Ke Zhou- FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China
Diverse proteins are found modified with glycosylphosphatidylinositol (GPI) at their carboxyl terminus in eukaryotes, which allows them to associate with membrane lipid bilayers and anchor on the external surface of the plasma membrane. GPI-anchored proteins (GPI-APs) play crucial roles in various processes, and more and more GPI-APs have been identified and studied. In this review, previous genomic and proteomic predictions of GPI-APs in Arabidopsis have been updated, which reveal their high abundance and complexity. From studies of individual GPI-APs in Arabidopsis, certain GPI-APs have been found associated with partner receptor-like kinases (RLKs), targeting RLKs to their subcellular localization and helping to recognize extracellular signaling polypeptide ligands. Interestingly, the association might also be involved in ligand selection. The analyses suggest that GPI-APs are essential and widely involved in signal transduction through association with RLKs.
Glycosylphosphatidylinositol (GPI) Modification and GPI-Anchored Protein (GPI-AP) Biosynthesis
The GPI oligosaccharide structure is ubiquitous among eukaryotes with a common minimal backbone consisting of three mannoses, one non-N-acetylated glucosamine (GlcN), and inositol phospholipid, which covalently links the carboxyl terminus (C terminus) of GPI-APs to the lipid bilayer (Figure 1A) (Stevens, 1995; Oxley and Bacic, 1999; Kinoshita and Fujita, 2016). Catalyzed by a series of enzyme complexes, GPI biosynthesis starts with a lipid molecule at the rough side of the endoplasmic reticulum (ER), and this then flips and the synthesis is completed on the luminal side of the ER (Figure 1C) (Stevens, 1995; Takeda and Kinoshita, 1995; Kinoshita and Fujita, 2016). The typical GPI-AP precursors possess a common structure that lead them to be modified by GPI moieties inside endomembrane systems: amino-terminal (N-terminal) hydrophobic signal peptides lead them to enter the ER lumen, and during translation and maturation, C-terminal hydrophobic signals are recognized and cleaved at the ω position by a series of catalytic complexes, where the peptide bond is replaced by a bond with ethanolamine phosphate (Figures 1A–C) (Eisenhaber et al., 1998; Kinoshita, 2014a; Kinoshita and Fujita, 2016).
Figure 1 Biosynthesis of GPI moiety and GPI-AP. (A) Minimal oligosaccharide structure of GPI modification, D-Manα (1–2)-D-Manα (1–6)-D-Manα (1–4)-D-GlcN-inositol, which covalently links the C-terminus of GPI-AP and lipid molecule. (B) Common structure of GPI-AP precursor. The hydrophobic regions at the N and C termini are in black and the spacer region is in light gray. (C) Biosynthesis of GPI-APs. ① Precursor of GPI-AP enters ER, ② C terminus of GPI-AP precursor is recognized when entering ER, ③ Oligosaccharide structure of GPI modification is synthesized separately, ④ Recognized C terminus of GPI-AP is cleaved and covalently linked to the GPI moiety.
The GPI moiety allows these GPI-APs, which possess no transmembrane region, to be anchored to membrane lipid bilayers. Compared to transmembrane association, GPI anchoring has its advantages: GPI-AP shedding and release due to the presence of GPI-specific phospholipases (PLC) makes this association reversible in mammalian cells (Orihashi et al., 2012; Fujihara and Ikawa, 2016). In plants, although similar shedding and release mechanisms are indicated as various GPI-APs were identified in cell walls, thus far, no GPI-specific PLC has been identified yet (Bayer et al., 2006; Yeats et al., 2018). However, a bacterial phosphatidylinositol-specific PLC (PI-PLC) has been used for shedding GPI-APs from lipid bilayers in vitro and identifying them by further proteomic analysis in Arabidopsis (Borner et al., 2003; Elortza et al., 2003; Takahashi et al., 2016; Yeats et al., 2018).
Importance of GPI Anchoring for GPI-APs
GPI-APs and their GPI moieties were demonstrated to be crucial for diverse developmental processes in mammals and in plants, because development was found to be broadly and severely affected if GPI moiety biosynthesis is disrupted (Kawagoe et al., 1996; Gillmor et al., 2005; Kinoshita, 2014b; Bundy et al., 2016).
As the most noticeable feature, GPI anchoring was thought to be essential for the functions of GPI-APs, and their enzymatic activities or subcellular localizations could be altered by the removal of the GPI moiety (Tozeren et al., 1992; Butikofer et al., 2001; Davies et al., 2010). However, there are exceptions: the GPI anchoring of ZERZAUST and FLA4/SOS5 was shown to be dispensable for their functions in Arabidopsis (Vaddepalli et al., 2017; Xue et al., 2017).
