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Bridging the GAPs in plant reproduction: a comparison of plant and animal GPI-anchored proteins

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Abstract

Key message

Glycosylphosphatidylinositol (GPI)-anchored proteins (GAPs) are a unique type of membrane-associated proteins in eukaryotes. GPI and GAP biogenesis and function have been well studied in non-plant models and play an important role in the fertility of mouse sperm and egg. Although GPI and GAP biogenesis and function in plants are less known, they are critical for flowering plant reproduction because of their essential roles in the fertility of the male and female gametophytes.

Abstract

In Eukaryotes, GPI, a glycolipid molecule, can be post-translationally attached to proteins to serve as an anchor in the plasma membrane. GPI-anchoring, compared to other modes of membrane attachment and lipidation processes, localizes proteins to the extracellular portion of the plasma membrane and confers several unique attributes including specialized sorting during secretion, molecular painting onto membranes, and enzyme-mediated release of protein through anchor cleavage. While the biosynthesis, structure, and role of GPI are mostly studied in mammals, yeast and protists, the function of GPI and GAPs in plants is being discovered, particularly in gametophyte development and function. Here, we review GPI biosynthesis, protein attachment, and remodeling in plants with insights about this process in mammals. Additionally, we summarize the reproductive phenotypes of all loss of function mutations in Arabidopsis GPI biosynthesis and GAP genes and compare these to the reproductive phenotypes seen in mice to serve as a framework to identify gaps in our understanding of plant GPI and GAPs. In addition, we present an analysis on the gametophyte expression of all Arabidopsis GAPs to assist in further research on the role of GPI and GAPs in all aspects of the gametophyte generation in the life cycle of a plant.

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Acknowledgements

This research was supported by an NSF grant to R.P. (IOS-1146090) and the Boynton Graduate Fellowship in Plant Molecular Biology, School of Plant Sciences, University of Arizona and University of Arizona Graduate Professional Student Council to N.D. We thank Dr. Taroh Kinoshita, Osaka University, Japan, for discussions and comments on GPI biology, and critical reading of the manuscript.

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  1. Nicholas Desnoyer

    Present address: Department of Plant and Microbial Biology, University of Zurich, Zollikerstrasse 107, CH-8008, Zurich, Switzerland

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  1. School of Plant Sciences, University of Arizona, Tucson, AZ, 85721, USA

    Nicholas Desnoyer & Ravishankar Palanivelu

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  1. Nicholas Desnoyer
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ND analyzed the data and prepared the figures. ND and RP conceived and wrote the manuscript.

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Correspondence to Ravishankar Palanivelu.

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Communicated by Thomas Dresselhaus.

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Supplementary Fig. 1

. Protein sequence analysis of PIGK, GPI8, and AtGPI8 proteins. a Multiple alignment of Homo sapiens PIGK, Saccharomyces cerevisiae GPI8, and Arabidopsis AtGPI8 (AT1G08750) using Clustal Omega and visualization using BOXSHADE 3.2. H. sapiens Cys92 is boxed in red and forms a functionally important and conserved disulfide bond with PIGT Cys182 (Ohishi et al. 2003). Asterisks indicate conserved residues in the catalytic dyad (Gamage and Hendrickson 2013). Identical residues are colored black and similar residues are colored gray. b Amino acid sequences from Arabidopsis AtGPI8 (388AA, 0-TM), H. sapiens PIGK (395AA, 1-TM), and S. cerevisiae GPI8 (411AA, 1-TM) analyzed in the TMHMM Server v. 2.0 for the presence and location of transmembrane helices. c Clustal Omega amino acid sequence alignment scores for Arabidopsis AtGPI8, H. sapiens PIGK, and S. cerevisiae GPI8. Similarity percentage was calculated using Blosum62 matrix with a threshold of >1. (TIF 797 kb)

Supplementary Fig. 2

. Protein sequence analysis of PIGT, GPI16, and AtPIGT proteins. a Multiple alignment of Saccharomyces cerevisiae GPI16, Arabidopsis AtPIGT (AT3G07140), and Homo sapiens PIGT amino acid sequences using Clustal Omega and visualization using BOXSHADE 3.2. Identical residues are colored black and similar residues are colored gray. H. sapiens Cys182 is boxed in red and forms a functionally important and conserved disulfide bond with GPI8/PIGK Cys92 (Ohishi et al. 2003). b Amino acid sequences of Arabidopsis AtPIGT (643AA, 1-TM), H. sapiens PIGT (578AA, 1-TM), and S. cerevisiae GPI16 (610AA, 1-TM) analyzed in the TMHMM Server v. 2.0 for the presence and location of transmembrane helices. c Clustal Omega amino acid sequence alignment scores for Arabidopsis AtPIGT, H. sapiens PIGT, and S. cerevisiae GPI16. Similarity percentage was calculated using Blosum62 matrix with a threshold of >1. (TIF 1156 kb)

