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Article information

Authors: Yingxuan Ma[a], Kim Johnson[a][i]ORCID iD.svg 

Ma, Y; Johnson, K. 




Abstract

Arabinogalactan-proteins (AGPs) are highly glycosylated proteins (glycoproteins) found in the cell walls of plants. AGPs account for only a small portion of the cell wall, usually no more than 1% of dry weight of the primary wall. AGPs are members of the hydroxyproline-rich glycoprotein (HRGP) superfamily that represent a large and diverse group of glycosylated wall proteins (Showalter, 1993). AGPs have attracted considerable attention due to their highly complex structures and potential roles in signalling. In addition, they have industrial and health applications due to their chemical/physical properties (water-holding, adhesion and emulsification) (Ellis et al., 2010). Glycosylation can account for more than 90% of the total mass. AGPs have been reported in a wide range of higher plants in seeds, roots, stems, leaves, inflorescences, and are particularly abundant in the stems of gymnosperms and angiosperms (Gaspar et al., 2001). They have also been reported in secretions of cell culture medium of root, leaf, endosperm and embryo tissues, and some exudate producing cell types such as stylar canal cells are capable of producing lavish amounts of AGPs (Fincher and Stone, 1983).

AGP protein backbones and classification[edit]

AGP sequence.tif

Figure 1 |  Protein sequence of a classical, GPI-anchored AGP3 from Arabidopsis thaliana. Features directing post-translational modification are highlighted: ER signal sequence highlighted purple, AGP glycomotifs highlighted blue and GPI signal sequence boxed

The protein component of AGPs is rich in the amino acids Proline (P), Alanine (A), Serine (S) and Threonine (T), or ‘PAST’ (Schultz et al., 2002; Ma and Zhao, 2010; Showalter et al., 2010; Johnson et al., 2017a; Johnson et al., 2017b). Proline residues in the protein backbone can be hydroxylated to Hydroxyproline (O) depending on the surrounding amino acids. The ‘Hyp contiguity hypothesis’ (Kieliszewski and Lamport, 1994; Johnson et al., 2017a; Johnson et al., 2017b) predicts that when O occurs in a non-contiguous manner, for example SOTO, such as occurs in AGPs, this acts as a signal for O-linked glycosylation of large branched type II arabinogalactan (AG) polysaccharides (Tan et al., 2003). Sequences that direct AG glycosylation (SO, TO, AO, VO) are called AGP glycomotifs (Figure 1).

All AGP protein backbones contain a minimum of 3 clustered AGP glycomotifs and an N-terminal signal peptide that directs the protein into the endoplasmic reticulum (ER) where post-translational modifications begin (Schultz et al., 1998). Prolyl hydroxylation of P to O is fulfilled by prolyl 4-hydroxylases (P4Hs) belonging to the 2-oxoglutarate dependant dioxygenase family (Koski et al., 2007). P4H has been identified in both the ER and Golgi apparatus (Ellis et al., 2010). The addition of the glycosylphosphatidylinositol (GPI)-anchor occurs in most but not all AGPs (Schultz et al., 2002).

AGP family of glycoproteins[edit]

AGP Figure wiki v1.tif

Figure 2 |  Schematic of the predicted structures of selected AGP sub-families. Classical AGPs contain glycomotifs directing hydroxylation of P to O and subsequent O-glycosylation to which large type II arabinogalactan chains (Type II AG, yellow shapes) are attached. Many AGPs are predicted to contain a GPI-anchor at the C-terminus. Hybrid AGPs contain motifs characteristic of more than one HRGP family, for example glycomotifs typical of extensins (SP3-5; red bars) that direct addition of short arabinose (Ara) side chains (dark red) on Hyp and galactose (Gal; green) on Ser residues. Cross-linking Tyr motifs (dark blue bars) may also be present in the protein backbone. Chimeric AGPs have a recognised PFAM domain (green) in addition to the AGP region

