Into the deep: new discoveries at the base of the green plant phylogeny

Recent data have provided evidence for an unrecognised ancient lineage of green plants that 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 unicellular organisms, but the discovery of an ancient group of deep-water seaweeds has challenged 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 plant lineage.     

Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences

A phylogenetic tree of most of the major groups of organisms has been constructed from the 352 5S ribosomal RNA sequences now available. The tree suggests that there are several major groups of eubacteria that diverged during the early stages of their evolution. Metabacteria (= archaebacteria) and eukaryotes separated after the emergence of eubacteria. Among eukaryotes, red algae emerged first; and, later, thraustochytrids (a Proctista group), ascomycetes (yeast), green plants (green algae and land plants), "yellow algae" (brown algae, diatoms, and chrysophyte algae), basidiomycetes (mushrooms and rusts), slime- and water molds, various protozoans, and animals emerged, approximately in that order. Three major types of photosynthetic eukaryotes--i.e., red algae (= Chlorophyll a group), green plants (Chl. a + b group) and yellow algae (Chl. a + c)--are remotely related to one another. Other photosynthetic unicellular protozoans--such as Cyanophora (Chl. a), Euglenophyta (Chl. a + b), Cryptophyta (Chl. a + c), and Dinophyta (Chl. a + c)--seem to have separated shortly after the emergence of the yellow algae.      

Phylogeny and Molecular Evolution of the Green Algae

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 flagellate. 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 lineages, the relationships among core chlorophyte clades (Chlorodendrophyceae, Ulvophyceae, Trebouxiophyceae and Chlorophyceae), and the relationships among the streptophytes. Current phylogenetic hypotheses provide an evolutionary framework for molecular evolutionary studies and comparative genomics. This review summarizes 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 evolution of genetic codes and the translational apparatus in green seaweeds. Finally, we discuss molecular evolution in the streptophyte lineage, emphasizing the genetic facilitation of land plant origins.     

Migration of the plastid genome to the nucleus in a peridinin dinoflagellate

Dinoflagellate algae are important primary producers and of significant ecological and economic impact because of their ability to form "red tides". They are also models for evolutionary research because of an unparalleled ability to capture photosynthetic organelles (plastids) through endosymbiosis. The nature and extent of the plastid genome in the dominant perdinin-containing dinoflagellates remain, however, two of the most intriguing issues in plastid evolution. The plastid genome in these taxa is reduced to single-gene minicircles encoding an incomplete (until now 15) set of plastid proteins. The location of the remaining photosynthetic genes is unknown. We generated a data set of 6,480 unique expressed sequence tags (ESTs) from the toxic dinoflagellate Alexandrium tamarense (for details, see the Experimental Procedures in the Supplemental Data) to find the missing plastid genes and to understand the impact of endosymbiosis on genome evolution. Here we identify 48 of the non-minicircle-encoded photosynthetic genes in the nuclear genome of A. tamarense, accounting for the majority of the photosystem. Fifteen genes that are always found on the plastid genome of other algae and plants have been transferred to the nucleus in A. tamarense. The plastid-targeted genes have red and green algal origins. These results highlight the unique position of dinoflagellates as the champions of plastid gene transfer to the nucleus among photosynthetic eukaryotes.     

Regulation of PSII function in Cyanothece sp. ATCC 51142 during a light–dark cycle

Photosynthesis Research - Cyanobacteria, as well as green algae and higher plants, have highly conserved photosynthetic machinery. Cyanothece sp. ATCC 51142 is a unicellular, aerobic, diazotrophic...     

Nondestructive evaluation of photosynthesis by delayed luminescence in Arabidopsis in Petri dishes

Nondestructive evaluation of photosynthesis is a valuable tool in the field and laboratory. Delayed luminescence (DL) can reflect charge recombination through the backflow of electrons. However, DL detection has not yet been adapted for whole plants in Petri dishes. To compensate for differences in DL decay between sibling Arabidopsis plants grown under the same conditions, we developed a time-sequential double measurement method. Using this method, we examined the influence of photosynthetic electron flow inhibitors, and differences in the DL decay curves were categorized by considering the initial and late phases of the decay curves, as well as their intermediate slopes. The appearance of concavity and convexity in DL curves in Arabidopsis was different from unicellular algae, suggesting complexity in the photosynthetic machinery of higher plants. This detection method should be invaluable for evaluating photosynthetic defects in higher plants under sterile conditions without interrupting plant culture.     

