as parasites [56].

An ancient lineage of deep-water green seaweeds

A recently published study has provided evidence for another early-diverging chlorophytic lineage, the Palmophyllales [57]. This group includes the little-known seaweeds Palmophyllum, Verdigellas, and possibly Palmoclathrus, three genera that thrive in deep-water and other dimly lit, benthic marine habitats. Although gene sequence-based phylogenies support a deeply-branching Palmophyllales, its exact phylogenetic placement remains uncertain. Analyses of two large plastid-encoded genes (atpB and rbcL) placed the Palmophyllales sister to the remaining Chlorophyta. On the other hand, analysis of nuclear 18S rDNA sequences allied the Palmophyllales with the early-diverging Prasinococcales (Fig. 1). The latter relationship is supported by a number of shared cytological features, such as a mucus-secreting system [48,58] and similarities in cell division [37,47,59].

Members of the Palmophyllales feature a unique type of multicellularity. They form well-defined macroscopic bodies composed of small spherical cells embedded in a firm gelatinous matrix (palmelloid organization) [58,60-62]. Although cells throughout the gelatinous matrix are morphologically identical (Fig. 2F), certain members have evolved large, complex erect bodies. For example, species of Verdigellas (Figs 1, 2G) attach to the substrate by means of a holdfast structure above which the rest of the body expands, resulting in umbrella-like plants that are well-adapted to maximally capture the sparse light penetrating from the sea surface and reflected from the underlying calcareous substratum. Palmoclathrus, a genus from seasonally changing temperate waters, features a stout, perennial holdfast system consisting of a basal disc and one to several cylindrical stalks from which seasonal blades grow [60] (Fig. 2I). Palmophyllum is morphologically simpler, forming irregular lobed crusts that are tightly attached to the substrate (Fig. 2H). Despite careful investigation, motile stages or ultrastructural traces from flagella have never been observed [58,59,61]. Interestingly, a number of prasinophytes have been described to have palmelloid stages in their life cycle, although they never form large and complex bodies like the Palmophyllales (Table 1). The early-diverging nature of the non-flagellate Palmophyllales and Prasinococcales, along with the wide phylogenetic distribution of non-motile prasinophytes, raises questions about the nature of the green ancestor. Although there is little doubt that flagella must have been present in a life cycle stage of the green plant ancestor, it may be possible that this ancestor was a non-motile unicell with transient motile stages.

It is striking that an ancient lineage of green algae such as the Palmophyllales occurs almost exclusively in dimly lit deep-water benthic habitats. Low-light ecosystems present a challenging environment for photosynthetic organisms and relatively few algae live in such habitats [63]. Verdigellas has been recorded from depths down to 200 m [57,62], where only about 0.05% of the irradiance at the water surface remains [63]. This results in extremely low primary productivity of Verdigellas compared to shallow-water green seaweeds [64]. Palmophyllum and Palmoclathrus species occur in somewhat shallower water, generally between 10 and 100 m [60,61].

Member of the Palmophyllales lack the green light-harvesting photosynthetic pigments siphonoxanthin and siphonein typically found in low-light adapted green algae [59,61]. Instead, they seem to have adapted to low-light conditions by maintaining high concentrations of chlorophyll b, which absorbs the blue-green light of deeper water more efficiently than chlorophyll a does [65].

The ability to grow in deep, low-light habitats may be of key importance to the Palmophyllales' persistence. Deep habitats feature diminished abiotic stressors (e.g., wave action and temperature variation) and reduced grazing and competition for substrate. Whereas the more recently evolved green seaweeds (Ulvophyceae) of the core chlorophytes possess morphological and biochemical adaptations that allow them to withstand such stresses [66], the Palmophyllales lack protective attributes such as calcification or cortication, and they may have found refuge from competition and herbivory in deep-water habitats.

Marine deep-water environments are home to phylogenetic relicts of other lineages of organisms such as the hagfishes [67], chimaeras and cow sharks [68], stalked crinoids and other invertebrates [69]. The onshore-offshore hypothesis describes the onshore origination and offshore retreat of marine groups in the fossil record [70]. The early-branching position of the taxon-poor, deep-water Palmophyllales as compared to the taxon-rich and predominantly shallow-water prasinophytes and core chlorophytes may be interpreted as an example of this phenomenon in photosynthetic organisms.

Ancient streptophytes and the progenitors of land plants

The origin of land plants was a key event in the history of life and has led to dramatic changes in the earth's environment, including the development of the entire terrestrial ecosystem [25]. Many studies have focused on the relationship among charophytes and have sought to determine the origins of land plants [9,10,71-73].