AGPs belong to large multigene families and are divided into several sub-groups depending on the predicted protein sequence (Showalter, 2001; Schultz et al., 2002; Gaspar et al., 2004; Huang et al., 2013; Johnson et al., 2017a; Johnson et al., 2017b). ‘Classical’ AGPs include the GPI-AGPs that consist of a signal peptide at the N-terminus, a PAST-rich sequence of 100-150 aa and a hydrophobic region at the C-terminus that directs addition of a GPI-anchor; non GPI-AGPs that lack the C-terminal GPI signal sequence, Lysine(K)-rich AGPs that contain a K-rich region within the PAST-rich backbone and AG-peptide that have a short PAST-rich backbone of 10-15 aa (Figure 2). Chimeric AGPs consist of proteins that have an AGP region and an additional region with a recognised PFAM (protein family) domain. Chimeric AGPs include fasciclin-like AGPs (FLAs), phytocyanin-like AGPs (PAGs/PLAs, also known as early-nodulin-like proteins, ENODLs) and xylogen-like AGPs (XYLPs) that contain lipid-transfer-like domains (Showalter et al., 2010). Other ‘non-classical’ AGPs exist such as histidine (H)-rich and cysteine (C)-containing domains as well as many hybrid HRGPs that have motifs characteristic of AGPs and other HRGP members, usually extensins (Baldwin, 2001; Gaspar, 2001; Gaspar et al., 2004; Showalter et al., 2010; Johnson et al., 2017; Johnson et al., 2017).

AGP biosynthesis[edit]

After translation, the AGP protein backbones are highly decorated with complex carbohydrates, primarily type II AG polysaccharides (Liang et al., 2013). The biosynthesis of the mature AGP involves cleavage of the signal peptide at the N-terminus, hydroxylation on the P residues and subsequent glycosylation and in many cases addition of a GPI-anchor.

The structure of the AG glycans consists of a backbone of β-1,3 linked Gal (galactose), with sidechains of β-1,6 linked Gal and have terminal residues of Ara (arabinose), Rha (rhamnose), Gal, Fuc (fucose), and GlcA (glucuronic acid). Glycosylation of the AGP backbone is initiated in the ER (Oka et al., 2010) followed by chain extension primarily in the GA (Kato et al., 2003). The AG glycan moiety of AGPs is assembled by glycosyltransferases (Showalter and Basu, 2016). O-glycosylation of AGPs is initiated by the action of Hyp-O-galactosyltransferases (Hyp-O-GalTs) that add the first Gal onto the protein. The complex glycan structures are then elaborated by a suite of glycosyl transferase (GTs) the majority of which are bio-chemically uncharacterized. The GT31 family is the most likely family involved in AGP glycan backbone biosynthesis (Egelund, 2007; Qu et al., 2008). Numerous members of the GT31 family have been identified with Hyp-O-GALT activity (Basu, 2015; Ogawa-Ohnishi and Matsubayashi, 2015) and the core β-(1,3)-galactan backbone is also likely to be synthesized by the GT31 family (Qu et al., 2008). Members of the GT14 family are implicated in adding β-(1,6)- and β-(1,3)-galactans to AGPs (Knoch et al., 2013; Dilokpimol and Geshi, 2014). In Arabidopsis terminal sugars such as fucose are proposed to be added by AtFUT4 (fucosyl transferase) and AtFUT6 in the GT37 family (Wu et al., 2010; Tryfona et al., 2014) and the terminal GlcA incorporation can be catalysed by the GT14 family (Knoch et al., 2013; Dilokpimol, 2014). A number of GTs remain to be identified, for example those responsible for terminal Rha.