Origin of land plants: Do conjugating green algae hold the key?

Background  

The terrestrial habitat was colonized by the ancestors of modern land plants about 500 to 470 million years ago. Today it is widely accepted that land plants (embryophytes) evolved from streptophyte algae, also referred to as charophycean algae. The streptophyte algae are a paraphyletic group of green algae, ranging from unicellular flagellates to morphologically complex forms such as the stoneworts (Charales). For a better understanding of the evolution of land plants, it is of prime importance to identify the streptophyte algae that are the sister-group to the embryophytes. The Charales, the Coleochaetales or more recently the Zygnematales have been considered to be the sister group of the embryophytes However, despite many years of phylogenetic studies, this question has not been resolved and remains controversial.     

Adaptation of the Photosynthetic Apparatus of Chlorella and Ankistrodesmus to Blue and Red Light

The mode of adaptation of the photosynthetic apparatus of three unicellular green algae, Ankistrodesmus braunii, Chlorella fusca and Chlorella saccharophila to red and blue light are documented by the fluence-rate curves of photosynthetic oxygen evolution. For all three algae tested photosynthetic capacity, respiration and light compensation point were higher for cells grown under red light, while the chlorophyll content increased in blue light-grown cells. Blue light-adapted cells have a lower chlorophyll a to chlorophyll b ratio and more chlorophyll in the light-harvesting system than red light-adapted cells, as shown in the electrophoretic profile of the pigment-protein complexes. It is concluded that the action of red light resembles that of high levels of white light, while blue light causes the same effects as low levels of white light. In agreement with previous publications these findings indicate that the mode of adaptation to different light qualities is ubiquitous in unicellular green algae.     

Multiple origins of the symbioses in Paramecium bursaria

Many organisms have symbioses with photosynthetic algae as typified by corals, clams, lichens, and some protozoa. Paramecium bursaria contains green algal symbionts and this unicellular ciliate is a textbook example used for microscopic observation in junior high school science projects. We have determined molecular phylogenies for the green algal symbionts. The symbiotic algae are the main constituent of the Paramecium cytoplasm, and we have recognized a total of four species, of which two were newly discovered in the present study. One should be regarded genetically as Chlorella vulgaris, and it belongs phylogenetically to the Chlorella clade (Chlorellaceae, Trebouxiophyceae) as well as "American" and "European" groups, which we previously introduced. Their genetic dissimilarities are 0.50-0.83% in 18S rDNA comparisons, but those of the internal transcribed spacer 2 (ITS2) reach an unambiguous level (22.6-26.6%). These dissimilarities suggest that they are equivalent to discrete species derived from multiple origins as paramecian symbionts. Another newcomer was clearly separated from the Chlorellaceae, and this alga clustered with Coccomyxa spp. in ITS2 analyses. These symbiotic relations indicate multiple origins of symbionts.     

Phylogenetic viewpoints on regulation of light harvesting and electron transport in eukaryotic photosynthetic organisms

The comparative study of photosynthetic regulation in the thylakoid membrane of different phylogenetic groups can yield valuable insights into mechanisms, genetic requirements and redundancy of regulatory processes. This review offers a brief summary on the current understanding of light harvesting and photosynthetic electron transport regulation in different photosynthetic eukaryotes, with a special focus on the comparison between higher plants and unicellular algae of secondary endosymbiotic origin. The foundations of thylakoid structure, light harvesting, reversible protein phosphorylation and PSI-mediated cyclic electron transport are traced not only from green algae to vascular plants but also at the branching point between the “green” and the “red” lineage of photosynthetic organisms. This approach was particularly valuable in revealing processes that (1) are highly conserved between phylogenetic groups, (2) serve a common physiological role but nevertheless originate in divergent genetic backgrounds or (3) are missing in one phylogenetic branch despite their unequivocal importance in another, necessitating a search for alternative regulatory mechanisms and interactions.     