The charophytes are mostly freshwater green algae with diverse morphologies ranging from simple unicells and filaments to complex and highly specialized macrophytes. Morphological and molecular data have revealed six distinct groups of charophytes: Mesostigmatophyceae, Chlorokybophyceae, Klebsormidiophyceae, Zygnematophyceae, Charophyceae and Coleochaetophyceae [11] (Fig. 1). Considerable progress has been made during the past decade in clarifying the relationships among these lineages, and elucidating the closest living relative of the land plants [9,10,71-75].

Multi-gene data have provided evidence that the morphologically simple charophytes Mesostigma (Mesostigmatophyceae) and Chlorokybus (Chlorokybophyceae) form the earliest-diverging streptophytic lineages (Fig. 1) [9,10,72,75]. This result is consistent with ultrastructural features of their cells [1,32] and discrete molecular characteristics such as shared multi-gene families or gene duplications [76,77]. Some phylogenies inferred from nuclear multi-gene data placed Mesostigma sister to the remaining Streptophyta [22,72], a position that is supported by the fact that Mesostigma is the only streptophyte with flagella in its vegetative stage, a presumed ancestral feature of the green algae. Conversely, phylogenies based on complete chloroplast genomes have suggested a sister relationship between Mesostigma and Chlorokybus [9,10]. Mesostigma is a freshwater, scaly, asymmetrical unicell with two flagella and a unique suite of photosynthetic pigments. Chlorokybus occurs in moist terrestrial habitats where it forms packets of a few cells, which may produce motile spores [11].

Gene sequence-based phylogenies unambiguously show that the freshwater or terrestrial filamentous Klebsormidiophyceae diverged after the Mesostigmatophyceae and Chlorokybophyceae [71,72,78] (Fig. 1), a phylogenetic position that is further supported by several chloroplast genomic features [79].

Interestingly, sexual reproduction has not been observed in any of these early-diverging lineages and is only known in the later-diverging streptophytes [11]. However, determining whether these lineages are truly asexual will require genomic screening, as numerous allegedly asexual chlorophytic members have been shown to have cryptic potential for sex by the presence of meiosis and sex-related genes in their genomes [12,42,80].

In contrast to the three early-diverging streptophytic lineages (Mesostigmatophyceae, Chlorokybophyceae and Klebsormidiophyceae) that undergo cell division by furrowing, the cluster consisting of the Charophyceae, Zygnematophyceae, Coleochaetophyceae and the land plants evolved a new mechanism of cell-wall formation during cell division, which involved the production of a phragmoplast. In addition, most of the later-diverging streptophytes have cell-walls with plasmodesmata, facilitating cytoplasmic communication between cells and development of complex tissues [81].

Numerous studies have focussed on identifying the closest living relative to the land plants, and several lineages have been proposed based on morphological, ultrastructural and molecular data [11,23]. Multi-gene phylogenies have been sensitive to taxon and gene sampling and provided equivocal results, suggesting the morphologically complex Charophyceae [22,71,82] or Coleochaetophyceae [35,72], or the structurally simpler Zygnematophyceae [9,10,73,75] as the sister lineage of the land plants.

The colonization of dry land involved many challenges such as desiccation, increased temperature fluctuations, exposure to UV radiation and gravity [83-85]. Several physiological and morphological innovations have allowed successful adaption to life on land [23,81,83]. Some of these are also found in one or more algal relatives of embryophytes and thus likely evolved before the origin of land plants, including cellulosic cell walls, multicellularity, differentiated cells and tissues, intercellular communication networks (plasmodesmata and plant hormones), zygote retention and placenta. Other innovations, such as a life cycle involving alternation of two distinct multicellular generations and protected embryos appear to be unique to land plants [81]. Additional adaptations to life on dry land include enhanced osmoregulation, desiccation and freezing tolerance, and heat resistance [83,86].

Comparative genomic studies have indicated that the molecular bases of many land plant innovations evolved before the transition to land [23,73,87]. For example, several genes that have been hypothesized to be important in the evolution of land plants [81] may have true orthologs in the Coleochaetophyceae and/or Zygnematophyceae [73,87]. The diversification of embryophytes and evolution of complex plants was associated with expansion of numerous gene families, including MADS box genes [88], homeobox genes [89], OPR genes [90] and genes involved in signalling pathways, such as auxin, ABA and cytokinin [86,87,91]. Expansion of the glutaredoxins gene family likely resulted in genes with novel functions in development and pathogenesis response [92]. The unique sexual life cycle of land plants possible evolved through expansion of homeodomain gene networks [88].

