Arabinogalactan proteins: rising attention from plant biologists

Pereira, Ana Marta; Pereira, Luís Gustavo; Coimbra, Sı́lvia

doi:10.1007/s00497-015-0254-6

Cited by 85 publications

(94 citation statements)

References 100 publications

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“…These results suggest that the microspore phenotype has an impact on the reproductive success of kns4. Considerable evidence has now accumulated implicating the involvement of AGPs in pollen fertility and pollen tube growth (for review, see Nguema-Ona et al, 2012, Pereira et al, 2015. KNS4, as a b-(1,3)-GalT, is predicted to be involved in the synthesis of b-(1,3)-galactan backbone of type II AGs, which can either be attached to AGPs or pectin.…”

Section: Discussionmentioning

confidence: 99%

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

et al. 2016

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Pollen exine is essential for protection from the environment of the male gametes of seed-producing plants, but its assembly and composition remain poorly understood. We previously characterized Arabidopsis (Arabidopsis thaliana) mutants with abnormal pollen exine structure and morphology that we named kaonashi (kns). Here we describe the identification of the causal gene of kns4 that was found to be a member of the CAZy glycosyltransferase 31 gene family, identical to UNEVEN PATTERN OF EXINE1, and the biochemical characterization of the encoded protein. The characteristic exine phenotype in the kns4 mutant is related to an abnormality of the primexine matrix laid on the surface of developing microspores. Using light microscopy with a combination of type II arabinogalactan (AG) antibodies and staining with the arabinogalactan-protein (AGP)-specific b-Glc Yariv reagent, we show that the levels of AGPs in the kns4 microspore primexine are considerably diminished, and their location differs from that of wild type, as does the distribution of pectin labeling. Furthermore, kns4 mutants exhibit reduced fertility as indicated by shorter fruit lengths and lower seed set compared to the wild type, confirming that KNS4 is critical for pollen viability and development. KNS4 was heterologously expressed in Nicotiana benthamiana, and was shown to possess b-(1,3)-galactosyltransferase activity responsible for the synthesis of AG glycans that are present on both AGPs and/or the pectic polysaccharide rhamnogalacturonan I. These data demonstrate that defects in AGP/pectic glycans, caused by disruption of KNS4 function, impact pollen development and viability in Arabidopsis.Pollen, the male gametophyte of all seed plants, is crucial for reproductive success. Due to the harsh environmental conditions that pollen must survive in, it has developed an elaborate and specialized cell wall. However, despite its importance our knowledge of the fine structure and assembly of the pollen grain wall is poorly understood (Newbigin et al., 2009;Ariizumi and Toriyama, 2011;Quilichini et al., 2015;Shi et al., 2015). Arabidopsis (Arabidopsis thaliana) provides an ideal genetic and cell biological model to dissect the assembly of the components of the pollen grain wall. Arabidopsis pollen grains have a typical surface structure that consists of an inner intine layer, which is usually made up of cellulose and pectin, and the outer exine, which is largely composed of sporopollenin (Li et al., 1995). The exine is further subdivided into inner nexine and outer sexine. The sexine has a three-dimensional (3D) structure composed of many columns called baculae and a roof called tectum. These two structures give the Arabidopsis pollen surface a reticulate appearance with a uniform mesh size. The nexine is composed of outer nexine I (foot layer), which contains sporopollenin, and inner nexine II (endexine; Ariizumi and Toriyama, 2011;Jiang et al., 2013). A recent study suggests that arabinogalactan proteins (AGPs) are key constituents of nexine with express...

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Section: Discussionmentioning

confidence: 99%

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

et al. 2016

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“…Collectively, the functional characterization of HRGPs points toward their involvement in many processes within the wall, including signaling and cell wall integrity pathways (Costa et al, 2013;Pereira et al, 2015Pereira et al, , 2016Voxeur and Höfte, 2016). As plants evolved multicellularity and transitioned to land, it is likely that greater complexity in signaling networks was required, a role that could seemingly be fulfilled by HRGPs, due to their distinct protein and glycan characteristics.…”

