Moss Cell Walls: Structure and Biosynthesis Alison W
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University of Rhode Island DigitalCommons@URI Biological Sciences Faculty Publications Biological Sciences 2012 Moss cell walls: structure and biosynthesis Alison W. Roberts University of Rhode Island, [email protected] Eric M. Roberts See next page for additional authors Creative Commons License This work is licensed under a Creative Commons Attribution 3.0 License. Follow this and additional works at: https://digitalcommons.uri.edu/bio_facpubs Citation/Publisher Attribution Roberts AW, Roberts EM and Haigler CH (2012) Moss cell walls: structure and biosynthesis. Front. Plant Sci. 3:166. doi: 10.3389/ fpls.2012.00166 Available at: https://doi.org/10.3389/fpls.2012.00166 This Article is brought to you for free and open access by the Biological Sciences at DigitalCommons@URI. It has been accepted for inclusion in Biological Sciences Faculty Publications by an authorized administrator of DigitalCommons@URI. For more information, please contact [email protected]. Authors Alison W. Roberts, Eric M. Roberts, and Candace H. Haigler This article is available at DigitalCommons@URI: https://digitalcommons.uri.edu/bio_facpubs/205 MINI REVIEW ARTICLE published: 19 July 2012 doi: 10.3389/fpls.2012.00166 Moss cell walls: structure and biosynthesis Alison W. Roberts1*, Eric M. Roberts2 and Candace H. Haigler3,4 1 Department of Biological Sciences, University of Rhode Island, Kingston, RI, USA 2 Department of Biology, Rhodes Island College, Providence, RI, USA 3 Department of Crop Science, North Carolina State University, Raleigh, NC, USA 4 Department of Plant Biology, North Carolina State University, Raleigh, NC, USA Edited by: The genome sequence of the moss Physcomitrella patens has stimulated new research Seth DeBolt, University of Kentucky, examining the cell wall polysaccharides of mosses and the glycosyl transferases that syn- USA thesize them as a means to understand fundamental processes of cell wall biosynthesis Reviewed by: and plant cell wall evolution. The cell walls of mosses and vascular plants are composed of Vincent Bulone, Royal Institute of Technology, Sweden the same classes of polysaccharides, but with differences in side chain composition and Gregory Buda, Cornell University, USA structure. Similarly, the genomes of P.patens and angiosperms encode the same families *Correspondence: of cell wall glycosyl transferases, yet, in many cases these families have diversified inde- Alison W. Roberts, Department of pendently in each lineage. Our understanding of land plant evolution could be enhanced Biological Sciences, University of by more complete knowledge of the relationships among glycosyl transferase functional Rhode Island, 120 Flagg Road, Kingston, RI 02881, USA. diversification, cell wall structural and biochemical specialization, and the roles of cell walls e-mail: [email protected] in plant adaptation. As a foundation for these studies, we review the features of P.patens as an experimental system, analyses of cell wall composition in various moss species, recent studies that elucidate the structure and biosynthesis of cell wall polysaccharides in P. patens, and phylogenetic analysis of P. patens genes potentially involved in cell wall biosynthesis. Keywords: cell wall, polysaccharide, cellulose, cellulose synthesis complex, glycosyl transferase, moss, Physcomitrella patens MOSS BIOLOGY AND EVOLUTION by diploid sporophytes, which develop from eggs fertilized by The common ancestor of land plants is believed to have resem- swimming sperm at the gametophore apex (Schumaker and bled extant mosses in having a biphasic life cycle with a dominant Dietrich, 1998). haploid gametophyte and rudimentary adaptations for tolerating Although structurally simple, moss gametophytes contain dif- the aerial environment. Because they have retained these charac- ferent cell types. The protonema is differentiated into chloroplast- teristics, mosses are often referred to as “lower” plants (Mishler rich chloronemal cells and caulonemal cells, which elongate three and Oliver, 2009). Despite this designation, mosses are highly suc- times faster (Menand et al., 2007). In response to dehydration cessful, comprising more than 10,000 species adapted to diverse stress, protonemal cells resume division and differentiate into habitats ranging from submerged aquatic to desert (Buck and thick-walled, dehydration-tolerant brachycytes, and subtending Goffinet, 2000). Mosses differ from vascular plants in the strat- tmema cells, which undergo programmed cell death (Decker et al., egy they employ to survive in the dry aerial environment. Vascular 2006). Gametophores include a stem, leaves, axillary hairs, and plants are homeohydric with a thick cuticle to reduce dehydra- rhizoids. The stem