REVIEW article

Front. Plant Sci., 29 August 2019

Sec. Plant Physiology

Volume 10 - 2019 | https://doi.org/10.3389/fpls.2019.01022

Glycosylphosphatidylinositol-Anchored Proteins in Arabidopsis and One of Their Common Roles in Signaling Transduction

  • FAFU-UCR Joint Center for Horticultural Biology and Metabolomics, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China

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Abstract

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

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

GroupSub-groupTotalGene No.NameDescriptions
AGPClassical AGP17At1g68725AGP19AGP17-19 encode a subclass of lysine-rich AGPs, among which AGP18 was reported to be essential for the initiation of female gametogenesis both at the sporophytic and gametophytic levels, and AGP19 functions in cell division and expansion (Acosta-Garcia and Vielle-Calzada, 2004; Sun et al., 2005; Yang et al., 2007; Yang et al., 2011; Zhang et al., 2011a; Zhang et al., 2011b).
At4g37450AGP18
At2g23130AGP17
At5g14380AGP6AGP6 and AGP10 are co-expressed and co-localized in pollen grains and pollen tubes and essential for pollen grain development and pollen early germination, possibly because they are essential components of the nexine layer in pollen cell wall (Levitin et al., 2008; Coimbra et al., 2009; Coimbra et al., 2010; Costa et al., 2013; Palareti et al., 2016).
At4g09030AGP10
At3g01700AGP11Its GPI modification has been experimentally confirmed, but its function has not been characterized yet (Schultz et al., 2000).
At5g64310AGP1
At2g22470AGP2
At4g40090*AGP3Shown as At4g40091 in Borner et al. (2003).
At5g10430AGP4/JAGGEREssential for the degeneration of synergid cells, which guide the pollen tube attraction after acceptance of the unique pollen tube, and for prohibition of polytubey (Pereira et al., 2016a; Pereira et al., 2016b).
At1g35230AGP5
At5g65390AGP7
At2g14890AGP9
At5g18690AGP25
At2g47930AGP26
At3g06360AGP27
At4g16980*Shown as At4g16985 in Borner et al. (2003).
AG peptides (Schultz et al., 2004), a group of GPI-anchored arabinogalactan polypeptides12At3g13520AGP12
At4g26320AGP13
At5g56540AGP14AGP14 and At3g01730 regulate root hair elongation exhibiting environmental response behavior, potentially by controlling root hair cell wall synthesis (Lin et al., 2011).
At3g01730
At5g11740AGP15
At2g46330AGP16
At3g61640AGP20
At1g55330AGP21
At5g53250AGP22
At3g57690AGP23
At5g40730AGP24
At3g20865AGP40
FLAs (fasciclin-like AGPs)16At5g55730FLA1Involved in lateral root initiation and shoot regeneration potentially by regulating cell-type specification (Johnson et al., 2011).
At4g12730FLA2
At2g24450FLA3Specifically expressed in pollen grains and tubes and involved in microspore development potentially through the regulation of cellulose deposition (Li et al., 2010).
At3g46550FLA4/SOS5Directly associates with cell wall RLKs FEI1/2 to perceive environmental stimuli in apoplast by altering its conformation and association with FEI1/2. This complex could regulate cell wall synthesis and composition by collaborating with CESA5. Interestingly, this regulation could also be controlled by ethylene and ABA with unclear mechanism. Surprisingly, the absence of GPI anchors only affected their PM localization but not their function (Harpaz-Saad et al., 2012; Seifert et al., 2014; Basu et al., 2016; Griffiths et al., 2016; Xue et al., 2017; Turupcu et al., 2018).
At4g31370FLA5
At2g20520FLA6
At2g04780FLA7
At2g45470FLA8/AGP8
At1g03870FLA9Response to drought stress in maize and Arabidopsis (Cagnola et al., 2018).
At3g60900FLA10
At5g03170FLA11FLA11 and FLA12 affect cellulose deposition and formation of secondary cell wall composition (Ito et al., 2005; MacMillan et al., 2010).
At5g60490FLA12
At5g44130FLA13
At3g12660FLA14
At1g30800
At4g12950
Extensin relatedExtensin related7At1g02405Proline-rich protein
Proline-rich protein
Proline-rich protein
Proline-rich protein
At1g70990
At4g16140
At5g11990
At3g06750Hydroxyproline-rich glycoprotein family protein
Hydroxyproline-rich glycoprotein family protein
At1g23040
At5g49280Hydroxyproline-rich glycoprotein family protein