GPI moieties also play crucial roles for driving the transient, relatively ordered membrane domains rich in sphingolipids and sterols, which are called lipid rafts or microdomains, to their target regions (Saha et al., 2016; Sezgin et al., 2017; Hellwing et al., 2018; Lebreton et al., 2018). In mammalian and yeast cells, GPI-APs are co-clustered and organized in a mixture of monomers and cholesterol-dependent nanoclusters in the same lipid raft. These exit the ER in vesicles distinct from other secretory proteins and are predominantly sorted to the apical surface to serve in protein trafficking and signaling transduction (Eisenhaber et al., 1998; Morsomme et al., 2003; Legler et al., 2005; Muniz and Zurzolo, 2014; Miyagawa-Yamaguchi et al., 2015; Sezgin et al., 2017). In Arabidopsis, although GPI modification was found essential for protein delivery from the ER to ht eplasmodesmata (Zavaliev et al., 2016), the lipid raft mechanism has not been well revealed yet.
Prediction and Identification of GPI-APs in Arabidopsis
To identify GPI-APs, various bioinformatics tools were developed, generally depending on the prediction of a specific hydrophobic region at the C terminus. Examples are big-PI Plant Predictor (http://mendel.imp.ac.at/sat/gpi/gpi_server.html) (Eisenhaber et al., 1998), PredGPI (http://gpcr2.biocomp.unibo.it/gpipe/info.htm) (Pierleoni et al., 2008), GPI-SOM (http://gpi.unibe.ch/) (Fankhauser and Maser, 2005), and fragAnchor (Poisson et al., 2007). According to the latest genomic scanning by these tools, among lower and higher eukaryotes, about 0.21% to 2.01% of total proteins from diverse families are predicted to be modified by GPI moieties, and the percentage in Arabidopsis is 0.83% (Eisenhaber et al., 2001; Poisson et al., 2007). In the meantime, proteomic assays, which depend on cleavage from membranes by bacterial PI-PLC treatment in vitro and enrichment in particular membrane fractions, were performed to compare proteomic data to bioinformatic data. To date, more than 300 GPI-APs have been identified in Arabidopsis (Borner et al., 2002; Borner et al., 2003; Elortza et al., 2003; Bayer et al., 2006; Takahashi et al., 2016).
Arabidopsis GPI-APs identified in 2003 (Borner et al., 2003; Elortza et al., 2003) and 2016 (Takahashi et al., 2016) are assembled in Tables 1 and 2 , respectively, and their functions are discussed.
Table 1 A review of predicted GPI-APs updated from (Borner et al., 2003; Elortza et al., 2003).
Table 2 GPI-APs identified in 2016 that not included in previous study in 2003.
In Table 1, 248 genes predicted to encode GPI-APs in 2003 have been listed. Some corrections have been made, as some of them could not be found in databases or turned out to encode non-coding RNA. However, according to more recent experimental data, genes not included in 2003 also turned out to encode GPI-APs, such as At1g09460, At2g30933, At2g03505, and At4g13600 (Simpson et al., 2009), LORELEI (Tsukamoto et al., 2010), and XYP2 (Motose et al., 2004). Interestingly, due to recent achievements on alternative splicing, transcriptional variants of SKS3 (Zhou, 2019a) and CRK10 (Grojean and Downes, 2010) have been found to encode GPI-APs besides their ordinarily reported proteins (Figure 2). Alternative splicing largely enhanced the diversity of transcriptome and proteome, and more and more genes (up to 80% according to recent RNA-seq achievements) have been found to be alternatively spliced in Arabidopsis, which could greatly increase the abundance of GPI-APs (Wang et al., 2009; Filichkin et al., 2010; Severing et al., 2011; Reddy et al., 2013; Lee and Rio, 2015; Bush et al., 2017).
Figure 2 GPI-anchored SKS3 and CRK10 encoded by alternatively spliced transcriptional variants. (A) Alternative splicing of SKS3. (B) Alternative splicing of CRK10. ExD, extracellular domain; TM, transmembrane domain; KD, intracellular kinase domain. Exons are dark gray, introns are black lines, and untranslated transcribed regions are light gray.
In addition, 163 GPI-APs were predicted in 2016, and those not included in Table 1 are listed in Table 2. In this study, a large proportion of possible GPI-APs were discounted as typical GPI-APs in spite of being predicted to possess a GPI signal at the C terminus by various bioinformatics tools. Some of those discounted were transmembrane proteins, such as PIN3 and PIN4 and some receptor-like kinases (RLKs), and the other were cytoplasmic proteins without N-terminal secretory signal peptide, such as SNARE family proteins (listed at the end of Table 2).