Conclusions and prospects

Molecular phylogenetic studies have drastically reshaped our views of green plant evolution [1,2,43]. It is now generally accepted that the green plants diverged into two discrete lineages (Fig. 1). One lineage, the Chlorophyta, includes several early-diverging clades of unicellular green algae (the prasinophytes) and the morphologically diverse core chlorophytes. The other lineage, the Streptophyta, comprises the early-branching charophytic green algae and the land plants.

Resolving the relationships between these early-branching clades is crucial to address questions about the origin of the green lineage and to learn about the evolutionary trajectories responsible for the remarkable diversity of green algae and the emergence of the land plants. However, the antiquity of the green lineage makes the phylogenetic reconstruction of early-branching events difficult due to the lack of information in current DNA sequence datasets and potential methodological biases.

It has become clear that to achieve a reliable phylogenetic resolution for ancient groups like the green plants, a large number of genes from many species must be analysed by applying state of the art phylogenetic techniques [93,94]. Multi-gene phylogenetic investigations are just starting to shed light on the basal branches of the green plant phylogeny [9,10,35]. High-throughput DNA sequencing techniques can facilitate broader gene and taxon sampling and will undoubtedly lead to more robust phylogenies [72,73].

The identification of deep-branching lineages is crucial to make robust inferences about the nature of the common ancestor of the green plant lineage. Sequencing of culture collections and environmental picoplankton samples has led to the discovery of several ancient green algal lineages [27,30,36,50-52]. In addition, sampling of challenging habitats such as marine deep water ecosystems has recently revealed an unrecognized deep-branching lineage of green plants [57]. Further exploration of diversity in understudied ecosystems such as deep marine waters, tropical coral reefs and sand habitats may lead to the discovery of other ancient groups and further alter our understanding of the early evolution of green plants.


Biflagellate: Having two flagella

Body scales: organic (non-mineralized) plate-like structures, produced within the Golgi apparatus, and covering de cell surface of many prasinophytic species.

Clade: Group of organisms allied by common descent (also called a lineage).

Coccoid: Spherical, non-motile unicellular microorganism.

Mixotrophic: Having partly autotrophic and partly heterotrophic nutrition.

Flagella: long whip-like organelles that propels cells through a liquid medium. Flagella contain a highly conserved (9 + 2) arrangement of microtubules. They are homologous with cilia, but generally longer and less numerous.

Flagellate: Noun: Motile unicellular eukaryotic microorganism, which swim by means of flagella. Flagellates include photosynthetic and non-photosynthetic heterotrophic species, which do not form a natural group of organisms but are distributed in several distantly related eukaryotic groups. Adjective: bearing one or more flagella.

Paraphyletic group: A group of organisms that has evolved from a common ancestor but which does not contain all descendants of that ancestor. Green algae and charophytes are paraphyletic groups because they do not include the land plants. Similarly, prasinophytes are paraphyletic with the exclusion of the core chlorophytes. Paraphyletic groups are characterized by shared primitive (plesiomorphic) characters. For the green algae these include the presence of double membrane-bound plastids containing chlorophyll a and b, and several ultrastructural features of the chloroplast and flagella, all of which are also shared with the land plants.

Palmelloid: A kind of organization of the algal body with cells that are separate but remain enclosed within a mucilage envelope.

Phagotroph: Heterotrophic or mixotrophic organism that ingests nutrients by engulfing solid particles.

Phragmoplast: Array of microtubules oriented perpendicularly to the plane of cell division, determining the formation of the cell plate and new cell wall. Phragmoplasts occur in land plants and their closest charophytic relatives, Charophyceae, Zygnematophyceae and Coleochaetophyceae.

Phycoma: A resistant, thick-walled, cyst-like stage in the life cycle of certain prasinophytes.

Phycoplast: Array of microtubules oriented parallel to the plane of cell division, determining the formation of a new cell wall. Phycoplasts occur in the core chlorophytic classes Chlorodendrophyceae, Trebouxiophyceae and Chlorophyceae.

Picoplankton: The fraction of the plankton composed by cells between 0.2 and 3 µm.

Plasmodesmata: Cytoplasmic threads running transversely through cell walls and connecting the cytoplasm of adjacent cells.

Quadriflagellate: Having four flagella.

Red-type plastid: plastids derived from a red alga via secondary or tertiary endosymbiosis.

Siphonein and siphonoxanthin: Xanthophyll accessory pigments found in Ulvophyceae and some prasinophytes. The possession of the two pigments is believed to be an adaptation to life in deep water, because they are well suited to the harvesting of the green light found there [65].

Uniflagellate: Having a single flagellum.