Phytocyanins (Nersissian et al., 1998)Stellacyanin like (Hart et al., 1996)4At5g20230BCB/SAG14Regulates lignin biosynthesis induced by oxidative stress (Ezaki et al., 2005; Kim et al., 2011; Ji et al., 2015; Tang et al., 2016).
At2g31050Copredoxin superfamily protein
Copredoxin superfamily protein
At2g26720
At5g26330Copredoxin superfamily protein
Uclacyanin like8At1g22480Copredoxin superfamily protein
At1g72230Copredoxin superfamily protein
At3g27200Copredoxin superfamily protein
At2g32300UCC1UCC1, UCC2 and UCC3 encode copper binding proteins (Nersissian et al., 1998).
At2g44790UCC2
At3g60280UCC3
At3g60270Copredoxin superfamily protein
At5g07475Copredoxin superfamily protein
ENODL (early nodulin like)17At5g53870ENODL1
At4g27520ENODL2Catalyzes the formation of pyroglutamic acid at the N-terminus of several peptides and proteins (Schilling et al., 2007).
At4g28365ENODL3
At4g32490ENODL4
At3g18590ENODL5
At1g48940ENODL6
At1g79800ENODL7
At1g64640*ENODL8Classified as unknown/hypothetical in Borner et al. (2003).
At3g20570ENODL9Involved in starch mobilization and reproductive progresses (Khan et al., 2007).
At2g23990ENODL11
At4g30590ENODL12
At5g25090ENODL13
At2g25060ENODL14ENODL14 and ENODL15 directly interact with RLK FERONIA and regulate maternally controlled male-female communication and fertilization (Escobar-Restrepo et al., 2007; Hou et al., 2016).
At4g31840ENODL15
At3g01070ENODL16
At5g15350ENODL17
At1g08500ENODL18
COBRA familyCOBRA family [all 12 COBRA members, except COBL5, was predicted to be GPI-AP (Roudier et al., 2002)]10At5g60920COBRA/COBLocalizes on plasma membrane polarly and regulates cell wall biosynthesis and cellulose microfibrils in Arabidopsis and tomato (Schindelman et al., 2001; Roudier et al., 2005). Its regulation responses to various stresses potentially by involving in jasmonic acid-related signaling pathway (Ko et al., 2006; Dinneny et al., 2008; Sorek et al., 2015).
At3g02210COBL1
At3g29810COBL2Plays a role in the deposition of crystalline cellulose in secondary cell wall structures during seed coat epidermal cell differentiation, and the regulation is independent of the FEI-SOS pathway (Ben-Tov et al., 2015; Ben-Tov et al., 2018).
At5g15630COBL4/IRX6Participates in regulating secondary cell wall biosynthesis (Taylor-Teeples et al., 2015; Niu et al., 2018).
At1g09790COBL6
At3g16860COBL8
At3g20580COBL10Crucial for pollen tube directional growth by affecting the deposition of the apical pectin cap and cellulose microfibrils of pollen tubes and might also be involved in male-female communications (Li et al., 2013).
At4g16120COBL7/SEB1
At4g27110COBL11
At5g49270COBL9/DER9/SHV2Involved in ethylene and auxin controlled root hair development (Parker et al., 2000; Ringli et al., 2005; Jones et al., 2006).
GPDL glycerophosphodiester phosphodiesterase like (GDPD-like) family (Cheng et al., 2011)6At1g66970GDPDL1/SHV3-Like2/SVL2Homologue of the extracellular domain of RLK GDPDL2/AT1g66980. Possesses the capacity to hydrolyze glycerophosphodiesters, which is stimulated by Ca2+ in Arabidopsis, and plays an important role in various physiological processes (Cheng et al., 2011).
At3g20520GDPDL5
At4g26690GDPDL3/SHV3SHV3 and GDPDL4 are involved in primary cell wall organization, which regulates cell polar expansion by coordinating proton pumping and cellulose synthesis (Parker et al., 2000; Hayashi et al., 2008; Yeats and Somerville, 2016; Yeats et al., 2016).
At5g55480GDPDL4/SVL1
At5g58050GDPDL6/SVL4
At5g58170GDPDL7/SVL5
HIPL3At1g74790
At5g39970
At5g62630HIPL2
β-1,3 Glucanas-es31At1g11830**Does not existShown in Borner et al. (2003) but could not be found in databases
At1g26450Carbohydrate-binding X8 domain superfamily protein
At1g64760ZERZAUST, ZETRequired for cell wall organization during tissue morphogenesis potentially by being mediated by RLKs. Interestingly, the presence of GPI anchor is dispensable for its function (Fulton et al., 2009; Vaddepalli et al., 2017; Vaddepalli et al., 2019).
At2g19440ZETHHomolog of ZET and works redundantly with ZET (Vaddepalli et al., 2019).
At1g32860Glycosyl hydrolase superfamily protein
At1g77780Glycosyl hydrolase superfamily protein
At2g26600Glycosyl hydrolase superfamily protein
At3g15800Glycosyl hydrolase superfamily protein
At1g66250O-Glycosyl hydrolase family 17 protein
