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Green plants (Viridiplantae) include around 450,000–500,000 species 1 , 2 of great diversity and have important roles in terrestrial and aquatic ecosystems. Here, as part of the One Thousand Plant Transcriptomes Initiative, we sequenced the vegetative transcriptomes of 1,124 species that span the diversity of plants in a broad sense (Archaeplastida), including green plants (Viridiplantae), glaucophytes (Glaucophyta) and red algae (Rhodophyta). Our analysis provides a robust phylogenomic framework for examining the evolution of green plants. Most inferred species relationships are well supported across multiple species tree and supermatrix analyses, but discordance among plastid and nuclear gene trees at a few important nodes highlights the complexity of plant genome evolution, including polyploidy, periods of rapid speciation, and extinction. Incomplete sorting of ancestral variation, polyploidization and massive expansions of gene families punctuate the evolutionary history of green plants. Notably, we find that large expansions of gene families preceded the origins of green plants, land plants and vascular plants, whereas whole-genome duplications are inferred to have occurred repeatedly throughout the evolution of flowering plants and ferns. The increasing availability of high-quality plant genome sequences and advances in functional genomics are enabling research on genome evolution across the green tree of life. The One Thousand Plant Transcriptomes Initiative provides a robust phylogenomic framework for examining green plant evolution that comprises the transcriptomes and genomes of diverse species of green plants.

The early evolutionary history of the chloroplast lineage remains an open question. It is widely accepted that the endosymbiosis that established the chloroplast lineage in eukaryotes can be traced back to a single event, in which a cyanobacterium was incorporated into a protistan host. It is still unclear, however, which Cyanobacteria are most closely related to the chloroplast, when the plastid lineage first evolved, and in what habitats this endosymbiotic event occurred. We present phylogenomic and molecular clock analyses, including data from cyanobacterial and chloroplast genomes using a Bayesian approach, with the aim of estimating the age for the primary endosymbiotic event, the ages of crown groups for photosynthetic eukaryotes, and the independent incorporation of a cyanobacterial endosymbiont by Paulinella. Our analyses include both broad taxon sampling (119 taxa) and 18 fossil calibrations across all Cyanobacteria and photosynthetic eukaryotes. Phylogenomic analyses support the hypothesis that the chloroplast lineage diverged from its closet relative Gloeomargarita, a basal cyanobacterial lineage, ∼2.1 billion y ago (Bya). Our analyses suggest that the Archaeplastida, consisting of glaucophytes, red algae, green algae, and land plants, share a common ancestor that lived ∼1.9 Bya. Whereas crown group Rhodophyta evolved in the Mesoproterozoic Era (1,600–1,000 Mya), crown groups Chlorophyta and Streptophyta began to radiate early in the Neoproterozoic (1,000–542 Mya). Stochastic mapping analyses indicate that the first endosymbiotic event occurred in low-salinity environments. Both red and green algae colonized marine environments early in their histories, with prasinophyte green phytoplankton diversifying 850–650 Mya.

Steroid biomarkers provide evidence for a rapid rise of marine planktonic algae between 659 and 645 million years ago, establishing more efficient energy transfers and driving ecosystems towards larger and increasingly complex organisms. When algae bloomed The sudden appearance of complex animals in the Cambrian period puzzled Darwin. He regarded it as one of the most important problems to beset his theory of evolution by natural selection. Here, Jochen Brocks and colleagues show that the Cambrian 'explosion' was preceded by a 'rise of algae' during an interval in which the world may have been largely frozen over. Various steroids preserved in sediments are distinctive markers of eukaryotes, but steroids typical of algae only abound for a short interval in the Cryogenian period between the Sturtian (720–660 Ma) and Marinoan (650–635 Ma) glaciations. In this relatively short, warm interval, phosphorus released by Sturtian weathering allowed eukaryotes to flourish. This broke the stranglehold on Earth's ecology by cyanobacteria, which can get by in lower phosphorus concentrations. This 'rise of algae' created shorter, more efficient food webs, driving an escalatory race towards larger and increasingly complex organisms and the rise of animals. The transition from dominant bacterial to eukaryotic marine primary productivity was one of the most profound ecological revolutions in the Earth’s history, reorganizing the distribution of carbon and nutrients in the water column and increasing energy flow to higher trophic levels. But the causes and geological timing of this transition, as well as possible links with rising atmospheric oxygen levels 1 and the evolution of animals 2 , remain obscure. Here we present a molecular fossil record of eukaryotic steroids demonstrating that bacteria were the only notable primary producers in the oceans before the Cryogenian period (720–635 million years ago). Increasing steroid diversity and abundance marks the rapid rise of marine planktonic algae (Archaeplastida) in the narrow time interval between the Sturtian and Marinoan ‘snowball Earth’ glaciations, 659–645 million years ago. We propose that the incumbency of cyanobacteria was broken by a surge of nutrients supplied by the Sturtian deglaciation 3 . The ‘Rise of Algae’ created food webs with more efficient nutrient and energy transfers 4 , driving ecosystems towards larger and increasingly complex organisms. This effect is recorded by the concomitant appearance of biomarkers for sponges 5 and predatory rhizarians, and the subsequent radiation of eumetazoans in the Ediacaran period 2 .

