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How Plants Conquered Land

2020; Cell Press; Volume: 181; Issue: 5 Linguagem: Inglês

10.1016/j.cell.2020.05.011

1097-4172

Stefan A. Rensing,

Plant Taxonomy and Phylogenetics

Approximately 500 Ma ago, freshwater algae adapted to live on Earth's surface, subsequently enabling animal life to pursue. Over the last decade, genomes of non-seed plants enabled us to infer trait evolution of early land plants. In this issue of Cell, Jiao et al. uncovered another genome, of the streptophyte algae Penium, enhancing our understanding of the water-to-land transition. Approximately 500 Ma ago, freshwater algae adapted to live on Earth's surface, subsequently enabling animal life to pursue. Over the last decade, genomes of non-seed plants enabled us to infer trait evolution of early land plants. In this issue of Cell, Jiao et al. uncovered another genome, of the streptophyte algae Penium, enhancing our understanding of the water-to-land transition. The green plants (Viridiplantae) live in very diverse habitats such as seawater, freshwater, soil, rock, and snow. They encompass organisms of very different anatomy, such as single-cell algae (e.g., the model organism Chlamydomonas), multicellular green seaweeds such as Ulva (sea lettuce), morphologically complex freshwater algae such as Chara, mosses such as the small-in-stature evo-devo model organism P. patens, and giant trees such as the iconic sequoia. Traits such as multicellularity or the adaptation to diverse habitats evolved several times within the green plants. However, the transition to the terrestrial habitat that eventually led to the stunning diversity of land plants (Embryophyta) most likely occurred only once. The Zygnematophyceae (conjugating algae) are the sister lineage to the land plants (One Thousand Plant Transcriptomes Initiative, 2019One Thousand Plant Transcriptomes InitiativeOne thousand plant transcriptomes and the phylogenomics of green plants.Nature. 2019; 574: 679-685Crossref PubMed Scopus (317) Google Scholar) and thus are of key importance to determine how molecular adaptation of plant life to land occurred. The genome of one of these algae (Penium) is published in this issue of Cell (Jiao et al., 2020Jiao C. Sørensen I. Sun X. Sun H. Behar H. Alseekh S. Philippe G. Lopez K.P. Sun L. Reed R. et al.The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants.Cell. 2020; 181 (this issue): 1097-1111Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar) and shows that carbohydrate-active enzymes (CAZymes) are expanded in this species, probably involved in the generation of mucilage that acts as a protective sheet against drought, one of the prime abiotic stress factors that land plants have to cope with. The Zygnematales belong to the Zygnematophyceae and are filamentous algae with peculiar properties. Their elaborately structured plastids have been subject of study in countless courses around the world, e.g., Mougeotia with its plate-shaped plastid exhibiting light-stimulated movement and Spirogyra with its iconic spiral-shaped plastid, name-inspiring of at least two bands. The Zygnematales went through evolutionary reduction of morphological features; for example, they secondarily lost flagellated sperm and sexually reproduce via conjugation, a process involving the fusion of male and female cells via bridges formed between filaments. Inference of the ancestral traits that the most recent common ancestor (MRCA) of land plants and Zygnematophyceae possessed thus needs to take into account the different evolutionary trajectories that the lineages went through over the past ca. 550 Ma. Interestingly, Jiao et al., 2020Jiao C. Sørensen I. Sun X. Sun H. Behar H. Alseekh S. Philippe G. Lopez K.P. Sun L. Reed R. et al.The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants.Cell. 2020; 181 (this issue): 1097-1111Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar find that desiccation, but not other abiotic stresses, lead to differential expression of transcription factors (TFs) of the GRAS and DREB families that are expanded in Penium. Recent sequencing of two other subaerial Zygnematophyceae genomes found that GRAS genes might have been horizontally transferred into the ancestral algal genome from bacteria (Cheng et al., 2019Cheng S. Xian W. Fu Y. Marin B. Keller J. Wu T. Sun W. Li X. Xu Y. Zhang Y. et al.Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution.Cell. 2019; 179: 1057-1067.e14Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar). The ability to resist drought (the absence of an ambient water supply) is a hallmark of land plants. The successful conquest of the terrestrial habitat required the molecular adaptation to drought. Given that key features of this particular abiotic stress resistance most likely evolved in the MRCA of Zygnematophyceae and Embryophyta, they might be considered "Anydrophyta" (Figure 1), i.e., plants that can cope without water. Genomes for five of the six lineages of streptophyte algae have been published in the past few years (Figure 1). Besides the namesake "twisted" appearance of the sperm cells, the MRCA of Streptophyta already featured a phytochrome (red-light sensor) and a plant-like cell wall and was on its way to adapting to subaerial/terrestrial habitats (Wang et al., 2020Wang S. Li L. Li H. Sahu S.K. Wang H. Xu Y. Xian W. Song B. Liang H. Cheng S. et al.Genomes of early-diverging streptophyte algae shed light on plant terrestrialization.Nat. Plants. 2020; 6: 95-106Crossref PubMed Scopus (51) Google Scholar). The comparative analyses of streptophyte algae genomes suggest that on the trajectory toward Anydrophyta phytohormone biosynthesis and signaling gradually evolved into what is known in extant land plants (Nishiyama et al., 2018Nishiyama T. Sakayama H. 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: 448-464.24Abstract Full Text Full Text PDF PubMed Scopus (166) Google Scholar). For example, some parts of the biosynthesis and signaling toolkit of abscisic acid (ABA), a key phytohormone involved in abiotic stress signaling, are present in most streptophyte algae, but a "canonical" (plant-like) ABA receptor of the PYRABACTIN RESISTANCE (PYR/PYL/RCAR) family can only be detected in Anydrophyta (de Vries et al., 2018de Vries J. Curtis B.A. Gould S.B. Archibald J.M. Embryophyte stress signaling evolved in the algal progenitors of land plants.Proc. Natl. Acad. Sci. USA. 2018; 115: E3471-E3480Crossref PubMed Scopus (57) Google Scholar). Similarly, components of the auxin synthesis and signaling pathway are evolutionarily old, whereas the auxin repressors Aux/IAA of, e.g., Chara are part of a clade of non-canonical proteins (lacking domains I and II). The Penium proteins are part of the clade that includes land plant (canonical) Aux/IAAs, and the same is true for plant-like A/B type auxin response factor (ARF) TFs (Jiao et al., 2020Jiao C. Sørensen I. Sun X. Sun H. Behar H. Alseekh S. Philippe G. Lopez K.P. Sun L. Reed R. et al.The Penium margaritaceum Genome: Hallmarks of the Origins of Land Plants.Cell. 2020; 181 (this issue): 1097-1111Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar). That the other two published Zygnematales genomes lack the genes encoding Aux/IAA underlines the need to further sample species diversity among streptophyte algae and non-seed plants in order to truly understand plant evolution. This argument is further reinforced by evidence for a whole genome duplication (WGD) event in Spirogloea (Cheng et al., 2019Cheng S. Xian W. Fu Y. Marin B. Keller J. Wu T. Sun W. Li X. Xu Y. Zhang Y. et al.Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution.Cell. 2019; 179: 1057-1067.e14Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar) but not in Mesotaenium, Penium, or any other studied streptophyte alga. This is significant because the propensity for WGD, considered to provide an evolutionary playground for sub- and neofunctionalization of the resulting paralogs, is a hallmark of land plants. TF genes are often retained after WGD, and the expanded Penium GRAS family might have resulted from such an event. There are many ways in which the GRAS genes might be linked to the evolutionary success of the Anydrophyta. Not only are they linked to stress responses but they co-occur in species that mutualistically interact with arbuscular mycorrhiza fungi (AMF). Loss of symbiotic status, as well as secondary adaptation to aquatic habitats, coincides with loss of GRAS genes (Cheng et al., 2019Cheng S. Xian W. Fu Y. Marin B. Keller J. Wu T. Sun W. Li X. Xu Y. Zhang Y. et al.Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution.Cell. 2019; 179: 1057-1067.e14Abstract Full Text Full Text PDF PubMed Scopus (97) Google Scholar). After the water-to-land transition, plants evolved a subfamily of GRAS proteins harboring a DELLA domain. Acting initially as transcriptional co-activators, DELLA proteins evolved as interactors of the gibberellic acid (another phytohormone) receptor GID1 in vascular plants (Hernández-García et al., 2019Hernández-García J. Briones-Moreno A. Dumas R. Blázquez M.A. Origin of Gibberellin-Dependent Transcriptional Regulation by Molecular Exploitation of a Transactivation Domain in DELLA Proteins.Mol. Biol. Evol. 2019; 36: 908-918Crossref PubMed Scopus (15) Google Scholar). Many species of Streptophyta follow the trend that the number of TFs encoded by their genome correlates with their morphological complexity, especially given that many of these TFs evolved in the streptophyte algae (Wilhelmsson et al., 2017Wilhelmsson P.K.I. Mühlich C. Ullrich K.K. Rensing S.A. Comprehensive Genome-Wide Classification Reveals That Many Plant-Specific Transcription Factors Evolved in Streptophyte Algae.Genome Biol. Evol. 2017; 9: 3384-3397Crossref PubMed Scopus (45) Google Scholar). However, there are exceptions, like the high number of TFs in Penium (potentially because of the WGD and expansion of a few families) or the low numbers in bryophytes Marchantia and Anthoceros, that probably went through a secondary evolutionary reduction (Puttick et al., 2018Puttick M.N. Morris J.L. Williams T.A. Cox C.J. Edwards D. Kenrick P. Pressel S. Wellman C.H. Schneider H. Pisani D. et al.The Interrelationships of Land Plants and the Nature of the Ancestral Embryophyte.Curr Biol. 2018; 28: 733-745.e2Abstract Full Text Full Text PDF PubMed Scopus (161) Google Scholar, Li et al., 2020Li F.W. Nishiyama T. Waller M. Frangedakis E. Keller J. Li Z. Fernandez-Pozo N. Barker M.S. Bennett T. Blázquez M.A. et al.Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts.Nat. Plants. 2020; 6: 259-272Crossref PubMed Scopus (45) Google Scholar). The Anthoceros (hornwort) genomes are one of the most recent additions to the repository of non-seed plant genomes (Figure 1) and show secondary loss of TFs, such as KNOX1, but also the presence of YABBY TF—suggesting that the land plant MRCA already possessed YABBY, which has since been lost in the other bryophyte lineages, so far represented mainly by Marchantia and Physcomitrella (Li et al., 2020Li F.W. Nishiyama T. Waller M. Frangedakis E. Keller J. Li Z. Fernandez-Pozo N. Barker M.S. Bennett T. Blázquez M.A. et al.Anthoceros genomes illuminate the origin of land plants and the unique biology of hornworts.Nat. Plants. 2020; 6: 259-272Crossref PubMed Scopus (45) Google Scholar). Extended species sampling of these interesting organisms will further inform our understanding of plant evolution. I am deeply grateful to all the great recent work enabling insights into the early evolution of plants—and very sorry that I could not cite all papers. Thank you, Debbie Maizels, for drawing a great figure again. The Penium margaritaceum Genome: Hallmarks of the Origins of Land PlantsJiao et al.CellMay 21, 2020In BriefThe genome sequence of Penium margaritaceum reveals that this freshwater algal species and member of the sister lineage to land plants contains several advantageous features for life on land, including an expanded repertoire of genes for cell wall biosynthesis, traces of pathways to form hydrophobic polymer classes that limit water loss, and flavonoid pigments that protect against UV radiation. Full-Text PDF Open Archive