At2g01630O-Glycosyl hydrolase family 17 protein
At3g04010O-Glycosyl hydrolase family 17 protein
At3g13560O-Glycosyl hydrolase family 17 protein
At3g24330O-Glycosyl hydrolase family 17 protein
At4g29360O-Glycosyl hydrolase family 17 protein
At4g31140O-Glycosyl hydrolase family 17 protein
At5g18220O-Glycosyl hydrolase family 17 protein
At5g20870O-Glycosyl hydrolase family 17 protein
At5g42720O-Glycosyl hydrolase family 17 protein
At5g56590O-Glycosyl hydrolase family 17 protein
At5g58090O-Glycosyl hydrolase family 17 protein
At5g58480O-Glycosyl hydrolase family 17 protein
At5g64790O-Glycosyl hydrolase family 17 protein
At5g42100BG_PPAPRegulates the gating of plasmodesmata and the palsmodesmatal transport through plasmodesmal callose degradation (Zavaliev et al., 2016).
At5g61130PDCB1PCDB1-PDCB3, At1g69295, and At3g58100 encode a subgroup of X8-domian containing GPI-APs, which localize to the plasmodesmata and predicted to bind callose (Simpson et al., 2009; Zavaliev et al., 2016).
At5g08000PDCB2
At1g18650PDCB3
At1g69295
At3g58100
At1g09460***At1g09460, At2g30933, At2g03505, and At4g13600 encode a subgroup of X8-domain-containing GPI-APs (Simpson et al., 2009) but not included in Borner et al. (2003).
At2g30933***
At2g03505***
At4g13600***
Polygalacturonase1At3g15720Pectin lyase-like superfamily protein
Pectate lyases3At3g53190Pectin lyase-like superfamily protein
At3g54920PMR6Required for fungal infection progress and effects cell wall composition through pectin synthesis (Vogel et al., 2002; Vogel et al., 2004).
At5g04310Pectin lyase-like superfamily protein
ProteasesAspartyl proteases10At1g05840
At1g08210
At5g36260A36A36 and A39 co-localize with GPI-anchored COBL10 and involved in pollen tube germination, vitality, and pollen tube guidance (Gao et al., 2017; Gao et al., 2017).
At1g65240A39
At2g17760
At3g02740
At3g51330
At3g51350
At4g35880
At5g10080
Metalloproteases5At1g24140AT3-MMPThis subgroup of proteases contribute to the MAMP-triggered callose deposition in response to the bacterial flagellin peptide flg22, which suggests their involvement in the pattern-triggered immunity in interactions with necrotrophic and biotrophic pathogen (Zhao et al., 2017).
At1g59970AT5-MMP
At1g70170AT2-MMP
At2g45040AT4-MMP
At4g16640AT1-MMP
Cys proteases1At3g43960Regulates root hair elongation (Lin et al., 2011).
LTPL (lipid transfer-like protein)26At1g05450
At1g18280LTPG3
At1g27950LTPG1/LTPGLTPG1, LTPG2, LTPG5, and LPTG6 are involved in cuticular wax export or accumulation in epidermal cells and during pathogen defense (Debono et al., 2009; Kim et al., 2012; Guo et al., 2013; Edstam and Edqvist, 2014; Fahlberg et al., 2019).
At3g43720LTPG2
At3g22600LTPG5
At1g55260LTPG6
At1g62790
At1g73890
At2g13830
At2g27130
At2g44290
At2g44300
At2g48130LTPG15Involved in suberin monomer export in seed coats (Lee and Suh, 2018).
At2g48140EDA4
At1g36150
At3g22611**Does not existShown in Borner et al. (2003) but could not be found in databases.
At3g58550
At4g08670LTPG4
At4g12360
At4g14805
At4g14815
At4g22630
At4g22640
At5g09370
At5g13900
At5g64080XYP1XYP1 and XYP2 function as mediators of inductive cell-cell interaction in vascular development (Motose et al., 2004). XYP2 was not shown in (Borner et al., 2003) due to its alternative splicing.
At2g13820***XYP2
SKU5-Similar family4At4g12420SKU5SKU5 is involved in root directional growth (Sedbrook et al., 2002), and this group of genes is redundantly essential for root development by regulating cell polar expansion and cell wall synthesis (Zhou, 2019a, Zhou, 2019b). SKS3 was not shown in Borner et al. (2003) due to alternative splicing.
At4g25240SKS1
At5g51480SKS2
At5g48450***SKS3
RLPRLK3 like (DUF26)5At1g63550This subgroup of RLPs homolog with the extracellular region of a group of cysteine-rich RLKs (CRKs).
At1g63580
At5g41280
At5g41290
At5g41300
PRK5 like3At1g20030This subgroup of pathogenesis-related thaumatin superfamily proteins are similar with the extracellular region of an osmotin/thaumatin-like protein kinase PR5K (PR5-like receptor kinase) (Wang et al., 1996; Abdin et al., 2011).
At4g36010
At4g38660
Lectin like1At1g07460Homologue of L-type lectin receptor kinase III, 1 (LECRK-III, 1)