Canonical plant phytochromes are master regulators of photomorphogenesis and the shade avoidance response. They are also part of a widespread superfamily of photoreceptors with diverse spectral and biochemical properties. Plant phytochromes belong to a clade including other phytochromes from glaucophyte, prasinophyte, and streptophyte algae (all members of the Archaeplastida) and those from cryptophyte algae. This is consistent with recent analyses supporting the existence of an AC (Archaeplastida + Cryptista) clade. AC phytochromes have been proposed to arise from ancestral cyanobacterial genes via endosymbiotic gene transfer (EGT), but most recent studies instead support multiple horizontal gene transfer (HGT) events to generate extant eukaryotic phytochromes. In principle, this scenario would be compared to the emerging understanding of early events in eukaryotic evolution to generate a coherent picture. Unfortunately, there is currently a major discrepancy between the evolution of phytochromes and the evolution of eukaryotes; phytochrome evolution is thus not a solved problem. We therefore examine phytochrome evolution in a broader context. Within this context, we can identify three important themes in phytochrome evolution: deletion, duplication, and diversification. These themes drive phytochrome evolution as organisms evolve in response to environmental challenges.

Plastids evolved from a cyanobacterium that was engulfed by a heterotrophic eukaryotic host and became a stable organelle. Some of the resulting eukaryotic algae entered into a number of secondary endosymbioses with diverse eukaryotic hosts. These events had major consequences on the evolution and diversification of life on Earth. Although almost all plastid diversity derives from a single endosymbiotic event, the analysis of nuclear genomes of plastid-bearing lineages has revealed a mosaic origin of plastid-related genes. In addition to cyanobacterial genes, plastids recruited for their functioning eukaryotic proteins encoded by the host nucleus and also bacterial proteins of noncyanobacterial origin. Therefore, plastid proteins and plastid-localised metabolic pathways evolved by tinkering and using gene toolkits from different sources. This mixed heritage seems especially complex in secondary algae containing green plastids, the acquisition of which appears to have been facilitated by many previous acquisitions of red algal genes (the ‘red carpet hypothesis’).

Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria, which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically, or heterotrophically, and is being developed as an industrial source of vitamins and pigments because of its high biomass productivity. Here, we show that Galdieria exhibits a sexual life cycle, alternating between cell-walled diploid and cell wall–less haploid, and that both phases can proliferate asexually. The haploid can move over surfaces and undergo self-diploidization or generate heterozygous diploids through mating. Further, we prepared the whole genome and a comparative transcriptome dataset between the diploid and haploid and developed genetic tools for the stable gene expression, gene disruption, and selectable marker recycling system using the cell wall–less haploid. The BELL/KNOX and MADS-box transcription factors, which function in haploid-to-diploid transition and development in plants, are specifically expressed in the haploid and diploid, respectively, and are involved in the haploid-todiploid transition in Galdieria, providing information on the missing link of the sexual life cycle evolution in Archaeplastida. Four actin genes are differently involved in motility of the haploid and cytokinesis in the diploid, both of which are myosin independent and likely reflect ancestral roles of actin. We have also generated photosynthesis-deficient mutants, such as blue-colored cells, which were depleted in chlorophyll and carotenoids, for industrial pigment production. These features of Galdieria facilitate the understanding of the evolution of algae and plants and the industrial use of microalgae.

The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in members of the eukaryotic supergroup Archaeplastida. All known archaeplastids still retain some form of primary plastids, which are widely assumed to have a single origin. Here, we use single-cell genomics from natural samples combined with phylogenomics to infer the evolutionary origin of the phylum Picozoa, a globally distributed but seemingly rare group of marine microbial heterotrophic eukaryotes. Strikingly, the analysis of 43 single-cell genomes shows that Picozoa belong to Archaeplastida, specifically related to red algae and the phagotrophic rhodelphids. These picozoan genomes support the hypothesis that Picozoa lack a plastid, and further reveal no evidence of an early cryptic endosymbiosis with cyanobacteria. These findings change our understanding of plastid evolution as they either represent the first complete plastid loss in a free-living taxon, or indicate that red algae and rhodelphids obtained their plastids independently of other archaeplastids. The origin of primary plastids in an ancestor of Archaeplastida gave eukaryotes photosynthetic capabilities. This study used single-cell genomics and phylogenomics to infer the evolutionary origin of the plastid-lacking phylum Picozoa, a group of marine microbial heterotrophic eukaryotes, showing that they belong to the Archaeplastida and changing our understanding of plastid evolution.

