A high confidencePhyscomitrium patensplasmodesmata proteome by iterative scoring and validation reveals diversification of cell wall proteins during evolution
Sven GombosManuel MirasVicky HoweLin XiMathieu PottierNeda S. Kazemein JasemiMoritz SchladtJ. Obinna EjikeUlla NeumannSebastian HänschFranziska KuttigZhaoxia ZhangMarcel DickmannsPeng XuTorsten StefanWolfgang BaumeisterWolf B. FrommerRüdiger SimonWaltraud X. Schulze
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Abstract Cells of multicellular organisms exchange nutrients, building blocks and information. In animals, this happens via gap junctions, in plants via plasmodesmata (PD). PD have striking properties, translocating a large range of molecules from ions, to metabolites, RNA and proteins up to 40 kDa. PD are hard to characterize due to being deeply embedded into cell walls and the presence of several membranes. While previous studies of protein composition of PD from angiosperms identified large lists of proteins, few were validated. Here, we developed a PD scoring approach in conjunction with systematic localization on a large scale to define a high-confidence PD proteome of Physcomitrium patens . This high confidence PD proteome comprises nearly 300 proteins, which together with the bona fide PD proteins from literature, are made available in the public PDDB database. Conservation of localization across plant species strengthens the reliability of plant PD proteomes and provides a basis for exploring the evolution of this important organelle. In particular, the P. patens PD proteome was highly enriched in cell wall modifying proteins. Callose-degrading glycolyl hydrolase family 17 (GHL17) proteins are presented as an abundant PD protein family with representatives across an evolutionary scale. Exclusively members of the alpha-clade of the GHL17 family are shown to be PD localized and their orthologs occur only in plant species which have developed PD. Members of the EXORDIUM-family and xyloglucan transglycosylases are additional cell-wall located proteins highly abundant in the P. patens PD proteome also showing evolutionary diversification of PD localized family members from other clade members.Keywords:
Proteome
Plasmodesma
Multicellular organism
Protein family
A unique cell wall component has been observed in the aleurone layer of barley ( Hordeum vulgare L. cv. Himalaya). This wall component has been shown to be localized adjacent to the plasmalemma. Unlike the surrounding cell wall matrix it is resistant to “Onozuka” cellulase and remains intact during gibberellic acid‐stimulated hydrolase release. After treatment of the tissue with gibberellic acid followed by digestion with “Onozuka” cellulase this resistant wall component can be isolated free of protoplast. Study of its surface features revealed the presence of numerous tubular extensions, 120 nm wide, connecting adjacent resistant walls. These tubes resembled light microscope images of plasmodesmata in size and appearance. E.M. sections of resistant walls showed the presence of unit membrane lining the inner surface of the wall tubes. It was concluded that the resistant wall constitutes a modified wall layer that is secreted uniformly across all plasmalemma surfaces, including those in the wall (plasmodesmata). The presence of wall tubes surrounding plasmodesmata enhances the apparent size of the plasmodesmata in the light microscope. This may account for previous inconsistencies in the literature between light and electron microscope determinations of plasmodesmata diameters.
Plasmodesma
Aleurone
Protoplast
Callose
Apical cell
Gibberellic acid
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Plant cell wall proteomics has been a very dynamic field of research for about fifteen years. A full range of strategies has been proposed to increase the number of identified proteins and to characterize their post-translational modifications. The protocols are still improving to enlarge the coverage of cell wall proteomes. Comparisons between these proteomes have been done based on various working strategies or different physiological stages. In this review, two points are highlighted. The first point is related to data analysis with an overview of the cell wall proteomes already described. A large body of data is now available with the description of cell wall proteomes of seventeen plant species. CWP contents exhibit particularities in relation to the major differences in cell wall composition and structure between these plants and between plant organs. The second point is related to methodology and concerns the present limitations of the coverage of cell wall proteomes. Because of the variety of cell wall structures and of the diversity of protein/polysaccharide and protein/protein interactions in cell walls, some CWPs can be missing either because they are washed out during the purification of cell walls or because they are covalently linked to cell wall components.
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Cell type
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Plasmodesma
Root tip
Electron micrographs
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Plasmodesma
Plant cell
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Plant cells are surrounded by cell walls playing many roles during development and in response to environmental constraints. Cell walls are mainly composed of polysaccharides (cellulose, hemicelluloses and pectins), but they also contain proteins which are critical players in cell wall remodeling processes. Today, the cell wall proteome of Arabidopsis thaliana , a major dicot model plant, comprises more than 700 proteins predicted to be secreted (cell wall proteins—CWPs) identified in different organs or in cell suspension cultures. However, the cell wall proteome of rosettes is poorly represented with only 148 CWPs identified after extraction by vacuum infiltration. This new study allows enlarging its coverage. A destructive method starting with the purification of cell walls has been performed and two experiments have been compared. They differ by the presence/absence of protein separation by a short 1D‐electrophoresis run prior to tryptic digestion and different gradient programs for peptide separation before mass spectrometry analysis. Altogether, the rosette cell wall proteome has been significantly enlarged to 361 CWPs, among which 213 newly identified in rosettes and 57 newly described. The identified CWPs fall in four major functional classes: 26.1% proteins acting on polysaccharides, 11.1% oxido‐reductases, 14.7% proteases and 11.7% proteins possibly related to lipid metabolism.