Leveraging metabolomics for functional investigations in sequenced marine diatoms

Recent years have witnessed the genomic decoding of a wide range of photosynthetic organisms from the model plant Arabidopsis thaliana and the complex genomes of important crop species to single-celled marine phytoplankton. The comparative sequencing of green, red and brown algae has provided considerable insight into a number of important questions concerning their evolution, physiology and metabolism. The combinatorial application of metabolomics has further deepened our understanding both of the function of individual genes and of metabolic processes. Here we discuss the power of utilising metabolomics in conjunction with sequencing data to gain greater insight into the metabolic hierarchies underpinning the function of individual organisms, using unicellular marine diatoms as a case study to exemplify the advantages of this approach.     

Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye

The transition from unicellular to differentiated multicellular organisms constitutes an increase in the level complexity, because previously existing individuals are combined to form a new, higher-level individual. The volvocine algae represent a unique opportunity to study this transition because they diverged relatively recently from unicellular relatives and because extant species display a range of intermediate grades between unicellular and multicellular, with functional specialization of cells. Following the approach Darwin used to understand "organs of extreme perfection" such as the vertebrate eye, this jump in complexity can be reduced to a series of small steps that cumulatively describe a gradual transition between the two levels. We use phylogenetic reconstructions of ancestral character states to trace the evolution of steps involved in this transition in volvocine algae. The history of these characters includes several well-supported instances of multiple origins and reversals. The inferred changes can be understood as components of cooperation–conflict–conflict mediation cycles as predicted by multilevel selection theory. One such cycle may have taken place early in volvocine evolution, leading to the highly integrated colonies seen in extant volvocine algae. A second cycle, in which the defection of somatic cells must be prevented, may still be in progress.     

Algal genomics: exploring the imprint of endosymbiosis

The nuclear genomes of photosynthetic eukaryotes are littered with genes derived from the cyanobacterial progenitor of modern-day plastids. A genomic analysis of Cyanophora paradoxa - a deeply diverged unicellular alga - suggests that the abundance and functional diversity of nucleus-encoded genes of cyanobacterial origin differs in plants and algae.     

Interaction, functional relations and evolution of large and small subunits in Rubisco from prokaryota and eukaryota

In early biological evolution anoxygenic photosynthetic bacteria may have been established through the acquisition of ribulose bisphosphate carboxylase-oxygenase (Rubisco). The establishment of cyanobacteria may have followed and led to the production of atmospheric oxygen. It has been postulated that a unicellular cyanobacterium evolved to cyanelles which were evolutionary precursors of chloroplasts of both green and non-green algae. The latter probably diverged from ancestors of green algae as evidenced by the occurrence of large (L) and small (S) subunit genes for Rubisco in the chloroplast genome of the chromophytic algae Olisthodiscus luteus. In contrast, the gene for the S subunit was integrated into the nucleus in the evolution of green algae and higher plants. The evolutionary advantages of this integration are uncertain because the function of S subunits is unknown. Recently, two forms of Rubisco (L8 and L8S8) of almost equivalent carboxylase and oxygenase activity have been isolated from the photosynthetic bacterium Chromatium vinosum. This observation perpetuates the enigma of S subunit function. Current breakthroughs are imminent, however, in our understanding of the function of catalytic L subunits because of the application of deoxyoligonucleotide-directed mutagenesis. Especially interesting mutated Rubisco molecules may have either enhanced carboxylase activity or higher carboxylase:oxygenase ratios. Tests of expression, however, must await the insertion of modified genes into the nucleus and chloroplasts. Methodology to accomplish chloroplast transformation is as yet unavailable. Recently, we have obtained the first transformation of cyanobacteria by a colE1 plasmid. We regard this transformation as an appropriate model for chloroplast transformation.     