Background Complex multicellularity requires elaborate developmental mechanisms, often based on the versatility of heterodimeric transcription factor (TF) interactions. Homeobox TFs in the TALE superclass are deeply embedded in the gene regulatory networks that orchestrate embryogenesis. Knotted-like homeobox (KNOX) TFs, homologous to animal MEIS, have been found to drive the haploid-to-diploid transition in both unicellular green algae and land plants via heterodimerization with other TALE superclass TFs, demonstrating remarkable functional conservation of a developmental TF across lineages that diverged one billion years ago. Here, we sought to delineate whether TALE-TALE heterodimerization is ancestral to eukaryotes. Results We analyzed TALE endowment in the algal radiations of Archaeplastida, ancestral to land plants. Homeodomain phylogeny and bioinformatics analysis partitioned TALEs into two broad groups, KNOX and non-KNOX. Each group shares previously defined heterodimerization domains, plant KNOX-homology in the KNOX group and animal PBC-homology in the non-KNOX group, indicating their deep ancestry. Protein-protein interaction experiments showed that the TALEs in the two groups all participated in heterodimerization. Conclusions Our study indicates that the TF dyads consisting of KNOX/MEIS and PBC-containing TALEs must have evolved early in eukaryotic evolution. Based on our results, we hypothesize that in early eukaryotes, the TALE heterodimeric configuration provided transcription-on switches via dimerization-dependent subcellular localization, ensuring execution of the haploid-to-diploid transition only when the gamete fusion is correctly executed between appropriate partner gametes. The TALE switch then diversified in the several lineages that engage in a complex multicellular organization.

Photorespiration and oxygenic photosynthesis are intimately linked processes. It has been shown that under the present day atmospheric conditions cyanobacteria and all eukaryotic phototrophs need functional photorespiration to grow autotrophically. The question arises as to when this essential partnership evolved, i.e. can we assume a coevolution of both processes from the beginning or did photorespiration evolve later to compensate for the generation of 2-phosphoglycolate (2PG) due to Rubisco’s oxygenase reaction? This question is mainly discussed here using phylogenetic analysis of proteins involved in the 2PG metabolism and the acquisition of different carbon concentrating mechanisms (CCMs). The phylogenies revealed that the enzymes involved in the photorespiration of vascular plants have diverse origins, with some proteins acquired from cyanobacteria as ancestors of the chloroplasts and others from heterotrophic bacteria as ancestors of mitochondria in the plant cell. Only phosphoglycolate phosphatase was found to originate from Archaea. Notably glaucophyte algae, the earliest branching lineage of Archaeplastida, contain more photorespiratory enzymes of cyanobacterial origin than other algal lineages or land plants indicating a larger initial contribution of cyanobacterial-derived proteins to eukaryotic photorespiration. The acquisition of CCMs is discussed as a proxy for assessing the timing of periods when photorespiratory activity may have been enhanced. The existence of CCMs also had marked influence on the structure and function of photorespiration. Here, we discuss evidence for an early and continuous coevolution of photorespiration, CCMs and photosynthesis starting from cyanobacteria via algae, to land plants.

The PII superfamily consists of signal transduction proteins found in all domains of life. Canonical PII proteins sense the cellular energy state through the competitive binding of ATP and ADP, and carbon/nitrogen balance through 2-oxoglutarate binding. The ancestor of Archaeplastida inherited its PII signal transduction protein from an ancestral cyanobacterial endosymbiont. Over the course of evolution, plant PII proteins acquired a glutamine-sensing C-terminal extension, subsequently present in all Chloroplastida PII proteins. The PII proteins of various algal strains (red, green and nonphotosynthetic algae) have been systematically investigated with respect to their sensory and regulatory properties. Comparisons of the PII proteins from different phyla of oxygenic phototrophs (cyanobacteria, red algae, Chlorophyta and higher plants) have yielded insights into their evolutionary conservation vs adaptive properties. The highly conserved role of the controlling enzyme of arginine biosynthesis, N-acetyl-L-glutamate kinase (NAGK), as a main PII-interactor has been demonstrated across oxygenic phototrophs of cyanobacteria and Archaeplastida. In addition, the PII signalling system of red algae has been identified as an evolutionary intermediate between that of Cyanobacteria and Chloroplastida. In this review, we consider recent advances in understanding metabolic signalling by PII proteins of the plant kingdom.