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Recent studies on plasmodesmata have shown that these important intercellular passages for communication and transport are much more sophisticated in both structure and regulatory abilities than previously imagined. A complex, but not well understood, substructure has been revealed by a variety of increasingly reliable ultrastructural techniques. Proteinaceous particles are seen within the cytoplasmic sleeve surrounding the desmotubule. Dye‐coupling studies have provided experimental evidence for the physical pathway of solute movement, supporting conclusions about substructural dimensions within plasmodesmata drawn from the ultrastructural studies. Calcium has been identified as a major factor in the regulation of intercellular communication via plasmodesmata. Evidence from studies on virus movement through plasmodesmata suggests a direct interaction between virallycoded movement proteins and plasmodesmata in the systemic spread of many viruses. There is increasing evidence, albeit indirect, that in some plant species phloem loading may involve transport of photoassimilate entirely within the symplast from mesophyll cells to the sieve element‐companion cell complexes of minor veins.
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Symplast
Movement protein
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Summary A cell wall preparation of high purity was obtained using a procedure which involved repeated grindings of etiolated maize mesocotyl tissue and filtration through 200 mesh nylon cloth, followed by cell disruption via a nitrogen disruption bomb, and recovery of the cell walls via filtration. The cell wall fraction was free of particulate contaminants as determined both by phase‐contrast and electron microscopy. The only membrane components found associated with the wall fraction as determined by electron microscopy were pladmodesmata embedded in the cell wall. The specific concentration of PAP26, a plasmodesmatal‐associated polypeptide, was greatly increased in the cleanest cell wall fraction. A second plasmodesmatal‐associated protein, PAP27, which was previously shown to be associated with the neck region of the plasmodesmata, was diminished as a result of passage through the nitrogen disruption bomb suggesting a partial fragmentation of the plasmodesmata. In addition to PAP26, the specific concentrations of at least three other cell wall‐associated polypeptides with molecular weights of 80, 21 and 18 kDa, as revealed by SDS‐PAGE, were also increased greatly in the cleanest cell wall fraction.
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Filtration (mathematics)
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▪ Abstract Cell walls separate individual plant cells. To enable essential intercellular communication, plants have evolved membrane-lined channels, termed plasmodesmata, that interconnect the cytoplasm between neighboring cells. Historically, plasmodesmata were viewed as facilitating traffic of low-molecular weight growth regulators and nutrients critical to growth. Evidence for macromolecular transport via plasmodesmata was solely based on the exploitation of plasmodesmata by plant viruses during infectious spread. Now plasmodesmata are revealed to transport endogenous proteins, including transcription factors important for development. Two general types of proteins, non-targeted and plasmodesmata-targeted, traffic plasmodesmata channels. Size and subcellular location influence non-targeted protein transportability. Superimposed on cargo-specific parameters, plasmodesmata themselves fluctuate in aperture between closed, open, and dilated. Furthermore, plasmodesmata alter their transport capacity temporally during development and spatially in different regions of the plant. Plasmodesmata are exposed as major gatekeepers of signaling molecules that facilitate or regulate developmental programs, maintain physiological status, and respond to pathogens.
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Plant cell
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Plasmodesmata are supracellular organelles connecting two adjacent plant cells, providing a pathway of direct intercellular communication. It is generally accepted that the size exclusion limit (SEL) of plasmodesmata is about 800～1000 Da. There are many evidences indicating that plasmodesmata SEL varies in different tissues under different physiological conditions. Under certain circumstances plasmodesmata SEL could be very high and macromolecules could traffic through plasmodesmata. Interaction with plasmodesmata, virus movement protein (MP) could modify SEL of plasmodesmata and enable virus transfer from cell to cell. In maize mutant kn1, the protein KN1 might be signal molecule which results in the formation of tumors in epidermis and other tissues. P protein could move from companian cell to sieve tube through plasmodesmata. The high plasmodesmal SEL in some tissues and the change of plasmodesmal SEL during development might play an important role in the regulation of development. The mechanisms of intercellular trafficking of macromolecules via plasmodesmata are discussed.
Plasmodesma
Cowpea mosaic virus
Plant cell
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Plasmodesma
Movement protein
Tobamovirus
Plant cell
Symplast
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