LysM domains3At1g21880LYM1/LYP2LYM1 and LYM3 physically interact with the major components of bacterial cell walls and peptidoglycans and work together with a LysM RLK CERK1 to mediate perception and immunity to infection (Willmann et al., 2011).
At1g77630LYM3/LYP3
At2g17120LYM2/LYP1
Cf-2/Cf-5 like3At1g80080ATRLP17/TMMForms various complexes with different transmembrane RLKs from ERECTA family (ERf) and/or SERKs to recognize their ligands, such as epidermal patterning factors (EPFs) and CHAL, and then to regulate stomatal development and immune response through the activation of intracellular MAPK cascade (Bundy et al., 2016; Abrash and Bergmann, 2010; Geisler et al., 2000; Geisler et al., 1998; Jakoby et al., 2006; Jorda et al., 2016; Kobe and Kajava, 2001; Lee et al., 2015; Lee et al., 2012; Lin et al., 2017; Meng et al., 2015; Rasmussen et al., 2011; Wang et al., 2008; Yan et al., 2014; Bhave et al., 2009).
At2g42800ATRLP29
At4g28560RIC7Interacts with a component of the vesicle trafficking machinery and acts as its linker with ROP2 (Jeon et al., 2008; Xu et al., 2010; Hwang et al., 2011; Hong et al., 2016). However, the presence of its GPI anchoring is doubted (Jeon et al., 2008; Yeats et al., 2018).
Other1At1g10375**Does not existShown in Borner et al. (2003) but could not be found in databases.
At4g23180***Encoded by an alternative variant of CRK10, which was believed to encode a cysteine-rich RLK (Grojean and Downes, 2010). Not shown in Borner et al. (2003) due to alternative splicing.
GPI-anchored peptidesGPI-anchored peptides8At3g01940
At3g01950
At5g14110
At5g40960
At5g40970
At5g40980AT.I.24-6
At5g50660
At5g63500
LORELEI-like family4AT4g26466***LORELEILLG1 chaperones transmembrane RLK FERONIA from the ER to the plasma membrane, where both LORELEI and LLG1 could associate with FERONIA to recognize extracellular ligands to regulate sperm cell release during double fertilization and early seed development (Capron et al., 2008; Duan et al., 2010; Tsukamoto et al., 2010; Meng et al., 2012; Yu et al., 2012; Li C 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). Interestingly, LLG1 was also reported to associate with RLK FLS2 and medicate PAMP recognition (Shen et al., 2017). LORELEI was not shown in Borner et al. (2003).
At2g20700LLG2
At4g28280LLG3
At5g56170LLG1
PLC-like phosphodiesterases1At5g67130*Regulates gametophytic self-incompatibility (Qu et al., 2017). Shown as At5g67131 in Borner et al. (2003).
Other6At5g07190SEED GENE 3
At5g62200ATS3B
At5g62210ATS3
At3g07390
At1g24520BCP1Active in both diploid tapetum and haploid microspores and required for pollen fertility (Theerakulpisut et al., 1991; Xu et al., 1995; Luo et al., 2000).
At4g15460A glycine-rich protein
Unknown/hypothetical33At1g54860Identified in oil bodies purified from Arabidopsis seeds (Jolivet et al., 2004).
At3g06035
At5g19230
At5g19250
At1g07135A glycine-rich protein
At1g09175
At3g04640A glycine-rich protein
At3g55790
At1g29980
At2g34510
At5g14150
At3g18050
At4g28100
At3g27410
At5g40620
At1g23050
At1g70985Hydroxyproline-rich glycoprotein family protein
At5g26290RAMCAPInvolved in both male and female gametophytic development (Singh et al., 2017).
At5g26300TRAF-like protein
At3g24518**Natural antisense transcript overlaps with AT3G24520
At5g35890β-galactosidase-related protein
At1g21090Cupredoxin superfamily protein
At1g56320
At1g61900
At2g28410
At2g29660Zinc finger (C2H2-type) family protein
At3g26110Anther-specific protein agp1-like protein
At3g44100MD-2-related lipid recognition domain-containing protein
At3g58890RNI-like superfamily protein
At3g61980KPI-1Putative Kazal-type serine proteinase inhibitor, which is supposed to limit and control the spread of serine proteinase activity, and function during defense mechanism (Pariani et al., 2016).
At4g14746Neurogenic locus notch-like protein
At4g28085
At4g38140RING/U-box superfamily protein
At5g08210**MIR834AEncoded a microRNA of unknown function
At5g14190**Does not existShown in Borner et al. (2003) but could not be found in genomic or proteomic database actually
At5g16670**Does not existShown in Borner et al. (2003) but could not be found in genomic or proteomic database actually
At5g22430Pollen Olee 1 allergen and extensin family protein

