Arabinogalactan-Proteins in the Evolution of Gravity Resistance In

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Arabinogalactan-Proteins in the Evolution of Gravity Resistance In Biological Sciences in Space, Vol.23 No.3, 143-149, 2009Kotake, T. et al. Special Issue: Gravity Responses and The Cell Wall in Plants Arabinogalactan-Proteins Introduction in The Evolution of Gravity As water-living organisms evolved into land plants, Resistance in Land Plants cell walls developed to support the plant body against 1 G of gravity on earth. The cell walls of higher plants mainly Toshihisa Kotake1†, Naohiro Hirata1, consist of cellulose, hemicellulose, pectin, lignin, structural 1 2 proteins and proteoglycans. It has been suggested that the Kiminari Kitazawa , Kouichi Soga , 1 flexible pectin network is the most ancient and the original and Yoichi Tsumuraya structure of the cell wall of plants. The cellulose and lignin 1 Division of Life Science, Graduate School of networks probably have reinforced the cell walls later, Science and Engineering, Saitama University, 255 giving mechanical strength to the bodies of land plants Shimo-okubo, Sakura-ku, Saitama 338-8570, (Volkmann and Baluska, 2006). Japan To resist gravity, plants regulate the metabolism of 2Department of Biology and Geosciences, cell wall polysaccharides. For example, the degradation Graduate School of Science, Osaka City University, of the anti-gravitational polysaccharide xyloglucan in 3-3-138 Sugimoto-cho, Sumiyoshi-ku, dicotyledonous plants and β-1,3:1,4-glucan in Poaceae plants, is suppressed under hypergravity, which causes Osaka 558-8585, Japan the increase in the cell wall rigidity (Soga et al., 1999a, 1999b, 2000; Hoson and Soga, 2003). Conversely, Abstract the degradation of anti-gravitational polysaccharides is accelerated under microgravity conditions in space The cell walls of land plants developed compared with 1 G on earth, leading to the decrease in under the influence of earth’s gravity. the cell wall rigidity (Hoson et al., 2002; Hoson and Soga, Arabinogalactan-proteins (AGPs) are a family 2003). of proteoglycans that localize on plasma Recently, Tamaoki et al. (2009) have reported the up- membranes and in cell walls of higher regulated expression of genes encoding core proteins plants. Recent studies have revealed that the of arabinogalactan-proteins (AGPs) in the inflorescence expression levels of genes encoding the core stems of Arabidopsis (Arabidopsis thaliana) under proteins of AGPs are modified by hypergravity, hypergravity. It thus seems that AGPs are involved in the indicating the involvement of AGPs in gravity gravity resistance of higher plants. resistance. A BLAST search in the genome databases of various organisms for genes General properties of arabinogalactan-protein encoding proteins related to fasciclin-like AGPs (FLAs), found FLAs in land plants including a AGPs are a family of proteoglycans commonly moss, Physcomitrella patens subsp. patens, found on the plasma membrane and in the cell wall of but not in the green algae, Chlamydomonas higher plants. They are implicated in many physiological reinhardtii or Volvox carteri. On the other hand, processes such as cell-to-cell signaling, cell adhesion, the backbone structure of arabinogalactan cell elongation, cell death, and stress responses in higher moieties of AGPs, β-1,3:1,6-galactan, is widely plants (Fincher et al., 1983; Nothnagel, 1997; Majewska- distributed among organisms and has been Sawka and Nothnagel, 2000; Shi et al., 2003), although confirmed in a species of Chlorellaceae, a many aspects of the molecular functions of AGPs have snail and a mammal. These facts suggest that not yet been clarified. AGPs consist of a hydroxyproline acquisition of some AGPs similar to those (Hyp)-rich core protein and arabinogalactan (AG) currently found, and FLAs in particular, was moieties attached to the Hyp, serine (S) and/or threonine important in the evolution of the resistance of (T) residues (Fig. 1). They are categorized into several plants to gravitational force. By studying the groups based on core protein structure and sequence. molecular functions of AGPs under diverse Classical AGPs consist of a core proteins having a large gravitational conditions, we should be able to number of alanine-proline (AP), SP, and TP motifs, which deepen our understanding of the evolutional undergo AG modification. AG peptides are AGPs whose process that turned aquatic organisms into core proteins are short in their mature forms. Fasciclin- terrestrial plants. ©2009 Jpn. Soc. Biol. Sci. like AGPs (FLAs) possess one or two domains with Space; Article ID: 092302016 similarity to fasciclin, which participates in cell-adhesion in vertebrates and insects, together with AP, SP, and TP motifs. Lysine-rich AGPs have a Lys-rich region in the core protein (Gaspar et al., 2001; Schultz et al., 2002). Received: June 26, 2009; Accepted: July 21, 2009 Most AGP core proteins contain a secretion signal at the †To whom correspondence should be addressed: N-terminus and a glycosylphosphatidylinositol (GPI)- Tel.:+81-(0)48-858-3955; Fax: +81-(0)48-858-3384; anchor signal