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PP62CH23-Popper ARI 4 April 2011 14:20 Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants Zoe¨ A. Popper,1 Gurvan Michel,3,4 Cecile´ Herve,´ 3,4 David S. Domozych,5 William G.T. Willats,6 Maria G. Tuohy,2 Bernard Kloareg,3,4 and Dagmar B. Stengel1 1Botany and Plant Science, and 2Molecular Glycotechnology Group, Biochemistry, School of Natural Sciences, National University of Ireland, Galway, Ireland; email: [email protected] 3CNRS and 4UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Bretagne, France 5Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 6Department of Plant Biology and Biochemistry, Faculty of Life Sciences, University of Copenhagen, Bulowsvej,¨ 17-1870 Frederiksberg, Denmark Annu. Rev. Plant Biol. 2011. 62:567–90 Keywords First published online as a Review in Advance on xyloglucan, mannan, arabinogalactan proteins, genome, environment, February 22, 2011 multicellularity The Annual Review of Plant Biology is online at plant.annualreviews.org Abstract This article’s doi: All photosynthetic multicellular Eukaryotes, including land plants 10.1146/annurev-arplant-042110-103809 by Universidad Veracruzana on 01/08/14. For personal use only. and algae, have cells that are surrounded by a dynamic, complex, Copyright c 2011 by Annual Reviews. carbohydrate-rich cell wall. The cell wall exerts considerable biologi- All rights reserved cal and biomechanical control over individual cells and organisms, thus Annu. Rev. Plant Biol. 2011.62:567-590. Downloaded from www.annualreviews.org 1543-5008/11/0602-0567$20.00 playing a key role in their environmental interactions. This has resulted in compositional variation that is dependent on developmental stage, cell type, and season. Further variation is evident that has a phylogenetic basis. Plants and algae have a complex phylogenetic history, including acquisition of genes responsible for carbohydrate synthesis and modi- fication through a series of primary (leading to red algae, green algae, and land plants) and secondary (generating brown algae, diatoms, and dinoflagellates) endosymbiotic events. Therefore, organisms that have the shared features of photosynthesis and possession of a cell wall do not form a monophyletic group. Yet they contain some common wall com- ponents that can be explained increasingly by genetic and biochemical evidence. 567 PP62CH23-Popper ARI 4 April 2011 14:20 The land plants, CGA, and chlorophytes Contents represent only part of the Archaeplastida, a monophyletic eukaryotic group that also com- INTRODUCTION.................. 568 prises red and glaucophyte algae (4). As is WALL COMPOSITION OF the case with all plastid-containing Eukary- PLANTS AND ALGAE . 570 otes, the emergence of the Archaeplastida is MULTICELLULARITY linked tightly to their photosynthetic history. ANDBODYPLAN............... 571 The Archaeplastida are thought to have orig- Generation of Multicellularity . 571 inated through a single shared event, primary Differentiation and Cell-Wall endosymbiosis with a cyanobacterium, over Diversity....................... 573 1,500 Mya. The chlorophyll c–containing algae, Cell-Cell Communication . 579 which include brown algae, evolved soon after Unicellularity . 579 through secondary endosymbiosis with a red TERRESTRIALIZATION, alga (95). Two scenarios are suggested for their VASCULARIZATION, AND endosymbiotic history: (a) a single endosymbi- DIVERSIFICATION............. 580 otic event followed by loss of the rhodobionts in AquaticHabitats................... 580 Rhizaria, and subsequent gain of chlorobionts Terrestrialization.................. 581 in the Chlorarchniophyta [the chromalveolate InnateImmunity................... 582 hypothesis (19, 54)], and (b) the increasingly CONCLUSIONS AND KEY more favored scenario in which multiple sec- PROBLEMS . 582 ondary endosymbiotic events occurred (9, 82, 126) (Figure 1). Both the Archaeplastida and brown algae share two distinctive features: the presence of a complex, dynamic, carbohydrate-rich cell wall, INTRODUCTION which, to some extent, is dependent on the Significant progress has been made in the past second feature, the ability to photosynthesize. 