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An Algal Greening of Land

2018; Cell Press; Volume: 174; Issue: 2 Linguagem: Inglês

10.1016/j.cell.2018.06.034

1097-4172

William Martin, John F. Allen,

Polar Research and Ecology

Photosynthetic eukaryotes arose ∼1.5 billion years ago by endosymbiosis with a cyanobacterium. Algae then evolved for a billion years before one lineage finally colonized land. Why the wait? The Chara braunii genome details a decisive step linking plant origins with Earth's history. Photosynthetic eukaryotes arose ∼1.5 billion years ago by endosymbiosis with a cyanobacterium. Algae then evolved for a billion years before one lineage finally colonized land. Why the wait? The Chara braunii genome details a decisive step linking plant origins with Earth's history. In this issue of Cell, Nishiyama et al., 2018Nishiyama T. Hidetoshi S. de Vries J. Buschmann H. Saint-Marcoux D. Ullrich K.K. Haas F.B. Vanderstraeten L. Becker D. Lang D. et al.The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization.Cell. 2018; 174 (this issue): 448-464Abstract Full Text Full Text PDF PubMed Scopus (255) Google Scholar present the genome of Chara braunii, a simple freshwater alga that enriches our understanding of life's eventual conquest of land. The fossil record tells us that the first land plants appeared about 450 million years ago (Kenrick et al., 2012Kenrick P. Wellman C.H. Schneider H. Edgecombe G.D. A timeline for terrestrialization: consequences for the carbon cycle in the Palaeozoic.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012; 367: 519-536Crossref PubMed Scopus (191) Google Scholar). Before life on land, all photosynthesis took place in aquatic environments, either marine or freshwater. In order to go ashore, plants had to obtain the tools necessary for life in thin air. Adaptation involves expressing suites of evolutionary innovations that arise blindly through mutation but prove useful (selectable) in new environments—provided they are expressed at the right time. For instance, photosynthetic tissue in air required stomatopores that opened to allow in atmospheric CO2 but also closed to limit water loss by evaporation. The Chara genome is rich with information about the evolutionary inventions that enabled life on land. Chara does not represent the first lineage of land plants; it represents their precursors, the lineages of freshwater algae from which land plants emerged (Delwiche and Cooper, 2015Delwiche C.F. Cooper E.D. The evolutionary origin of a terrestrial flora.Curr. Biol. 2015; 25: R899-R910Abstract Full Text Full Text PDF PubMed Scopus (199) Google Scholar) (Figure 1). Plotted onto phylogeny, the Chara genome pinpoints the evolutionary timing of key innovations (Nishiyama et al., 2018Nishiyama T. Hidetoshi S. de Vries J. Buschmann H. Saint-Marcoux D. Ullrich K.K. Haas F.B. Vanderstraeten L. Becker D. Lang D. et al.The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization.Cell. 2018; 174 (this issue): 448-464Abstract Full Text Full Text PDF PubMed Scopus (255) Google Scholar), giving insights into life on Earth's last frontier. Algae faced numerous hurdles as they risked the first steps onto the shoreline. They had to protect themselves against water loss with a cuticle. They had to support their own weight, requiring rigid cell walls with cellulose fibers. They required new tools to master photosynthesis using CO2 from the atmosphere while sensing an environment—life in air—to which their water-borne cousins were oblivious. The algal forebears of land plants also had to establish co-evolutionary links with bacterial and fungal partners for assimilation of nitrogen and phosphorus. Chara sheds light on the origin of environmental signaling via plant hormones and via the plastid. Plants regulate many aspects of organ development, growth timing, and stress response by producing hormones that act individually and in concert to elicit specific molecular, cellular, and organismal responses. The Chara genome uncovers important pieces in the stepwise evolutionary origin of plant signaling by means of auxins, cytokinins, ethylene, and abscisic acid (Nishiyama et al., 2018Nishiyama T. Hidetoshi S. de Vries J. Buschmann H. Saint-Marcoux D. Ullrich K.K. Haas F.B. Vanderstraeten L. Becker D. Lang D. et al.The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization.Cell. 2018; 174 (this issue): 448-464Abstract Full Text Full Text PDF PubMed Scopus (255) Google Scholar). The plastid of a land plant is heavily involved in environmental signaling because it has to integrate light and nutrient inputs for photosynthesis without generating reactive oxygen species (ROS) that cause damage to the cell. Several pathways of both internal plastid and plastid-to-nucleus signaling in plants and algae make cytoplasmic and nuclear transcriptional machinery responsive to environmental change (Puthiyaveetil et al., 2013Puthiyaveetil S. Ibrahim I.M. Allen J.F. Evolutionary rewiring: a modified prokaryotic gene-regulatory pathway in chloroplasts.