A review of predicted GPI-APs updated from (Borner et al., 2003; Elortza et al., 2003).

*Shown incorrectly in Borner et al. (2003).

**Shown in Borner et al. (2003) but does not exist in genomic or proteomic database or encodes non-coding RNA.

***Not shown in Borner et al. (2003) but could be predicted or studied as GPI-APs.

Table 2

GroupSub-groupTotalGene No.NameDescriptions
LTPL (lipid transfer protein)3AT3g22620
AT2g13820XYP2Functions as a mediator of inductive cell-cell interaction in vascular development (Motose et al., 2004).
AT4g22505Bifunctional inhibitor/lipid-transfer protein/seed storage 2S albumin superfamily protein
β-1,3 Glucanases3AT1g11820O-Glycosyl hydrolase family 17 protein
AT4g34480O-Glycosyl hydrolase family 17 protein
AT3g57240
PLC-like phosphodiesterases1AT4g36945
RLP2AT3g17350Wall-associated kinase family protein
AT4g18760RLP51/SNC2Functions upstream of ankyrin-repeat transmembrane protein BDA1 to regulate plant immunity through transcriptional factor WRKY70 (Zhang et al., 2010; Yang et al., 2012).
Oligogalacturonide oxidase 2AT5g66680DGL1Subunit of the oligosaccharyltransferase complex, which catalyzes N-glycosylation of nascent secretory polypeptides in the lumen of the ER (Lerouxel et al., 2005; Qin et al., 2013; Jeong et al., 2018).
AT4g20830ATBBE20/OGOX1Required in plant immunity (Benedetti et al., 2018).
β-Glucuronidase2AT5g07830GUS2Contributes to the glycosylation of AGPs (Eudes et al., 2008).
AT5g34940GUS3
LRR extensin1AT4g18670LRX5Physically associates with RALF peptides RALF22/23, which activate FERONIA and transduce extracellular signals to regulate plant growth and salt stress tolerance (Zhao et al., 2018).
AGP1AT1g28290AGP31Involved in cell wall structure and network (Hijazi et al., 2014).
Expansin1AT1g69530EXPA1Regulates stomatal opening by altering the structure of the guard cell wall (Wei et al., 2011; Zhang et al., 2011c).
PME and PMEI proteinsPME (pectin methylesterase)1AT3g14310PME3Catalyzes the demethylesterification of pectin homogalacturonan domains in plant cell walls, and its activity could be regulated by PMEIs (Guenin et al., 2011; Senechal et al., 2015).
PMEI
(pectin methylesterase inhibitors)		5AT2g31430PMEI5A pectin methylesterase inhibitor (Muller et al., 2013).
AT5g62360PMEI13Regulates root growth under cold and salt stresses (Chen et al., 2018).
AT3g62820Plant invertase/PMEI Inhibitor superfamily protein
AT3g17130Plant invertase/PMEI inhibitor superfamily protein
AT5g62350Plant invertase/PMEI inhibitor superfamily protein
GDSL motif esterase/acyltransferase/lipase4AT4g30140CDEF1Possesses esterase activity and candidates for the unidentified plant cutinase for cutile biosynthesis (Takahashi et al., 2010).
AT5g45950GDSL-motif esterase/acyltransferase/lipase
AT4g01130GDSL-motif esterase/acyltransferase/lipase
AT3g16370GDSL-motif esterase/acyltransferase/lipase
Proteases3AT1g30600Subtilisin-like serine protease
AT4g21650SBT3.13Subtilisin-like serine protease
AT3g61820Eukaryotic aspartyl protease family protein
Others25AT2g30700
AT1g65870Disease resistance responsive
AT5g42370Calcineurin-like metallophosphoesterase superfamily protein
AT2g03530UPS2Mediates high-affinity uracil and 5-fluorouracil (a toxic uracil analogue) transport (Schmidt et al., 2004).
