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PP62CH23-Popper ARI 4 April 2011 14:20

Evolution and Diversity of

Plant Cell Walls: From Algae

to Flowering Plants

Zo¨e A. Popper,

1

Gurvan Michel,

3,4

C´ecile Herv´e,

3,4

David S. Domozych,

5

William G.T. Willats,

6

Maria G. Tuohy,

2

Bernard Kloareg,

3,4 and Dagmar B. Stengel 1 1

Botany and Plant Science, and

2

Molecular Glycotechnology Group, Biochemistry,

School of Natural Sciences, National University of Ireland, Galway, Ireland; email: zoe.popper@nuigalway.ie 3

CNRS and

4 UPMC University Paris 6, UMR 7139 Marine Plants and Biomolecules, Station Biologique de Roscoff, F-29682 Roscoff, Bretagne, France 5 Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College,

Saratoga Springs, New York 12866

6 Department of Plant Biology and Biochemistry, Faculty of Life Sciences, University of

Copenhagen, B

¨ulowsvej, 17-1870 Frederiksberg, Denmark

Annu. Rev. Plant Biol. 2011. 62:567...90

First published online as a Review in Advance on

February 22, 2011

TheAnnual Review of Plant Biologyis online at

plant.annualreviews.org

This article"s doi:

10.1146/annurev-arplant-042110-103809

Copyright

c∞2011 by Annual Reviews.

All rights reserved

1543-5008/11/0602-0567$20.00

Keywords

xyloglucan, mannan, arabinogalactan proteins, genome, environment, multicellularity

Abstract

All photosynthetic multicellular Eukaryotes, including land plants and algae, have cells that are surrounded by a dynamic, complex, carbohydrate-rich cell wall. The cell wall exerts considerable biologi- cal and biomechanical control over individual cells and organisms, thus playing a key role in their environmental interactions. This has resulted in compositional variation that is dependent on developmental stage, 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 dino"agellates) endosymbiotic events. Therefore, organisms that have form a monophyletic group. Yet they contain some common wall com- ponents that can be explained increasingly by genetic and biochemical evidence.

567Annu. Rev. Plant Biol. 2011.62:567-590. Downloaded from www.annualreviews.orgby Universidad Veracruzana on 01/08/14. For personal use only.

PP62CH23-Popper ARI 4 April 2011 14:20

Charophycean

green algae (CGA,

Charophyceae):

a monophyletic group comprising pre- dominantly freshwater green algae that share several features of land plants and include the closest extant ancestors of land plants and their relatives

Archaeplastida:

a monophyletic supergroupcomprising the Glaucophyta, the Rhodophyta (red algae), and the

Chloroplastida (green

algae and land plants)

Contents

INTRODUCTION.................. 568

WALL COMPOSITION OF

PLANTS AND ALGAE........... 570

MULTICELLULARITY

ANDBODYPLAN............... 571

Generation of Multicellularity...... 571

Differentiation and Cell-Wall

Diversity....................... 573

Cell-Cell Communication.......... 579

Unicellularity...................... 579

TERRESTRIALIZATION,

VASCULARIZATION, AND

DIVERSIFICATION............. 580

AquaticHabitats................... 580

Terrestrialization.................. 581

InnateImmunity................... 582

CONCLUSIONS AND KEY

PROBLEMS ...................... 582

INTRODUCTION

Significant progress has been made in the past

40 years in our understanding of the structure,

of the research effort has been directed toward mostly "owering plants (angiosperms) of eco- nomic importance. However, more recently, potentially driven by the awareness that small modifications in their chemistry can have pro- found effects on the multifarious functions cell walls performŽ (88), there has been substan- tial interest in the wall biochemistry of early diverging plants and the charophycean green algae (CGA) (17, 30, 38, 39, 101, 103, 123,

124, 136). Gaining a complete understanding

of plant cell-wall evolution might be achieved evolved from CGA, which conquered freshwa- ter habitats after their separation from ancient chlorophyte green algae (10, 69).The land plants, CGA, and chlorophytes represent only part of the Archaeplastida, a monophyletic eukaryotic group that also com- prises red and glaucophyte algae (4). As is the case with all plastid-containing Eukary- otes, the emergence of the Archaeplastida is linked tightly to their photosynthetic history.

The Archaeplastida are thought to have orig-

inated through a single shared event, primary endosymbiosis with a cyanobacterium, over which include brown algae, evolved soon after through secondary endosymbiosis with a red alga (95). Two scenarios are suggested for their endosymbiotic history: (a) a single endosymbi-

Rhizaria, and subsequent gain of chlorobionts

in the Chlorarchniophyta [the chromalveolate hypothesis (19, 54)], and (b) the increasingly more favored scenario in which multiple sec- 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, which, to some extent, is dependent on the second feature, the ability to photosynthesize.

Stebbins (125) suggested the adaptive impor-

tance of cell wall differentiation,Ž and the sig- evident: both have independently evolved mul- ticellularity (20) and (along with the wall-less animals) are among the most extensively re- tant organisms on the planet. Although the two lineages do not form a natural group, and their cell walls have evolved independently (88), it is likely that at least some of their wall compo- nents have a shared ancestry (103).

Bioinformatics is beginning to resolve the

gene transfers associated with the origin of photosynthetic lineages, in particular those that occurred during the primary endosym- biotic event that led to the emergence of the Archaeplastida. It has been deduced that

18% of the nuclear genes in theArabidopsis

genome are potentially of cyanobacterial ori- gin (77). Although cyanobacterial cell walls,

568 Popper et al.Annu. Rev. Plant Biol. 2011.62:567-590. Downloaded from www.annualreviews.orgby Universidad Veracruzana on 01/08/14. For personal use only.