The addition of the GPI-anchor occurs in most but not all AGPs (Schultz et al., 2002). The early synthesis of the GPI moiety occurs on the ER cytoplasmic surface and subsequent assembly take place in the lumen of the ER. These include the assembly of tri-mannose, galactose and ethanolamine phosphate to form the mature GPI moiety. AGPs undergo GPI-anchor addition while co-translationally migrating into the ER and these two processes finally converge. Subsequently, a transamidase complex simultaneously cleaves the core protein at the C-terminus when it recognizes the ω cleavage site and transfers the fully assembled GPI-anchor onto the amino acid residue at the C-terminus of the protein. These events occur prior to prolyl hydroxylation and glycosylation (Imhof et al., 2004; Ellis et al., 2010). The core glycan structure of GPI anchors is Man-α-1,2-Man-α-1,6-Man-α-1,4-GlcN-inositol (Man: mannose, GlcN: glucosaminyl), which is conserved in many eukaryotes (Ferguson, 1988, 1999; Oxley, 1999; Ellis et al., 2010; Strasser, 2016). The only plant GPI anchor structure characterized to date is the GPI-anchored AGP from Pyrus communis suspension-cultured cells (Oxley, 1999). This showed a partially modified glycan moiety compared to previously characterized GPI anchors as it contained β-1,4-Gal. The GPI anchor synthesis and protein assemble pathway is proposed to be conserved in mammals and plants (Ellis et al., 2010). The integration of a GPI-anchor enables the attachment of the protein to the membrane of the ER transiting to the GA leading to secretion to the outer leaflet of the plasma membrane facing the wall (Muniz and Zurzolo, 2014). As proposed by Oxley and Bacic (1999), the GPI-anchored AGPs are likely released via cleavage by some phospholipases (PLs) (C or D) and secreted into the extracellular compartment.

AGPs functional roles[edit]

AGPs have been shown to regulate many aspects of plant growth and development including male-female recognition in reproduction organs, cell division and differentiation in embryo and post-embryo development, seed mucilage cell wall development and root salt tolerance (see Table 1) (Ellis et al., 2010). These studies suggest that they are multifunctional, similar to what is found in mammalian proteoglycans/glycoproteins (Filmus et al., 2008; Schaefer and Schaefer, 2010; Tan et al., 2012). Conventional methods to study functions of AGPs include the use of β-glycosyl (usually glucosyl) Yariv reagents and monoclonal antibodies (mAbs). β-Glycosyl Yariv reagents are synthetic phenylazo glycoside probes that specifically, but not covalently, bind to AGPs and can be used to precipitate AGPs from solution. They are also used commonly as histochemical stains to probe the locations and distribution of AGPs (Yariv et al., 1962; Tang et al., 2006). A number of studies have shown that addition of β-Yariv reagents to plant growth medium can inhibit seedling growth, cell elongation, block somatic embryogenesis and fresh cell wall mass accumulation (Willats and Knox, 1996; Chapman et al., 2000; Zagorchev et al., 2013). The use of mAbs that specifically bind to carbohydrate epitopes of AGPs have also been employed to infer functions based on the location and pattern of the AGP epitopes. Commonly used mAb against AGPs include CCRC-M7, LM2, JIM8, JIM13 and JIM14 (Seifert and Roberts, 2007).

The function of individual AGPs has largely been inferred through studies of mutants. For example, the Arabidopsis root-specific AtAGP30 was shown to be required for in vitro root regeneration suggesting a function in regenerating the root by modulating phytohormone activity (Van-Hengel and Roberts, 2003). Studies of agp6 and agp11 mutants in Arabidopsis have demonstrated the importance of these AGPs to prevent uncontrolled generation of the pollen-grain and for normal growth of the pollen-tube (Coimbra et al., 2010; Suzuki et al., 2017). Functions attributed to AGPs are outlined in Table 1.