40 years in our understanding of the structure, Stebbins (125) suggested the “adaptive impor- synthesis, and function of plant cell walls. Much tance of cell wall differentiation,” and the sig- of the research effort has been directed toward nificance of the cell wall to each lineage is highly Charophycean investigating the cell walls of only a few species, evident: both have independently evolved mul- green algae (CGA, mostly flowering plants (angiosperms) of eco- ticellularity (20) and (along with the wall-less Charophyceae): nomic importance. However, more recently, animals) are among the most extensively re- by Universidad Veracruzana on 01/08/14. For personal use only. a monophyletic potentially driven by the awareness that “small searched, ecologically and economically impor- group comprising pre- modifications in their chemistry can have pro- tant organisms on the planet. Although the two dominantly freshwater Annu. Rev. Plant Biol. 2011.62:567-590. Downloaded from www.annualreviews.org green algae that share found effects on the multifarious functions cell lineages do not form a natural group, and their several features of land walls perform” (88), there has been substan- cell walls have evolved independently (88), it is plants and include the tial interest in the wall biochemistry of early likely that at least some of their wall compo- closest extant ancestors diverging plants and the charophycean green nents have a shared ancestry (103). of land plants algae (CGA) (17, 30, 38, 39, 101, 103, 123, Bioinformatics is beginning to resolve the and their relatives 124, 136). Gaining a complete understanding gene transfers associated with the origin of Archaeplastida: of plant cell-wall evolution might be achieved photosynthetic lineages, in particular those a monophyletic supergroup comprising only by more closely investigating the origins of that occurred during the primary endosym- the Glaucophyta, cell walls. Niklas (88) highlighted that cell walls biotic event that led to the emergence of the Rhodophyta have “deep roots in the tree of life.” Land plants the Archaeplastida. It has been deduced that (red algae), and the evolved from CGA, which conquered freshwa- 18% of the nuclear genes in the Arabidopsis Chloroplastida (green ter habitats after their separation from ancient genome are potentially of cyanobacterial ori- algae and land plants) chlorophyte green algae (10, 69). gin (77). Although cyanobacterial cell walls, 568 Popper et al. PP62CH23-Popper ARI 4 April 2011 14:20 CesA Cyanobacteria CslH,F Poales: grasses CslE,J CslB,G Non-Poalean angiosperms: flowering plants excluding grasses Gymnosperms PE Pteridophytes: ferns, whisk ferns, horsetails Lycopodiophytes: club mosses CslA,C,D Archaeplastida CesA* Bryophytes: mosses, liverworts, hornworts CslA/C Charophyceae CesA Chlorophyta: green algae Rhodophyta: red algae CesA? Glaucophyta: Microalgae with cyanobacteria-like chloroplasts Excavates: includes Excavata photosynthetic Euglenozoa SE2 SE1 Apicomplexa Alveolata Dinoflagellata CesA Oomycetes Diatoms Stramenopiles CesA Phaeophyceae: brown algae Eukaryotes Prokaryotes Rhizaria: includes photosynthetic Rhizaria Chloroarachniophyta Haptophyta Cryptophyceae Animals Opisthokonta Fungi by Universidad Veracruzana on 01/08/14. For personal use only. Amoebozoa Amoebozoa Annu. Rev. Plant Biol. 2011.62:567-590. Downloaded from www.annualreviews.org Key Cellulose Pectins Agars (1–3),(1–4)-β-D-glucan Xyloglucan Carrageenans Lignin and lignin-like Arabinogalactan proteins Fucoidans compounds Ulvans Alginates Figure 1 Simplified Eukaryote phylogeny highlighting the occurrence of major wall components. The identification of specific wall components within lineages (1, 4, 43, 69) is symbolized as shown in the key. Genes responsible for cellulose and hemicellulose biosynthesis (144) are ∗ indicated in boxes: CesA represents members of the cellulose synthase family whose proteins assemble into rosette terminal complexes, CesA is the ancestral form of cellulose synthases, and CslA/C is a single gene that is most similar to the land plant CslA and CslC gene families. The arrows indicate the origin of the plastids: PE (solid arrow), primary endosymbiosis; SE1 (dotted arrow), secondary endosym- biosis scenario 1 in which the Alveolata, Cryptophyceae, Haptophyta, and Stramenopiles originate from a common ancestor, which acquired its plastids by a secondary endosymbiosis event with a red alga (19), which Rhizaria subsequently lost and the Chlorarchniophyta regained (54); SE2 (dashed arrows), secondary endosymbiosis scenario 2, separate acquisitions of rhodobionts (9, 82, 126). www.annualreviews.org • Cell-Wall Evolution of Photosynthetic Organisms 569 PP62CH23-Popper ARI 4 April 2011 14:20 consisting of a peptidoglycan-polysaccharide- and the involvement of the cell wall in these lipopolysaccharide matrix, fundamentally are processes. Algae: unifying term for the collection of different from the polysaccharide-rich cell walls distinct photosynthetic of plants and algae, it has been proposed that lineages that evolved genes present in the primary endosymbiont WALL COMPOSITION independently and can may have provided the basis for plant and algal OF PLANTS AND ALGAE live in terrestrial cell-wall biosynthesis (103). Current
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