Supplementary Fig. 3

. Protein sequence alignment of GAB1, PIGU, AtPIGU1, and AtPIGU2 proteins. a Multiple alignment of Saccharomyces cerevisiae GAB1, Homo sapiens PIGU, and Arabidopsis AtPIGU1 (AT1G63110) and AtPIGU2 (AT1G12730) amino acid sequences using Clustal Omega and visualization using BOXSHADE 3.2. Identical residues are colored black and similar residues are colored gray. Red box refers to the conserved 21 amino acid region described in (Hong et al. 2003). b Amino acid sequences of Arabidopsis AtPIGU1 (At1G63110; 397AA, 7-TM), AtPIGU2 (At1G12730; 474AA, 10-TM), H. sapiens PIGU (437AA, 9-TM), and S. cerevisiae GAB1 (396AA, 8-TM) analyzed in the TMHMM Server v. 2.0 for the presence and location of transmembrane helices. c Clustal Omega amino acid sequence alignment scores for Arabidopsis AtPIGU1 and AtPIGU2, H. sapiens PIGU, and S. cerevisiae GAB1. Similarity percentage was calculated using Blosum62 matrix with a threshold of >1. (TIF 4006 kb)

Supplementary Fig. 4

. Protein sequence analysis of GAA1, AtGAA1, and GPAA1 proteins. a Multiple alignment of Saccharomyces cerevisiae GAA1, Arabidopsis AtGAA1 (AT5G19130), and Homo sapiens GPAA1 amino acid sequences using Clustal Omega and visualization using BOXSHADE 3.2. Identical residues are colored black and similar residues are colored gray. b Amino acid sequences from Arabidopsis AtGAA1 (699AA, 6-TM), H. sapiens GPAA1 (621AA, 7-TM), and S. cerevisiae GAA1 (614AA, 6-TM) analyzed in the TMHMM Server v. 2.0 for the presence and location of transmembrane helices. c Clustal Omega amino acid sequence alignment scores for Arabidopsis AtGAA1, H. sapiens GPAA1, and S. cerevisiae GAA1. Similarity percentage was calculated using Blosum62 matrix with a threshold of >1. (TIF 1372 kb)

Supplementary Fig. 5

. Protein sequence analysis of GPI17, AtPIGS and PIGS proteins. a Multiple alignment of Saccharomyces cerevisiae GPI17, Arabidopsis AtPIGS (AT3G07180), and Homo sapiens PIGS, amino acid sequences using Clustal Omega and visualization with BOXSHADE 3.2. Identical residues are colored black and similar residues are colored gray. b Amino acid sequences of Arabidopsis AtPIGS (599AA, 2-TM), H. sapiens PIGS (555AA, 2-TM), and S. cerevisiae GPI17 (534AA, 2-TM) were analyzed in the TMHMM Server v. 2.0 for the presence and location of transmembrane helices within each protein. c Clustal Omega amino acid sequence alignment scores for Arabidopsis AtPIGS, H. sapiens PIGS, and S. cerevisiae GPI17. Similarity percentage was calculated using Blosum62 matrix with a threshold of >1. (TIF 1225 kb)

Supplementary Fig. 6

. Phylogenetic Gene Tree of PIGU in Brassicaceae. Best-scoring Maximum Likelihood phylogenetic tree from RAxML (Geneious Prime) built with 100 bootstrap replicates using the GTR GAMMA model of nucleotide substitution. Full length nucleotide CDS of AtPIGU1 and AtPIGU2 orthologs were identified via reciprocal BLAST for 7 Brassicaceae species as well as Carica papaya, Solanum lycopersicum, and Aquilegia coerulea using genomes available through Phytozome v12.1.6 and CoGe. Alignment was generated using Geneious Translation Alignment, MUSCLE algorithm, with the BLOSUM62 cost matrix. Scale bar is patristic distance based on the number of apomorphic changes separating two taxa on the cladogram. Red star indicates the node forming the Brassicaceae clade and blue box indicates species belonging to Lineage II of Brassicaceae. (TIF 158 kb)

Supplementary Fig. 7

. AtPIGU1 and AtPIGU2 expression in Arabidopsis development. Relative mRNA levels of AtPIGU1 (At1g63110) / AtPIGU2 (At1g12730) in different Arabidopsis tissues. Image was generated with the Klepikova eFP (RNA-Seq data) at bar.utoronto.ca/eplant (Waese et al. 2017). (TIF 496 kb)

Supplementary Table 1

. Microarray analysis of Arabidopsis GAP expression in gametophytes. Expression of 248 GAPs predicted by Borner et al. (2003) and two additional GAPs identified by PLD treatment in Elortza et al. (2006) were analyzed for gametophytic expression using publically available Affymetrix ATH1 GeneChip microarray data on cell types dissected from the MG and FG via laser capture microdissection (Wuest et al. 2010a). 207 GAPs out of the 250 predicted GAPs were on the chip. Microarray analysis was done with three biological replicates and analyzed for presence/absence calls using the PANP algorithm described in Wuest et al. (2010). Cells are colored in shades of red according to the number of biological replicates out of three total biological replicates with “present calls” for each gene and cell type. Genes are grouped either by gene family as described in Borner et al. (2003) (First sheet) or by expression pattern (Second sheet). Green cells indicate that gene was verified as pollen expressed via RT-PCR (Lalanne et al. 2004), Green text indicates that gene was verified as a pollen-expressed GAP through PI-PLC – Mass Spectrometry (Lalanne et al. 2004), italic texts indicate that gene was verified as a vegetatively expressed GAP through PI-PLC/PLD—Mass Spectrometry (Elortza et al. 2006; Elortza et al. 2003). Gene IDs highlighted have reproductive mutant phenotypes and are listed in Table 1. (XLSX 43 kb)

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Desnoyer, N., Palanivelu, R. Bridging the GAPs in plant reproduction: a comparison of plant and animal GPI-anchored proteins. Plant Reprod 33, 129–142 (2020). https://doi.org/10.1007/s00497-020-00395-9

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