Chloroplast-mitochondria cross-talk in diatoms

Diatoms are unicellular, mainly photosynthetic, eukaryotes living within elaborate silicified cell walls and believed to be responsible for around 40% of global primary productivity in the oceans. Their abundance in aquatic ecosystems is such that they have on different occasions been described as the insects, the weeds, or the cancer cells of the ocean. In contrast to higher plants and green algae which derive from a primary endosymbiosis, diatoms are now believed to originate from a serial secondary endosymbiosis involving both green and red algae and a heterotrophic exosymbiont host. As a consequence of their dynamic evolutionary history, they appear to have red algal-derived chloroplasts empowered largely by green algal proteins, working alongside mitochondria derived from the non-photosynthetic exosymbiont. This review will discuss the evidence for such an unusual assemblage of organelles in diatoms, and will present the evidence implying that it has enabled them with unorthodox metabolisms that may have contributed to their profound ecological success.     

Phylogeny of protozoa deduced from 5S rRNA sequences

Summary The nucleotide sequences of 5S rRNAs from three protozoa,Bresslaua vorax, Euplotes woodruffi andChlamydomonas sp. have been determined and aligned together with the sequences of 12 protozoa species including unicellular green algae already reported by the authors and others. Using this alignment, a phylogenic tree of the 15 species of protozoa has been constructed. The tree suggests that the ancestor for protozoa evolved at an early time of eukaryotic evolution giving two major groups of organisms. One group, which shares a common ancestor with vascular plants, contains a unicellular green flagellate (Chlamydomonas) and unicellular green algae. The other group, which shares a common ancestor with the multicellular animals, includes various flagellated protozoa (includingEuglena), ciliated protozoa and slime molds. Most of these protozoa appear to have separated from one another at a fairly early period of eukaryotic evolution.     

Twenty-fold difference in evolutionary rates between the mitochondrial and plastid genomes of species with secondary red plastids

Within plastid-bearing species, the relative rates of evolution between mitochondrial and plastid genomes are poorly studied, but for the few lineages in which they have been explored, including land plants and green algae, the mitochondrial DNA mutation rate is nearly always estimated to be lower than or equal to that of the plastid DNA. Here, we show that in protists from three distinct lineages with secondary, red algal-derived plastids, the opposite is true: their mitochondrial genomes are evolving 5-30 times faster than their plastid genomes, even when the plastid is nonphotosynthetic. These findings have implications for understanding the origins and evolution of organelle genome architecture and the genes they encode.     

Charophyte algae and land plant origins

The charophyte algae are six distinct groups of mostly freshwater green algae that are related to modern land plants. Charophyte algae exhibit diverse morphologies and reproductive strategies, from unicells to branching erect forms, and from swimming asexual spores to sex involving eggs and sperm, respectively. The green algae known as stoneworts (Charales) are suggested to be the extant sister group to all land plants, although the phylogeny is not conclusive. Here we review recent molecular phylogenetic work on the charophyte algae and its implications for our understanding of the origins of land plants and of characters in their aquatic ancestors that might have played a role in the explosive diversification of plants on land.     

Evolution of photoprotection mechanisms upon land colonization: evidence of PSBS‐dependent NPQ in late Streptophyte algae

Light is the energy source for photosynthetic organisms but, if absorbed in excess, it can drive to the formation of reactive oxygen species and photoinhibition. One major mechanism to avoid oxidative damage in plants and algae is the dissipation of excess excitation energy as heat, called non‐photochemical quenching (NPQ). Eukaryotic algae and plants, however, rely on two different proteins for NPQ activation, the former mainly depending on LHCSR (Lhc‐like protein Stress Related; previously called Li818, Light Induced protein 818), whereas in the latter the major role is played by a distinct protein, PSBS (photosystem II subunit S). In the moss Physcomitrella patens, which diverged from vascular plants early after land colonization, both these proteins were found to be present and active in inducing NPQ, suggesting that during plants evolution both mechanisms co‐existed. In order to investigate in more detail NPQ adaptation toward land colonization, we analyzed Streptophyte algae, the latest organisms to diverge from the land plants ancestors. Among them we found evidence of a PSBS‐dependent NPQ in species belonging to Charales, Coleochaetales and Zygnematales, the latest groups to diverge from land plants ancestors. On the contrary earlier diverging algae, as Mesostigmatales and Klebsormidiales, likely rely on LHCSR for their NPQ activation. Presented evidence thus suggests that PSBS‐dependent NPQ, although possibly present in some Chlorophyta, was stably acquired in the Cambrian period about 500 million years ago, before late Streptophyte algae diverged from plants ancestors.