Available online at www.sciencedirect.com Evolution and diversity of green plant cell walls Zoe¨ A Popper Plant cells are surrounded by a dynamic cell wall that performs biomass for the emerging biofuel industry. Cell walls have many essential biological roles, including regulation of cell been used as a source of fuel for millennia, for example in expansion, the control of tissue cohesion, ion-exchange and the form of wood, derived from dicotyledonous trees, and defence against microbes. Recent evidence shows that the peat, derived from Sphagnum moss. Algae, while being suite of polysaccharides and wall proteins from which the plant among the most efficient photosynthetic organisms and of cell wall is composed shows variation between monophyletic interest for biofuel generation, will not be specifically plant taxa. This is likely to have been generated during the discussed within this review because their greatest poten- evolution of plant groups in response to environmental stress. tial is as a source of oils (localised in the vacuole) for use in Understanding the natural variation and diversity that exists bio-diesel production, rather than cell wall biomass. This between cell walls from different taxa is key to facilitating their review will focus on the natural variation and diversity future exploitation and manipulation, for example by increasing that exists within land plant cell wall composition that is lignocellulosic content or reducing its recalcitrance for use in associated with land plant phylogeny (Table 1). biofuel generation. Address A more comprehensive investigation of diverse land plant Department of Botany, National University of Ireland Galway, Ireland cell walls not only is essential to facilitate wall modifi- cation enabling production of biomass with improved Corresponding author: Popper, Zoe¨ A([email protected]) qualities, for example an increased cellulose concen- tration; but may also suggest the potential of novel crop Current Opinion in Plant Biology 2008, 11:286–292 plants. This review comes from a themed issue on Types of cell wall Physiology and metabolism Edited by Ken Keegstra and Markus Pauly Cells walls are composed of three types of layers: the middle lamella, the primary cell wall and the secondary Available online 10th April 2008 cell wall. The middle lamella is deposited soon after mitosis creating a boundary between the two daughter 1369-5266/$ – see front matter # 2008 Elsevier Ltd. All rights reserved. nuclei and, once the cell plate is complete, the primary cell wall is deposited and continues to be deposited DOI 10.1016/j.pbi.2008.02.012 throughout cell growth and expansion. Therefore, although the primary cell wall is typically only 0.1– 10 mm thick, its composition is of importance for biomass Introduction accumulation through controlling cell growth. Cellulose-rich cell walls, one of the defining character- istics of plants, are of fundamental importance for normal The secondary cell wall is deposited internally to the plant growth and development. Despite recognition that primary cell wall at the onset of differentiation, once cell distinct differences exist in wall chemistry between growth has ceased. However, secondary cell walls are not Angiosperm taxa [1,2], the main focus of cell wall research present in all cell types, parenchyma and collenchyma has been on Angiosperm, primarily crop, species. frequently have only a primary cell wall, or in all plant Recently, however, there has been increasing interest taxa. In spermatophytes, secondary cell wall composition in the cell wall biochemistry of non-Angiosperm plants is known to vary from one cell type and reflects cell [3,4,5–8,9,10–14], and evidence has emerged to sup- function. For example, many secondary cell walls, port the hypothesis [15] that changes in cell wall com- particularly xylem cells, contain lignin that increases wall position are fundamentally involved with plant evolution strength. and diversification (Figure 1). Primary cell wall polysaccharides Interest in non-Angiosperm cell wall composition is not The majority of research regarding cell wall composition only of intrinsic interest, but the increasing use of Phys- in diverse plant groups has concentrated on the primary comitrella patens (Hedw.) B.S.G., a moss, as a tool for cell wall owing to the existence of cell type specific investigating Angiosperm cell wall biochemistry [16] variation between secondary cell walls. demands more complete characterisation of bryophyte walls. The main cell wall components, polysaccharides, The primary cell wall is composed of cellulose microfibrils represent a major and renewable source of photosynthe- embedded in a gel-like matrix of non-cellulosic polysac- tically fixed carbon and are of importance as a source of charides and glycoproteins. The cellulose–hemicellulose Current Opinion in Plant Biology 2008, 11:286–292 www.sciencedirect.com Cell wall diversity Popper 287 Figure 1 Key transitions in cell wall components mapped onto a land plant phylogeny (adapted from references [44,45]). Changes in composition are symbolised as: (+) appearance or substantial increase in occurrence; (#) either a reduction or loss; ( )(1! 