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013; 368: 20120260Crossref PubMed Scopus (28) Google Scholar). While the Chara chloroplast has only a plastid-encoded RNA polymerase, the Chara nuclear genome encodes a set of components of the plastid-to-nucleus, or "retrograde," signaling pathway found in higher plants. These features, together with hormones for long-distance signaling across cells and organs, reveal steps in the emergence of plant signal transduction. Chara's plastids points to a further, crucial aspect of land plant origin. All green algal ancestors of land plants have only one—usually very large—chloroplast in each cell (de Vries and Gould, 2018de Vries J. Gould S.B. The monoplastidic bottleneck in algae and plant evolution.J. Cell Sci. 2018; 131: jcs203414Crossref PubMed Scopus (33) Google Scholar). Only on land do green plants start to exhibit many plastids per cell. As early land plants faced new challenges in water budget, gas exchange, and waste disposal (vacuoles instead of the medium), plastids became smaller in size and larger in number, increasing plastid surface area for gas and metabolite exchange with the cytosol. The Chara genome highlights reactions involving gasses at the core of plant biology. Photorespiration, for example, is a consequence of O2 competing with CO2 as a substrate for the enzyme Rubisco in the Calvin cycle, thus limiting photosynthetic carbon assimilation. In common with plants but few other algae, Chara has glycollate oxidase and other enzymes of the photorespiratory pathway, reflecting a physiological innovation that could become beneficial, thus selected, at higher oxygen levels. A key cellular trait that maps to the origin of the lineages that include Chara and land plants is the phragmoplast, a structure that becomes the cell wall between daughter cells during mitosis. The phragmoplast underlies multicellularity in the land plant lineage and in Chara, a simpler multicellular form. This trait is coupled with the organization of cellulose synthase complexes into rosettes, which produce the cellulose fibrils we recognize as the tough, fibrous substance of plant cells and wood. The phragmoplast and cellulose synthase rosettes were present in the algal ancestors of land plants and were selected for more intense use during the conquest of land—classical evolutionary innovation. Looking forward, broader lineage sampling will enrich genomic resources for better understanding the algal progenitors of land plants, early land plant lineages, and microbial interactions in the rhizosphere. This knowledge will help uncover how nature solved problems like desiccation tolerance, nutrient acquisition, signaling, light management during photosynthesis, creation of fertile soil, and the physiological interplay between CO2 and O2. Evolutionary insights into how plants naturally adapted as the food chain reached land could impact modern agriculture, particularly where water is scarce. Land plants brought new biomass to Earth—and lots of it. Current estimates have it that land plants comprise 80% of the Earth's current biomass (Bar-On et al., 2018Bar-On Y.M. Phillips R. Milo R. The biomass distribution on Earth.Proc. Natl. Acad. Sci. USA. 2018; (Published online May 21, 2018)https://doi.org/10.1073/pnas.1711842115Crossref PubMed Scopus (1195) Google Scholar), a proportion that may have been reached rapidly soon after plants colonized land, a niche which at first was without competitors. The accumulation of biomass on land had consequences of extraordinary significance for Earth history, a recognition that is only now coming into focus. The story of land plant origin is a story of the oxygen we breathe. When cyanobacteria started producing oxygen 2.5 billion years ago, they did not immediately oxygenate either the atmosphere or the oceans (Fischer et al., 2016Fischer W.W. Hemp J. Johnson J.E. Evolution of oxygenic photosynthesis.Annu. Rev. Earth Planet. Sci. 2016; 44: 647-683Crossref Scopus (233) Google Scholar). It took almost 2 billion years for O2 to begin to reach modern levels. Independent lines of evidence now indicate that the big jump in Earth oxygen levels took place a mere 430 million years ago (Lenton et al., 2016Lenton T.M. Dahl T.W. Daines S.J. Mills B.J.W. Ozaki K. Saltzman M.R. Porada P. Earliest land plants created modern levels of atmospheric oxygen.Proc. Natl. Acad. Sci. USA. 2016; 113: 9704-9709Crossref PubMed Scopus (165) Google Scholar, Stolper and Keller, 2018Stolper D.A. Keller C.B. A record of deep-ocean dissolved O2 from the oxidation state of iron in submarine basalts.Nature. 2018; 553: 323-327Crossref PubMed Scopus (89) Google Scholar) (Figure 1). Early land plants are now implicated as causal agents behind increased O2 levels through a process called carbon burial. The first land plants buried so much carbon that O2 accumulated in the atmosphere to roughly present levels (Lenton et al., 2016Lenton T.M. Dahl T.W. Daines S.J. Mills B.J.W. Ozaki K. Saltzman M.R. Porada P. Earliest land plants created modern levels of atmospheric oxygen.Proc. Natl. Acad. Sci. USA. 2016; 113: 9704-9709Crossref PubMed Scopus (165) Google Scholar). In the bigger picture of Earth history, the late accumulation of O2 helps to explain why Earth's oceans remained anoxic for so long (Stolper and Keller, 2018Stolper D.A. Keller C.B. A record of deep-ocean dissolved O2 from the oxidation state of iron in submarine basalts.Nature. 2018; 553: 323-327Crossref PubMed Scopus (89) Google Scholar). It also explains why all major eukaryotic lineages retained pathways for anaerobic energy metabolism (Müller et al., 2012Müller M. Mentel M. van Hellemond J.J. Henze K. Woehle C. Gould S.B. Yu R.-Y. van der Giezen M. Tielens A.G.M. Martin W.F. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes.Microbiol. Mol. Biol. Rev. 2012; 76: 444-495Crossref PubMed Scopus (500) Google Scholar): land plants and land animals in their wake were the first eukaryotes to adapt to today's high oxygen conditions. The Chara genome helps us to understand how land plants came ashore, how they brought plentiful oxygen to air, and how a few evolutionary innovations can have consequences of planetary scale. The Chara Genome: Secondary Complexity and Implications for Plant TerrestrializationNishiyama et al.CellJuly 12, 2018In BriefThe draft genome of Chara braunii reveals many plant-like features important for colonization of land that evolved in charophytic algae and therefore prior to the earliest land plants. Full-Text PDF Open Archive