Table 1. Summary of proposed functions of AGPs in plant growth and development.
Biological role AGP1, 2 Location(s) Function(s) References
Embryogenesis GhPLA1 Somatic embryos Promoting somatic embryogenesis (Poon et al., 2012)
DcAGPs Somatic embryos Promoting somatic embryogenesis (McCabe et al., 1997; Toonen et al., 1997)
AtAGPs Embryos Embryo development and differentiation (Hu et al., 2006)
NtAGPs Embryos Embryo development (Qin and Zhao, 2006)
BgAGPs Somatic embryos Somatic embryo development rate and morphology (Steinmacher et al., 2012)
BnAGPs Embryos Embryo development (Tang et al., 2006)
MaAGPs Somatic embryos Promoting somatic embryogenesis (Pan et al., 2011)
PsAGPs Promoting somatic embryogenesis (Duchow et al., 2016)
FsAGPs Embryos Establishment and stability of the cell wall (Herve et al., 2016)
VcALGAL-CAM embryos embryo cell adhesion (Huber and Sumper, 1994)
VcISG embryos Embryo inversion (Hallmann and Kirk, 2000)
Reproduction AtAGP4 (JAGGER) Pistil Pollen tube blockage (Pereira et al., 2016)
AtAGP6, AtAGP11 Stamen, pollen grain and pollen tube Pollen grain development and pollen tube growth (Levitin et al., 2008; Coimbra et al., 2009)
AtAGP18 Ovule Megaspore selection (Acosta-Garcia and Vielle-Calzada, 2004) Demesa (Demesa-Arevalo and Vielle-Calzada, 2013)
AtFLA3 Pollen grain and pollen tube Microspore development (Li et al., 2010)
AtENODL11-15 Micropylar Pollen tube reception (Mashiguchi et al., 2009; Hou et al., 2016)
BcmMF8 Pollen grain and pollen tube Pollen wall development and pollen tube growth (Lin et al., 2014)
BcmMF18 Pollen grain Pollen grain development, intine formation (Lin et al., 2018)
NtTTS Pistil Pollen tube growth and guidance (Cheung et al., 1995)
Np/Na120kD Pistil S-specific pollen rejection (self-incompatibility) (Hancock et al., 2005)
OsMTR1 Male reproductive cells Anther development and pollen fertility (Tan et al., 2012)
Plant development AtAGP19 Stem, flower, root and leaf Cell division and expansion, leaf development and reproduction (Yang et al., 2007)
AtAGP57C Rosette leaf, silique, seed, flower, and shoot apex of inflorescence stem Cell wall structure maintenance (Tan et al., 2013)
AtFLA1 Stomata, trichome, leaf vasculature, primary root tip and lateral root Lateral root development and shoot regeneration (Johnson et al., 2011)
AtFLA4 (SOS5) Flower, leaf, stem, root, silique Root salt stress tolerance; seed mucilage adherence (Shi et al., 2003; Harpaz-Saad et al., 2011; Griffiths et al., 2014; Griffiths et al., 2016; Xue et al., 2017)
PpAGP1 Apical cells Apical cell expansion (Lee et al., 2005)
AtAGP30 Root Root regeneration and seed germination (van Hengel and Roberts, 2003)
BcrFLA1 Root Root hair elongation (Kirchner et al., 2017)
Secondary wall development AtFLA11, AtFLA12 Stem and branch Secondary cell wall synthesis/patterning (MacMillan et al., 2010)
AtXYP1, AtXYP2 Cell walls of differentiating tracheary elements Vascular tissue development and patterning (Motose et al., 2004)
GhAGP4 Cotton fiber Cotton fiber initiation and elongation (Li et al., 2010)
GhFLA1 Cotton fiber Fiber initiation and elongation (Huang et al., 2013)
PtFLA6 Stem xylem fiber Secondary cell wall synthesis/patterning (Wang et al., 2015)
Defense SlattAGP Site of parasite attack Promotes parasite adherence (Albert et al., 2006)

1Gh: Gossypium hirsutum. Dc: Daucus carota. At: Arabidopsis thaliana. Nt: Nicotiana tabacum. Bg: Bactris gasipaes. Bn: Brassica napus. Ma: Musa spp. AAA. Ps: Pelargonium sidoides. Fs: Fucus serratus. Vc: Volvox carteri. Bcm: Brassica campestris. Np: Nicotiana plumbaginifolia. Na: Nicotiana alata. Os: Oryza sativa. Pp: Physcomitrella patens. Bcr: Brassica carinata. Pt: Populus trichocarpa. Sl: Solanum lycopersicum.

2PLA: phytocyanin-like AGP. ALGAL-CAM: algal cell adhesion molecule. ISG: inversion-specific glycoprotein. FLA: fasciclin like AGP. ENODL: earlt nodulation like. MF: male fertility. TTS: transmitting tissue specific. MTR: microspore and tapetum regulator. SOS: salt overly sensitive. XYP: xylogen protein. attAGP: attachment AGP.

Additional information[edit]

Acknowledgements[edit]

The authors would like to acknowledge the support of the La Trobe Institute for Agriculture and Food and a La Trobe Research Focus Area grant 2000004372.

Competing interests[edit]

The authors have no competing interests to declare.

Ethics statement[edit]

No animal or human research was performed.

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