3), (1 ! 4)-b-D-glucan [18]; ( ) xyloglucan [13]; ( ) mannose; ( )3-O-Methylgalactose [13]; ( )3-O-Methylrhamnose [13]; ( ) galacturonic acid; ( ) glucuronic acid; ( ) tannins [12]; ( ) branched 4-linked xylan [6]; ( ), rhamnogalacturonan II [11]. Representatives of taxonomic groups shown are (a) Poales, wheat (Triticum aestivum L.); (b) Angiosperms (excluding Poales), Ox-eye Daisy (Leucanthemum vulgare Lam.); (c) Gymnosperms, Larch (Larix decidua L.); (d) Pteridophytes, Tree fern; (e) Lycopodiophytes, Selaginella (Selaginella martensii Spring.); (f) Bryopsida, mosses (Polytrichum sp.); (g) Marchantiopsida, Liverworts (Lunularia cruciata (L.) Lindb.); (h) Anthocerotopsida, hornworts (Phaeoceros carolinanus (Michx.) Prosk.); (i) Charophytes, (Nitella sp.) network co-exists with a network consisting of pectic Although relatively few detailed structural analyses have polysaccharides. A covalent linkage between xyloglucan been performed on cell walls from non-Angiosperm taxa, and pectin, interconnecting the two networks, appears to it appears that seed plants have cell walls with similar, be widespread among Angiosperm taxa [17]. though not identical, compositions. The quantitatively www.sciencedirect.com Current Opinion in Plant Biology 2008, 11:286–292 288 Physiology and metabolism Table 1 Occurrence of cell wall components shown to vary, with phylogenetic significance, between land plant taxa Plant group Monosaccharides Polysaccharides Proteins 3-O- 3-O- Uronic Xylan Mannan Xylo- RGII Pectin (1 ! 3), Expansins Ces/Csl MeRha MeGal acids glucana (1 ! 4)-b- D-glucan Charophytes + À + À + ÀÆ++ À Hornwort + À +++ ++Æ +++ À Liverworts and basal mosses + À + À +++Æ ++ À Advanced mosses + ÀÆ++ ++ Æ ++ À EXPA (conserved CesA, CslA, function) and CslC, CslDb EXPB Homosporous lycopodiophytes + + Æ ++ ++++ À Heterosporous lycopodiophytes + + Æ ++ ++++ À Eusporangiate ferns ÀÆÆ++ ++++ À Leptosporangiate ferns ÀÆÆ+ Æ ++ + + À Gymnosperms ÀÆÆ+ Æ ++ + + À Dicotyledonous Angiosperms ÀÆÆ+ Æ ++ + + À EXLA, EXLB, CesA, CslA, EXPA, EXPB CslB, CslC, CslD, CslE, CslG Poales members of ÀÆÆ+ Æ + + + + CesA, CslA, monocotyledonous CslC, CslD, Angiosperms CslE, CslF, CslH À, not detectable; Æ, trace; +, present at low concentration; ++, present at moderate concentration; +++, present at high concentration. a Xyloglucan shows diversity in glycosyl composition. b CslD is highly represented among P. patens ESTs that may reflect their involvement in tip growth of moss protonemata [16]. predominant monosaccharides present in the walls are D- Rhamnogalacturonan II (RGII) is required for growth and glucose (Glc), D-galactose (Gal), D-mannose (Man), D- development in Angiosperms, and comparable amounts xylose (Xyl), L-arabinose (Ara), L-fucose (Fuc), L-rham- occur in members of the most primitive extant plants nose (Rha) and D-galacturonic acid (GalA). Poales walls lycopodiophytes, equisetophytes, psilotophytes and pter- contain more Xyl and less GalA, Gal and Fuc than other idophytes. By contrast, gametophytes of bryophytes con- Angiosperms and Gymnosperms contain more Man resi- tain only 1% of the amounts present in vascular plants. dues. Differences in cell wall composition are correlated In addition the glycosyl sequence of RGII appears to be with diversification of specific plant taxa. The lycopodio- conserved with the exception that the non-reducing Rha phytes form a distinctive, basal, monophyletic clade residue present on the aceric acid containing side-chain of within extant vascular plants whose cell walls uniquely RGII is replaced by 3-O-methylrhamnose (3-O-MeRha) contain the unusual monosaccharide residue 3-O-methyl- in some lycopodiophytes and pteridophytes [11]. RGII is galatose [12] that is likely to be a component of many linked with the ability to form upright stem and formation lycopodiophyte primary cell wall polysaccharides in- of lignified cell walls, which correlates well with its cluding xyloglucan (MA O’Neill, personal communi- increased concentration in vascular plants. cation). Secondary cell wall polysaccharides Additional variation of cell wall composition exists at the Variation in secondary cell wall composition is perhaps polysaccharide level, (1 ! 3), (1 ! 4)-b-D-linked glucans the most pertinent in the context of biomass production. are restricted to the Poales [18] and xyloglucan is present Secondary cell