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confidence: 99%

Insights into the Evolution of Hydroxyproline-Rich Glycoproteins from 1000 Plant Transcriptomes

et al. 2017

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The carbohydrate-rich cell walls of land plants and algae have been the focus of much interest given the value of cell wall-based products to our current and future economies. Hydroxyproline-rich glycoproteins (HRGPs), a major group of wall glycoproteins, play important roles in plant growth and development, yet little is known about how they have evolved in parallel with the polysaccharide components of walls. We investigate the origins and evolution of the HRGP superfamily, which is commonly divided into three major multigene families: the arabinogalactan proteins (AGPs), extensins (EXTs), and proline-rich proteins. Using motif and amino acid bias, a newly developed bioinformatics pipeline, we identified HRGPs in sequences from the 1000 Plants transcriptome project (www.onekp.com). Our analyses provide new insights into the evolution of HRGPs across major evolutionary milestones, including the transition to land and the early radiation of angiosperms. Significantly, data mining reveals the origin of glycosylphosphatidylinositol (GPI)-anchored AGPs in green algae and a 3-to 4-fold increase in GPI-AGPs in liverworts and mosses. The first detection of cross-linking (CL)-EXTs is observed in bryophytes, which suggests that CL-EXTs arose though the juxtaposition of preexisting SP n EXT glycomotifs with refined Y-based motifs. We also detected the loss of CL-EXT in a few lineages, including the grass family (Poaceae), that have a cell wall composition distinct from other monocots and eudicots. A key challenge in HRGP research is tracking individual HRGPs throughout evolution. Using the 1000 Plants output, we were able to find putative orthologs of Arabidopsis pollen-specific GPI-AGPs in basal eudicots.Cell walls of plants and algae are widely used for food, textiles, paper, and timber, yet our understanding of their assembly and dynamic remodeling in response to growth, development, and environmental stresses (abiotic and biotic) remains rudimentary (Doblin et al., 2010(Doblin et al., , 2014. There are two contrasting types of walls/extracellular matrices in the green plant lineage, protein-rich walls of some green algae and the cellulose-rich walls of embryophytes (land plants). Recent studies of cell wall evolution suggest that the origins of many wall components occurred in the streptophyte green algae prior to the evolution of embryophytes (Sørensen et al., 2010;Popper et al., 2011;Domozych et al., 2012) with elaboration of a preexisting set of polysaccharides rather than an entirely new polymer framework. Although both the ultrastructure of plant walls and the fine structure of their component polymers vary widely, they all typically constitute a fibrillar network of cellulose microfibrils that is embedded within a gel-like matrix of noncellulosic polysaccharides, pectins, 904

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“…AGPs are prevalent in the reproductive tissues of plants, and they have been proposed to play prominent roles in plant sexual reproduction (Pereira et al, 2015). Our studies to investigate the process of competency control during pollen tube guidance led to the discovery of an ovular factor AMOR (Arabinogalactan molecule) that induces competency in Torenia pollen tubes to respond to LURE attractants released from the ovules (Mizukami et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Structure-Activity Relation of AMOR Sugar Molecule That Activates Pollen-Tubes for Ovular Guidance

et al. 2016

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ORCID IDs: 0000-0003-3726-3798 (J.J.); 0000-0002-0398-2113 (S.S.); 0000-0002-7346-360X (T.H.).Successful fertilization in flowering plants depends on the precise directional growth control of pollen tube through the female pistil tissue toward the female gametophyte contained in the ovule for delivery of nonmotile sperm cells. Cys-rich peptides LUREs secreted from the synergid cells on either side of the egg cell act as ovular attractants of pollen tubes. Competency control by the pistil is crucial for the response of pollen tubes to these ovular attractants. We recently reported that ovular 4-O-methylglucuronosyl arabinogalactan (AMOR) induces competency of the pollen tube to respond to ovular attractant LURE peptides in Torenia fournieri. The beta isomer of the terminal disaccharide 4-O-methyl-glucuronosyl galactose was essential and sufficient for the competency induction. However, critical and noncritical structures in the disaccharide have not been dissected deeply. Herein, we report the synthesis of new AMOR analogs and the structure-activity relationships for AMOR activity in the presence of these synthesized analogs. Removal of 4-O-methyl group or -COOH from the glucuronosyl residue of the disaccharide dramatically reduces AMOR activity. The pyranose backbone of the second sugar of disaccharide is essential for the activity but not hydroxy groups. The role of beta isomer of the disaccharide 4-Me-GlcA-b(1,6)-Gal is very specific for competency control, as there was no difference in effect among the sugar analogs tested for pollen germination. This study represents the first structure-activity relationship study, to our knowledge, of a sugar molecule involved in plant reproduction, which opens a way for modification of the molecule without loss of activity.

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Arabinogalactan proteins: rising attention from plant biologists

Cited by 85 publications

References 100 publications

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

KNS4/UPEX1: A Type II Arabinogalactan β-(1,3)-Galactosyltransferase Required for Pollen Exine Development

Insights into the Evolution of Hydroxyproline-Rich Glycoproteins from 1000 Plant Transcriptomes

Structure-Activity Relation of AMOR Sugar Molecule That Activates Pollen-Tubes for Ovular Guidance

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