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

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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

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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. Although the molecular functions of AGPs are still

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Distribution of FLA genes in plants patens subsp. patens (moss), Chlamydomonas reinhardtii (green alga), Volvox carteri (green alga), Synechocystis One can explore the evolution process of AGPs in sp. PCC 6803 (cyanobacterium), and Synechococcus plants by analyzing the distribution of related genes in sp. PCC 7335 (cyanobacterium) by BLAST search using the genomes of various organisms. To date more than 40 the sequences of Arabidopsis FLA2, 9, and 17, in the genes encoding AGP core proteins have been identified following databases: poplar, http://genome.jgi-psf.org/ in Arabidopsis (Gaspar et al., 2001; Schultz et al., 2002). cgi-bin/runAlignment?db=Poptr1_1&advanced=1; rice, Having a fasciclin domain in the core protein, FLAs are http://blast.jcvi.org/euk-blast/index.cgi?project=osa1; P. presumed to be involved in the cell-to-cell adhesion patens, http://genome.jgi-psf.org/cgi-bin/runAlignment?d that affects the growth anisotropy of plant cells and b=Phypa1_1&advanced=1; C. reinhardtii, http://genome. the formation of secondary cell walls important for the jgi-psf.org/cgi-bin/runAlignment?db=Chlre3&advanced=1 mechanical strength of the plant body. We thus looked ; V. carteri, http://genome.jgi-psf.org/cgi-bin/runAlignment for genes encoding FLAs in poplar (Populus trichocarpa, ?db=Volca1&advanced=1; Synechocystis sp. PCC 6803, dicot), rice (Oryza sativa, monocot), Physcomitrella http://genome.jgi-psf.org/cgi-bin/runAlignment?db=Chlr

SOS5/FLA4 (At5g37850.1) Group III Pp (XP_001784356) 0.1 Os03g0788700 Os03g0788600 Pt(XP_002309262) Syn (YP_002710357) Pt (XP_002336596) Pt (XP_002318499) FLA15 (At3g52370.1) FLA16 (At2g35860.1) Syn (YP_002713742) Os07g0160600 FLA17 (At5g06390.1) Pp (XP_001773169) FLA18 (At3g11700.1)

FLA19 (At1g15190.1) Pp (XP_001754444)

FLA20 (At5g40940.1) FLA2 (At12730.1) FLA1 (At5g55730.1)

FLA21 (At5g06920.1) Os09g0248100

Os02g0726000 FLA7 (At2g04780.1) FLA10 (At3g60900.1) FLA8 (At2g45470.1) Os02g0308800 Pt (XP_002320736)

Os04g0574200 Os02g0308400

Os03g0128000 Os01g0668100

Os05g0563600 FLA5 (At4g31370.1) FLA12 (At5g60490.1) FLA3 (At2g24450.1) Os05g0163300 Pt (XP_02330770) FLA11 (At5g03170.1) Os09g0476800 FLA6 (At2g20520.1) Os02g0461500 FLA9 (At1g03870.1) Group I FLA14 (At3g12660.1) FLA13 (At5g44130.1) Group II Os01g0841100 Os05g0459700

Fig. 3. Phylogenetic relationships of FLAs. Sequences with similarity to fasciclin were collected by BLAST search. The phylogenetic relationships were analyzed using ClustalW. Sequences used for the alignment in Fig. 2 are boxed. For the sequences from Arabidopsis and rice, the gene loci are shown. In the description for the other sequence names, the initial letters mean the source of sequences: Pp, P. patens; Pt, poplar; Syn, Synechococcus sp. PCC 7335. The accession numbers are indicated in parentheses. Partial sequences from poplar and P. patens are not included in the tree. The bar indicates substitutions per site.