Functional Diversity of GPI-APs in Arabidopsis
GPI-APs listed in Tables 1 and 2 are from diverse families, such as cell wall structure proteins, proteases, enzymes, receptor-like proteins (RLPs), lipid transfer proteins, and GPI-anchored peptides, which imply a functional diversity of GPI-APs: indeed, they were found functional in most processes, such as cell wall composition, cell wall component synthesis, cell polar expansion, stress responses, hormone signaling responses, pathogen responses, stomatal development, pollen tube elongation, and double fertilization in Arabidopsis.
Among these GPI-APs, the arabinogalactan protein (AGP) family, LORELEI family, COBRA family, and some RLPs, were better characterized. AGP family proteins are ubiquitous cell wall components anchoring on the plasma membrane throughout the Plant Kingdom and abundantly decorated at their Hyp residues by arabinogalactan polysaccharides, which make them be one of the most complex families of macromolecules in plants and play roles in various processes (Schultz et al., 2000; Ellis et al., 2010; Marzec et al., 2015; Showalter and Basu, 2016; Losada and Herrero, 2019; Palacio-Lopez et al., 2019). COBRA families were reported to be involved in various processes by regulating cell wall synthesis in plants (Hochholdinger et al., 2008; Cao et al., 2012; Niu et al., 2015; Niu et al., 2018). LORELEI family proteins associate with cell surface RLK, which is essential not only for ligand recognition but also for RLK transport (Capron et al., 2008; Duan et al., 2010; Tsukamoto et al., 2010; Meng et al., 2012; Yu et al., 2012; Li et al., 2015; Li et al., 2016; Liao et al., 2017; Stegmann et al., 2017; Feng et al., 2018; Guo et al., 2018; Yin et al., 2018).
Involvement of GPI-APs in Signaling Transduction in Arabidopsis
In Arabidopsis, hundreds of RLKs, which possess extracellular ligand recognition domains and intracellular kinase domains, control a wide range of processes, including development, disease resistance, hormone perception, and self-incompatibility (Shiu and Bleecker, 2001; Muschietti and Wengier, 2018; Wei and Li, 2018). Their association with extracellular ligands, including phytohormones, signaling polypeptides, and pathogen molecules, leads to the phosphorylation of the intracellular kinase domain, which consequently activate cytoplasmic signaling components and switch on response mechanisms (Figure 3A) (Pearce et al., 2001; Asai et al., 2002; Geldner and Robatzek, 2008; Murphy et al., 2012; Breiden and Simon, 2016; Yamaguchi et al., 2016; Chardin et al., 2017).
Figure 3 RLK-mediated signaling pathway and various associations between RLKs and GPI-APs. (A) Association with extracellular ligand activates and phosphorylates the intracellular kinase domain of RLK, which activates intracellular signaling components to regulate various processes. (B) GPI-AP is required for ligand recognition and its association with RLK. (C) GPI-AP is required not only for ligand recognition and its association with RLK but also for RLK localization by chaperoning its transport, and those un-chaperoned would reside in ER. (D) GPI-APs are required for ligand selection.
By summarizing the functional mechanism of those listed GPI-APs in Tables 1 and 2, a group of GPI-APs from various families was found to share a common mechanism of action involving RLK-related signal transduction (Table 3). The same mechanism has been reported in mammalian cells, for example, that GPI-anchored CD14 possessing leucine-rich repeats (LRR) region associates with not only Toll-like receptor TLR4 to perceive their polypeptide ligand lipopolysaccharide (LPS) leading them to activate mitogen-activated protein kinase (MAPK) cascades (Wright et al., 1990; Schumann, 1992; Zanoni et al., 2011; Li X. et al., 2015) but also TLR3 to perceive viral double-stranded RNA (dsRNA) leading them to activate (Vercammen et al., 2008). This common mechanism found in both animals and plants suggests that important and common roles are played by GPI-APs in signal transduction (Figure 3B).
Table 3 GPI-APs and their potential co-receptor RLKs and ligands.
Association Between GPI-AP and RLK
Interestingly, the association between GPI-AP and RLK could be involved in not only ligand recognition but also RLK transport and subcellular localization. One of the best characterized GPI-APs, LORELEI, not only participates in ligand recognition by associating with FERONIA but also plays a crucial role in chaperoning the transport of FERONIA from the ER to the plasma membrane (Capron et al., 2008; Duan et al., 2010; Tsukamoto et al., 2010; Meng et al., 2012; Yu et al., 2012; Li et al., 2015; Li et al., 2016; Liao et al., 2017; Stegmann et al., 2017; Feng et al., 2018; Guo et al., 2018; Yin et al., 2018) (Figure 3C). This special chaperone and transport mechanism might be due to the GPI-APs becoming involved with lipid rafts, which determine distinct protein sorting and protein traffic (Eisenhaber et al., 1998; Legler et al., 2005; Miyagawa-Yamaguchi et al., 2015; Sezgin et al., 2017).