at the C-terminus (Oxley and Bacic, E-mail: [email protected] 1999), with which AGPs are secreted and anchored on − 143 − Evolution of arabinogalactan-proteins AB Signal peptide β-1,3-Galactan main chain AG-modified region β-1,6-Galactan side chain Fasciclin-like domain GPI-anchor Fig. 1. Schematic diagrams of classical and fasciclin-like AGPs. Structures of classical AGP (A) and fasciclin-like AGP (B) are shown. In general, both AGPs have a signal sequence at the N-terminus and a GPI-anchoring signal at the C-terminus (Oxley and Bacic, 1999; Gaspar et al., 2001). AG moieties having β-1,3:1,6-galactan backbones are attached to AP, SP, and/or TP motifs of the core proteins through O-glycoside linkages (Fincher et al., 1983; Seifert and Roberts, 2007). the plasma membrane (Fig. 1). Recently, based on the [chemical name, 1,3,5-tri(p-glycosyloxyphenylazo)-2,4,6- Hyp-contiguity hypothesis, according to which clustered trihydroxybenzene] specifically binds to AG moieties of noncontiguous Hyp residues are modified with AGs, it has AGPs and perturbs their molecular functions (Yariv et been predicted that not just the typical AGPs described al., 1962; Komalavilas et al., 1991; Majewska-Sawka above, but also some 40% of other GPI-anchored and Nothnagel, 2000). In cultured cells of Arabidopsis, proteins on the cell surface undergo AG modification β-glycosyl-Yariv reagent induces programmed cell death, (Shpak et al., 1999, 2001; Borner et al., 2003; Seifert and possibly by disrupting the plasma membrane-cell wall Robert, 2007). One candidate is COBRA protein, which connections (Gao and Showalter, 1999). Moreover, the participates in the orientation of cellulose microfibrils in function of xylogen is suppressed when the Zinnia cells the primary cell walls and thus regulates the anisotropic are treated with β-glycosyl-Yariv reagent. expansion of plant cells (Roudier et al., 2005). The structure of the AG moieties of AGPs is complex Physiological functions of AGPs and varies depending on source plant, tissue, and developmental stage (Tsumuraya et al., 1984, 1988). Several lines of evidence indicate the involvement of Nevertheless, AG moieties do have several common AGPs in the regulation of growth and morphogenesis in structural features. They all consist of β-1,3-galactosyl plants. For example, β-glycosyl-Yariv reagent inhibits root backbones to which side chains of β-1,6-linked growth in Arabidopsis and cell elongation in suspension- galactosyl residues are attached through O-6 (Fig. 1). cultured carrot cells (Ding and Zhu, 1997; Willats and The β-1,6-linked galactosyl chains are further substituted Knox, 1996). The amount of β-glycosyl-Yariv-reactive with L-arabinofuranose and lesser amounts of other AGPs is closely related to hypocotyl length in Arabidopsis auxiliary sugars such as glucuronic acid, 4-O-methyl- (Takahashi et al., 1995), indicating the involvement of glucuronic acid, L-rhamnose, and L-fucose. AG moieties AGPs in the regulation of growth in plants. Some AGPs are important for the functions of AGPs. Xylogen, for are presumed to participate in the formation of secondary example, a non-classical AGP from Zinnia (Zinnia cell walls. Arabidopsis FLA11 exhibits an expression elegans) mesophyll cells, induces the differentiation to pattern closely related to those of secondary cell wall- tracheary elements, but the inductive function of xylogen specific cellulose synthase genes, IRX1 and IRX3 is lost when the carbohydrate moieties are removed (Brown et al., 2005). In loblolly pine (Pinus taeda L.), the from the xylogen by chemical treatment (Motose et al., occurrence of a classical AGP, PtaAGP6 is associated 2004). It is also well-known that β-glycosyl-Yariv reagent with secondary cell wall formation in differentiating xylem − 144 − Kotake, T. et al. Fig. 2. Amino acid sequences of FLAs. The amino acid sequence of Arabidopsis FLA17 (AtFLA17, At5g06390.1) was aligned with FLA-related sequences from poplar (XP-002309262), rice (Os07g0160600), and P. patens (XP-001784356) by the pairwise method using the ClustalW program. The amino acid residues are numbered from the first Met. Gaps (-) were introduced to achieve maximum similarity. Residues conserved for all sequences are highlighted in black. The signal peptide of AtFLA17 is indicated by a dotted line, and regions with similarity to fasciclin are indicated by solid lines. (Zhang et al., 2003). Additionally, a reduced level of elusive, it is probable that AGPs transmit intercellular AGP has been observed along with impaired cellulose signals to extracellular components in the gravity synthesis in the rice brittle culm 10 mutant, which shows resistance of plants. The spatial localization of AGPs on brittleness of the plant body (Zhou et al., 2009). It thus the plasma membrane raises the intriguing possibility that seems likely that AGPs also have a specific role in the AGPs mediate the signal transduction between cortical formation of secondary cell walls that provide mechanical microtubules and cellulose microfibrils. strength to the plant body, which has to resist 1 G on earth.
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