PP62CH23-Popper ARI 4 April 2011 14:20

Xyloglucan(1...3),(1...4)--D-glucan

Arabinogalactan proteinsCellulose

Fucoidans

AlginatesPectins Agars

Carrageenans

Lignin and lignin-likecompoundsUlvans

Key

AmoebozoaFungiAnimalsGlaucophyta: Microalgae withcyanobacteria-like chloroplastsRhodophyta: red algaeChlorophyta: green algaeCharophyceaeBryophytes: mosses, liverworts,hornworts Lycopodiophytes: club mossesPteridophytes: ferns,whisk ferns, horsetailsGymnospermsNon-Poalean angiosperms:

owering plants excluding grassesPoales: grasses

Excavates: includesphotosynthetic Euglenozoa

Dino?agellata

Apicomplexa

Oomycetes

Diatoms

Phaeophyceae: brown algae

Rhizaria: includes photosyntheticChloroarachniophyta

Haptophyta

CryptophyceaeCslH,F

CslB,G

CslE,J

CslA,C,D

CesA*

CslA/C

CesA CesA

CesA CesA?CesA Cyanobacteria

Eukaryotes Prokaryotes

PE SE1 SE2

ExcavataArchaeplastida

Alveolata

Stramenopiles

Rhizaria

Opisthokonta

Amoebozoa

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,

CesAis the ancestral form of cellulose synthases, andCslA/Cis 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 plastidsbyasecondaryendosymbiosiseventwith ared alga(19),which Rhizaria subsequentlylostand 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 569Annu. Rev. Plant Biol. 2011.62:567-590. Downloaded from www.annualreviews.orgby Universidad Veracruzana on 01/08/14. For personal use only.

PP62CH23-Popper ARI 4 April 2011 14:20

Algae:unifying term

for the collection of distinct photosynthetic lineages that evolved independently and can live in terrestrial environments, but predominantly inhabit aquatic habitats

Primary

endosymbiosis:the uptake and retention of a cyanobacterium by a heterotrophic eukaryotic cell

Brown algae

(Phaeophyceae): a group containing multicellular algae with chlorophylla/c- containing plastids that emerged ≂200 Mya, through secondary endosymbiosis with a red alga consisting of a peptidoglycan-polysaccharide- lipopolysaccharide matrix, fundamentally are of plants and algae, it has been proposed that genes present in the primary endosymbiont may have provided the basis for plant and algal cell-wall biosynthesis (103). Current genomic evidence indicates that at least 10% of the genome of "owering plants is associated with wall biosynthesis and metabolism (129). This situation likely is mirrored in the algae, thereby evolution.

Intensi"ed research on the cell-wall bio-

chemistry of plants and algae has brought recognition that wall modi"cation has been ex- tensive, enabling adaptation to different evo- lutionary pressures (17, 38, 39, 101, 102, 123,

124, 132, 136), and considerable attention has

focused recently on the evolution of cell-wall components (99, 103, 118, 123). In this review, we discuss several major events in the evolution of plant and algal lineages, including multicel- lularity, terrestrialization, and vascularization,

METHODS FOR INVESTIGATING CELL-WALL

BIODIVERSITY

Detailed analysis of cell-wall components from many species, tissues, and developmental stages is essential to recognize fully their diversity in plants and algae (103, 123). Several key meth- ods commonly employed for wall analyses has been compiled and described (37, 100). Considering the vast number of plant and algal species, high-throughput screening methods, including Comprehensive Microarray Polymer Profiling (CoMPP) (84), OLIigosaccharide Mass Profiling (OLIMP) (91), and Fourier- ther to provide an initial step preceding more extensive charac- terization (103, 123). Immunocytochemistry using monoclonal antibodies and carbohydrate-binding modules (49) is also an ex- components and, combined with specific wall treatments (76) or advanced microscopy such as electron tomography (92) and live- cell imaging (44), additionally can indicate interactions between wall components in their native environment.and the involvement of the cell wall in these processes.

WALL COMPOSITION

OF PLANTS AND ALGAE

Plant and algal cell-wall components are sub-

ject to intense research, not least because they are of high economic value within the paper, food, and fiber industries; have projected fu- ture use for biofuels, nutraceuticals, and phar- maceuticals; and are of ecological importance (88). Thus, a body of expertise facilitating the investigation of wall composition and knowl- ponents has been garnered (see the sidebar

Methods for Investigating Cell-Wall Biodiver-

sity). Although this was centered mostly on crop species of "owering plants and algae (e.g.,

LaminariaandGracilaria), sufficient evidence

was available to suggest that diversity in cell- wall composition between taxa has its foun- dation in the evolution of specific lineages.

Investigators have built on this data in the past

≂10 years, and several reviews give a detailed outline of the occurrence of specific wall com-

99, 103, 123, 124) (Figure 2). We summarize

the major trends seen in the polysaccharides in

Table 1and the genes that control their syn-

thesis inTable 2andFigure 1.Inbrief,the

CGA have cell walls that are closely similar in

compositiontothelandplants(Table2),which descendedfromthem,andthusappeartobeata pivotal position in wall evolution, making them ideal models for land-plant cell-wall research [see the sidebarPenium margaritaceum(Zygne- matophyta) as a Model Organism]. Within this monophyletic group (Figures 3and4), both major and subtle changes in wall composition have occurred and may indicate specific evolu- tionary pressures. However, these changes oc-quotesdbs_dbs23.pdfusesText_29

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