typically consists of small, thick-walled epi- tion, roots to extract water from the soil, and vascular tissue dermal and subepidermal cells, thin-walled parenchyma cells, to distribute water internally. In contrast, mosses are poikilo- and conducting cells. The conducting cells include hydroids hydric, depending on a surface film of free water to maintain and leptoids, which are functionally analogous to xylem and hydration. Although some mosses are confined to aquatic habitats, phloem (Buck and Goffinet, 2000). Similar to tracheary ele- many are dehydration tolerant and some are desiccation tolerant ments, hydroids are dead at maturity and connected by perfora- (Mishler and Oliver, 2009). tions, but they lack thick lignified secondary cell walls (Hebant, The life cycle, morphology, and biochemistry of mosses have 1977). Leaves are typically one cell layer thick except for the been influenced by selective pressure associated with poikilohydry. midribs and margins, which may consist of multiple layers of Because cellular water status is controlled by surface absorption differentiated cells. Leaf cells of Sphagnum species include pho- and diffusion, moss organs are small and thin, and lignin is not tosynthetic chlorocytes and hyalocytes with elaborate cell wall required to provide support against gravity or the negative pres- thickenings. Other leaf cell specializations include papillae and sures generated during transpiration (Mishler and Oliver, 2009). various surface elaborations. Additional differentiated cell types In most mosses, haploid spores produce protonemal filaments form the gametangia, gametes, and sterile paraphyses. The that extend by apical division and tip growth (Figure 1). The sporophyte stalk, sporangium, and spores also consist of spe- filaments produce buds that develop into leafy gametophores, cialized cell types (Buck and Goffinet, 2000), including stomata which enlarge by diffuse growth. Haploid spores are produced (Sack and Paolillo, 1983). www.frontiersin.org July 2012 | Volume 3 | Article 166 | 1 “fpls-03-00166” — 2012/7/18 — 14:17 — page1—#1 Roberts et al. Moss cell walls FIGURE 1 | Development of Physcomitrella patens. A haploid secondary caulonemata (not shown), or buds. Buds develop into leafy spore or protoplast germinates to form a primary chloronema with gametophores, which produce apical gametangia. Fertilization of an numerous chloroplasts and transverse cross walls, which subsequently egg by swimming sperm at the gametophore apex produces a zygote, differentiates into a more rapidly growing primary caulonema with fewer which develops into a diploid sporophyte consisting of a stalk and chloroplasts and oblique cross walls. The caulonemal subapical cells divide sporangium (not shown). Meiotic divisions within the sporangium generate to produce initials cells, which develop into lateral secondary chloronemata, haploid spores. Although mosses share a poikilohydric ecological strategy and PHYSCOMITRELLA PATENS, THE MODEL MOSS SPECIES common body plan, their diversification and colonization of As a member of the Funariales, Physcomitrella patens occupies different habitats have been accompanied by the evolution of spe- a phylogenetic position at the base of the true mosses. As an cialized morphological and biochemical adaptations that must be inhabitant of moist soils that tolerates dehydration, but not des- considered when inferring evolutionary trends from compara- iccation, it represents a “primitive moss ecology” (Mishler and tive studies of mosses and vascular plants. The mosses diverged Oliver, 2009). This lack of specialization for extreme conditions from the land plant lineage between the liverworts and the horn- combined with abundant genomic resources (Rensing et al., 2008), worts, which most recent phylogenies place as sister to the vascular efficient production of transgenic genotypes, and ease of culture plants. The moss lineage includes the“true mosses”and three early and experimental manipulation (Cove, 2005)providesanoppor- divergent and ecologically specialized lineages, the aquatic Sphag- tunity to relate the diversification of gene families to innovations nales, the desiccation-tolerant rock-dwelling Andreales, and the in cell wall composition, structure, and development that accom- morphologically diverse Polytricales (Mishler and Oliver, 2009). panied the adaptation of plants to life on land. Other advantages Whereas mosses have retained primitive aspects of cell wall struc- of P. patens include the ability to produce large amounts of tissue ture and composition due to poikilohydry, they have also evolved consisting of a single cell type (chloronemal filaments) and rapid special cell wall adaptations that enabled them to colonize diverse cell wall regeneration in protoplasts (Lee et al., 2005a; Lawton and habitats.