AT1g72610GLP1Localizes to the extracellular matrix and being considered to be involved in many physiological responses including environmental stress (Membre et al., 2000).
AT5g19240Glycoprotein membrane precursor GPI anchored
AT5g04885BGLC3Possesses β-glucosidases activity and works redundantly with its homolog BGLC1 with absent GPI anchor to remove unsubstituted Glc residues from the nonreducing end of xyloglucan molecule (Sampedro et al., 2017).
AT3g05910PAE12Pectin acetyesterase 12
AT3g47800Galactose mutarotase-like superfamily protein
AT5g55750Hydroxyproline-rich glycoprotein family protein
AT3g53010Carbohydrate esterase
AT4g29520SES1ER localized molecular chaperone and required for heat tolerance (Guan et al., 2019).
AT3g07570Cytochrome B561
AT1g75680GH9B7Glycosyl hydrolase
AT5g14030Translocon-associated protein beta unit (TRAPB)
AT3g29360UGD2Products UDP-glucuronic acid, which is the common precursor for arabinose, xylose, galacturonic acid, and apiose residues in cell wall biosynthesis (Reboul et al., 2011; Siddique et al., 2012).
AT5g64620C/VIF2Inhabits both plant cell wall invertase and vacuolar invertase (Link et al., 2004).
AT1g68560XYL1Releases xylosyl residues from xyloglucan oligosaccharides at the non-reducing end, which alters xyloglucan composition and results in growth defects (Sampedro et al., 2010; Gunl and Pauly, 2011).
AT4g34180CYCLASE1A negative regulator of cell death and regulates pathogen-induced symptom development in Arabidopsis (Smith et al., 2015).
AT4g35220CYCLASE2
AT5g08260SCPL35Serine carboxypeptidase-like 35
AT2g33530SCPL46
AT5g43600AAH-2/UAHIts allantoate amidohydrolases enzymatic activity is required for nitrogen recycling from purine ring in plants (Werner et al., 2008).
AT4g15630CASPL1E1
AT4g15620CASPL1E2
Not typical GPI-Aps
Transmembrane protein with predicted omega domain at C terminus8AT4g02420
AT1g53210
AT1g55910ZIP11
AT3g48200
AT1g42470ATNPC1-1
AT1g70940PIN3Auxin efflux carrier family protein
AT2g01420PIN4Auxin efflux carrier family protein
AT5g55960
Predicted cytosol protein without signal peptide at N terminus13AT1g65820Microsomal glutathione S-transferase
AT2g45140PVA12
AT2g32240PICC
AT5g22780AP-2Adaptin family protein
AT4g11380
AT5g22770AP2A1
AT3g27570 AT1g06530PMD2Sucrase/ferredoxin-like family protein
AT1g22882SUN3
AT4g32150
AT5g11150		VAMP711
VAMP713		VAMP711 and VAMP713 are SNARE family proteins that regulate endomembrane trafficking (Leshem et al., 2010; Ichikawa et al., 2015; Xue et al., 2018).
AT1g16240SYP51A SNARE family protein that interacts with aquaporin and regulates post-Golgi traffic and vacuolar sorting (De Benedictis et al., 2013; Barozzi et al., 2018).
AT5g16830PEP12/SYP21A SNARE family protein involved in protein sorting and plant development (Foresti et al., 2006; Silady et al., 2008; Shirakawa et al., 2010; Touihri et al., 2011).
AT5g46860SGR3/SYP22A SNARE family protein
Transmembrane RLKs3AT5g48380BIR1Functions as a negative regulator of basal immunity and cell death in Arabidopsis (Liu et al., 2016).
ATIg51940LYK3Regulates the cross-talk between immunity and abscisic acid responses (Paparella et al., 2014).
AT1g63430Transmembrane RLK