GPI-APs appear to be important not only for ligand recognition but also essential for ligand selection. For example, RLK FERONIA recognizes ligands RALF1 or RALF22/23 when associated with GPI-anchored LORELEI or LRX5, respectively (Li C et al., 2015; Li et al., 2016; Zhao et al., 2018). This potential GPI-AP-dependent selection mechanism could greatly enhance the ligand recognition abundance of RLK but could also mediate the cross-talk between various signaling perception and transduction (Figure 3D).
The associations between GPI-AP and RLK could be structure independent, such as SKU5-TMK1, LRE/LLGs-FERONIA, FLA4-FEI1/FEI2, ENODL14-FERONIA, and LRX5-FERONIA, or structure dependent, such as TMM and ERECTA both possessing LRR structure at the extracellular domain and LYM1/LYM3 and CERK1 both possessing LyM structure at extracellular domain in Arabidopsis. Interestingly, the same structure dependence is also present in one of the best characterized GPI-APs in mammalian cells, CD-14, and together with its partner receptor kinases TLR3 and TLR4 all possess an LRR structure.
The structure-dependent associations between GPI-APs and RLKs largely increased the curiosities of the group of GPI-anchored RLPs, which shared the same structures or sequence similarities with RLKs but lack intracellular kinase domains. They might recognize specific RLKs depending on sequence and structure similarities and form heterodimers with various RLKs in the ER or Golgi bodies and then chaperone them to specific plasma membrane regions through GPI-AP-driven lipid rafts. On arrival, they select and recognize ligands and activate the intracellular signaling components.
Whether the GPI-anchored RLKs encoded by transcriptional variants, such as GPI-CRK10 and its variant of CRK10, can form homodimers based on the same extracellular domains and play a role in RLK regulation, is a very interesting question.
Conclusion and Perspectives
Previous genomic and proteomic assays that predicted and identified GPI-APs from Arabidopsis have been listed. Due to recent experimental data and knowledge of alternative splicing, more and more GPI-APs have been identified, suggesting that GPI-APs in Arabidopsis might be more abundant than we expected.
Previous studies on those listed GPI-APs from diverse families were discussed, and they were found to be involved in diverse biological processes, including cell wall composition, cell wall component synthesis, cell polar expansion, hormone signaling response, stress response, pathogen response, stomata development, pollen tube elongation, and double fertilization. Those reports demonstrated the functional diversity and indispensability of GPI-APs in Arabidopsis.
Among these reports, direct associations were found between various GPI-APs and their partner cell surface RLKs, demonstrating not only participation in their ligand recognition but also essential roles in RLK transport and localization. Localization might due to specific protein sorting and protein traffic driven by GPI-AP-related lipid rafts. Surprisingly, GPI-APs have also been shown to participate in ligand selection, which made one RLK and its downstream intracellular target activated by various ligands. Such protein cross-reactivity greatly enhanced the ligand recognition abundance of RLKs, which can also be considered as a common mechanism of cross-talk between various ligands or various signaling pathways.
In this review, the most predicted or identified GPI-APs in Arabidopsis were listed and discussed, and a common involvement of them in signing transduction was summarized. This involvement could be very helpful for understanding the ligand-RLK signaling transduction in plants, especially for understanding the polar localization of RLKs, and the crosstalk between various ligand-RLK signaling transduction. It would be interesting to identify more associations between various GPI-APs and RLKs and study their recognition and selection of ligands and downstream intracellular signaling components in Arabidopsis.
Author Contributions
KZ wrote this manuscript.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Keywords: glycosylphosphatidylinositol (GPI), GPI-anchored protein (GPI-AP), receptor-like kinase (RLK), ligand, signaling transduction
Citation: Zhou K (2019) Glycosylphosphatidylinositol-Anchored Proteins in Arabidopsis and One of Their Common Roles in Signaling Transduction. Front. Plant Sci. 10:1022. doi: 10.3389/fpls.2019.01022
Received: 06 May 2019; Accepted: 22 July 2019;
Published: 29 August 2019.
Edited by:
Els JM Van Damme, Ghent University, BelgiumReviewed by:
Daisuke Takahashi, Max Planck Institute of Molecular Plant Physiology, GermanyHiroyasu Motose, Okayama University, Japan
Copyright © 2019 Zhou. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Ke Zhou, zhouke0525@gmail.com