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e3&advanced=1; Synechococcus sp. PCC 7335, http:// Distribution of carbohydrate moieties of AGPs www.uniprot.org/taxonomy/91464 (Altschul et al., 1990). In the genomes of poplar and rice, many sequences The backbone structure of AG moieties of AGPs, related to FLAs were found. To date 15 genes encoding β-1,3;1,6-galactan, is highly conserved in plants (Aspinall FLAs have been reported in poplar (Lafarguette et al., et al., 1958a, 1958b; Fincher et al., 1983; Tsumuraya et 2004). Out of these 15 poplar FLA sequences, we found al., 1984, 1988). Using β-glycosyl-Yariv reagent, which 14 in the BLAST search, suggesting that the search specifically reacts with AG moieties, presence of AGs procedure worked well. The number of the sequences in has been demonstrated in gymnosperms, ferns, mosses, rice (18) was comparable with that from Arabidopsis (21, and liverworts as well as angiosperms (Clarke et al., Johnson et al., 2003). P. patens also appeared to possess 1978; Komalavilas et al., 1991). Indeed, the treatment FLA-related genes, although the number was small (6). of P. patens cells with β-glycosyl-Yariv reagent inhibits An FLA-related sequence of P. patens appears to have apical cell expansion (Lee et al., 2005), indicating that both a signal peptide in the N-terminus and a GPI-anchor AG moieties are also important for the function of AGPs signal at the C-terminus according to analyses using the in moss. We have reported the structure of a β-galactan SignalP 3.0 and big-PI Predictor programs (Eisenhaber with β-1,3;1,6-galactan as the backbone from Prototheca et al., 1999; Emanuelsson et al., 2000; Bendtsen et al., zopfii, which belongs to the Chlorellaceae family (Okemoto 2004). Importantly, P. patens possesses a gene encoding et al., 2003). Moreover, β-1,3;1,6-galactan has been an FLA whose sequence is highly related to those from found in a snail and a mammal (Roy and Glaudemans, Arabidopsis, poplar and rice (Fig. 2). We could not find 1978; Iacomini et al., 1981). It thus seems that the origin related sequences in the green algae C. reinhardtii and V. of AG is relatively old. The present data support the idea carteri and the cyanobacterium, Synechocystis sp. PCC that higher plants have obtained a variety of functions 6803. However, Synechococcus sp. PCC 7335 has two from AGPs by coupling of AGs with core proteins. genes encoding proteins related to Arabidopsis FLA17. The AG moieties are necessary for the functions of To understand the relationship between FLAs in these AGPs. Because the metabolism of the carbohydrate organisms, a phylogenetic analysis was performed (Fig. moieties of AGPs is extremely rapid (Gibeaut and Carpita, 3). In the phylogenetic tree, at least three subgroups, 1991), the functions of AGPs are likely regulated via group I, II, and III, were observed. Rice FLA-related degradation catalyzed by glycoside hydrolases. To date, sequences were present in all three subgroups, as were three types of enzymes, the β-galactosidase of glycoside Arabidopsis FLAs. These facts suggest that the functions hydrolase family (GHF) 35, the α-L-arabinofuranosidase of FLAs are highly conserved in angiosperms. On the of GHF 3, and the β-glucuronidase of GHF 79, are known other hand, P. patens seems to lack FLAs of group I and to participate in the hydrolysis of AG moieties (Sekimata II. Sequences from Synechococcus sp. PCC 7335 formed et al., 1989; Henrissat, 1991; Hata et al., 1992; Henrissat a subgroup apart from these groups. Interestingly, the and Bairoch, 1993; Kotake et al., 2005, 2006; Eudes expression pattern of Arabidopsis FLA11, a member of et al., 2008). If, as seems likely, AGPs are part of the group II, suggests that it participates in the formation of molecular mechanism providing gravity resistance, it will secondary cell walls (Brown et al., 2005). Acquisition of be important to study the expression levels and behavior group II genes might thus be involved in the development of these enzymes under various gravitational conditions. of secondary cell walls. Genes of the other groups, I and III, are expected to have functions different from Conclusion those of the group II. A defect in the (ungrouped in Fig. 3) SOS5/FLA4 gene causes abnormal expansion of FLAs are found in many higher plants including epidermal, cortical, and endodermal cells in Arabidopsis mosses, but not in green alga. On the other hand, the roots, indicating that this FLA is required for proper root backbone structure of the carbohydrate moieties of AGPs, morphology (Shi et al., 2003). It is also possible that β-1,3:1,6-galactan, is widely shared among an even wider other FLAs related to SOS5/FLA4 play roles in the growth range of organisms including a Chlorellaceae, a snail, and anisotropy of roots regulated by gravity. a mammal. The acquisition of AGPs of the present forms, We also tried to identify genes encoding core particularly FLAs, may be involved in the development of proteins of classical AGPs in poplar, rice, P. patens, C. resistance to gravitational force. Through the study of the reinhardtii, V. carteri, Synechocystis sp. PCC 6803, and molecular functions of AGPs under different gravitational Synechococcus sp. PCC 7335. As reported previously conditions, we should be able to add valuable information (Lee et al., 2005), several genes possibly encoding to our understanding of the evolutional process of water- classical AGPs were found in P. patens. However, we living organisms to land plants. could not find sequences related to the classical AGPs of higher plants in C. reinhardtii, V. carteri, Synechocystis References sp. PCC 6803, or Synechococcus sp. PCC 7335. This suggests that classical AGPs have evolved only in higher Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and plants, including mosses. However, we can not exclude Lipman, D.J. (1990) Basic local alignment search tool, the possibility that we missed genes for core proteins J. Mol. Biol., 215, 403-410. of classical AGPs in the green algae and cyanobacteria because the BLAST search with sequences extremely rich in Pro is technically difficult.

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