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

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

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-APsCo-receptor RLKsLigandsIntracellular signaling components
PlantsSKU5TMK1ABP1ROP GTPase (Shimomura, 2006; Xu et al., 2014)*
LRE/LLGsFERONIARALF1RopGEFs-RAC/ROPs (Li et al., 2015; Li et al., 2016; Stegmann et al., 2017)
FLA4FEI1/FEI2UnidentifiedUnidentified (Seifert et al., 2014; Basu et al., 2016; Griffiths et al., 2016; Xue et al., 2017; Turupcu et al., 2018)
ENODL14FERONIAUnidentifiedUnidentified (Escobar-Restrepo et al., 2007; Hou et al., 2016)
LRX5FERONIA RALF22/23RopGEFs-RAC/ROPs (Zhao et al., 2018)
TMMERfEPFsMAPK (Geisler et al., 1998; Geisler et al., 2000; Kobe and Kajava, 2001; Jakoby et al., 2006; Wang et al., 2008; Bhave et al., 2009; Abrash and Bergmann, 2010; Rasmussen et al., 2011; Lee et al., 2012; Yan et al., 2014; Lee et al., 2015; Meng et al., 2015; Bundy et al., 2016; Jorda et al., 2016; Lin et al., 2017)
LYM1/LYM3CERK1PeptidoglycansUnidentified (Willmann et al., 2011)
LLG1FLS2flg22Heterotrimeric G proteins (Liang et al., 2016; Shen et al., 2017)
MammalsCD14TLR4LPSMAPK (Wright et al., 1990; Schumann, 1992; Zanoni et al., 2011; Li et al., 2015)
CD14TLR3Viral dsRNALipid kinase PI3K (Vercammen et al., 2008)

GPI-APs and their potential co-receptor RLKs and ligands.

*Both SKU5 and TMK1 were identified through their association with ABP1, but no direct association has been identified between TMK1 and SKU5.

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.

Statements

Author contributions

KZ wrote this manuscript.

Conflict of interest

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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Summary

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

Volume

10 - 2019

Edited by

Els JM Van Damme, Ghent University, Belgium

Reviewed by

Daisuke Takahashi, Max Planck Institute of Molecular Plant Physiology, Germany; Hiroyasu Motose, Okayama University, Japan

Updates

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,

This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

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All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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