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Constitutive expression of a grapevine polygalacturonase-inhibiting protein affects gene expression and cell wall properties in uninfected tobacco.

ABSTRACT: BACKGROUND: Polygalacturonase-inhibiting proteins (PGIPs) directly limit the effective ingress of fungal pathogens by inhibiting cell wall-degrading endopolygalacturonases (ePGs). Transgenic tobacco plants over-expressing grapevine (Vitis vinifera) Vvpgip1 have previously been shown to be resistant to Botrytis infection. In this study we characterized two of these PGIP over-expressing lines with known resistance phenotypes by gene expression and hormone profiling in the absence of pathogen infection. RESULTS: Global gene expression was performed by a cross-species microarray approach using a potato cDNA microarray. The degree of potential cross-hybridization between probes was modeled by a novel computational workflow designed in-house. Probe annotations were updated by predicting probe-to-transcript hybridizations and combining information derived from other plant species. Comparing uninfected Vvpgip1-overexpressing lines to wild-type (WT), 318 probes showed significant change in expression. Functional groups of genes involved in metabolism and associated to the cell wall were identified and consequent cell wall analysis revealed increased lignin-levels in the transgenic lines, but no major differences in cell wall-derived polysaccharides. GO enrichment analysis also identified genes responsive to auxin, which was supported by elevated indole-acetic acid (IAA) levels in the transgenic lines. Finally, a down-regulation of xyloglucan endotransglycosylase/hydrolases (XTHs), which are important in cell wall remodeling, was linked to a decrease in total XTH activity. CONCLUSIONS: This evaluation of PGIP over-expressing plants performed under pathogen-free conditions to exclude the classical PGIP-ePG inhibition interaction indicates additional roles for PGIPs beyond the inhibition of ePGs.

SUBMITTER: Alexandersson E

PROVIDER: S-EPMC3339426 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Constitutive expression of a grapevine polygalacturonase-inhibiting protein affects gene expression and cell wall properties in uninfected tobacco.

Alexandersson Erik E Becker John Vw JV Jacobson Dan D Nguema-Ona Eric E Steyn Cobus C Denby Katherine J KJ Vivier Melané A MA

BMC research notes 20111113

<h4>Background</h4>Polygalacturonase-inhibiting proteins (PGIPs) directly limit the effective ingress of fungal pathogens by inhibiting cell wall-degrading endopolygalacturonases (ePGs). Transgenic tobacco plants over-expressing grapevine (Vitis vinifera) Vvpgip1 have previously been shown to be resistant to Botrytis infection. In this study we characterized two of these PGIP over-expressing lines with known resistance phenotypes by gene expression and hormone profiling in the absence of pathoge ...[more]

PMID: 22078230

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Project description:In pectin regulation, polygalacturonases (PGs) and pectin methylesterases (PMEs) are critical components in the transformation, disassembly network, and remodeling of plant primary cell walls. In the current study, we identified 36 PG and 47 PME genes using the available genomic resources of grapevine. Herein, we provide a comprehensive overview of PGs and PMEs, including phylogenetic and collinearity relationships, motif and gene structure compositions, gene duplications, principal component analysis, and expression profiling during developmental stages. Phylogenetic analysis of PGs and PMEs revealed similar domain composition patterns with Arabidopsis. The collinearity analysis showed high conservation and gene duplications with purifying selection. The type of duplications also varied in terms of gene numbers in PGs (10 dispersed, 1 proximal, 12 tandem, and 13 segmental, respectively) and PMEs (23 dispersed, 1 proximal, 16 tandem, and 7 segmental, respectively). The tissue-specific response of PG and PME genes based on the reported transcriptomic data exhibited diverged expression patterns in various organs during different developmental stages. Among PGs, VvPG8, VvPG10, VvPG13, VvPG17, VvPG18, VvPG19, VvPG20, VvPG22, and VvPG23 showed tissue- or organ-specific expression in majority of the tissues during development. Similarly, in PMEs, VvPME3, VvPME4, VvPME5, VvPME6, VvPME19, VvPME21, VvPME23, VvPME29, VvPME31, and VvPME32 suggested high tissue-specific response. The gene ontology (GO), Kyoto Encyclopedia of Genes and Genomics (KEGG) enrichment, and cis-elements prediction analysis also suggested the putative functions of PGs and PMEs in plant development, such as pectin and carbohydrate metabolism, and stress activities. Moreover, qRT-PCR validation of 32 PG and PME genes revealed their role in various organs of grapevines (i.e., root, stem, tendril, inflorescence, flesh, skins, and leaves). Therefore, these findings will lead to novel insights and encourage cutting-edge research on functional characterization of PGs and PMEs in fruit crop species.

Project description:The noteworthy fine remodeling that plant cell walls (CWs) undergo to adapt to developmental, physiological and environmental cues and the observation that its composition and dynamics differ between species represents an opportunity to couple crop species agronomic studies with research on CW modifications. Vitis vinifera is one of the most important crops from an economic point-of-view due to the high value of the fruit, predominantly for winemaking. The availability of some information related to this species' CWs allows researching its responses to imposed conditions that affect the plant's development. Mineral deficiency, in particular nitrogen, phosphorus, potassium and sulfur, strongly affects plant metabolism, reducing both growth and crop yield. Despite the importance of mineral nutrition in development, its influence on CW synthesis and modifications is still insufficiently documented. Addressing this knowledge gap, V. vinifera experimental models were used to study CW responses to imposed mineral depletion in unorganized (callus) and organized (shoots) tissues. The discussion of the obtained results is the main focus of this review. Callus and shoots submitted to mineral restriction are impaired in specific CW components, predominantly cellulose. Reorganization on structure and deposition of several other polymers, in particular the degree and pattern of pectin methyl-esterification and the amount of xyloglucan (XyG), arabinan and extensin, is also observed. In view of recently proposed CW models that consider biomechanical hotspots and direct linkages between pectins and XyG/cellulose, the outcome of these modifications in explaining maintenance of CW integrity through compensatory stiffening can be debated. Nutrient stresses do not affect evenly all tissues with undifferentiated callus tissues showing more pronounced responses, followed by shoot mature internodes, and then newly formed internodes. The impact of nitrogen depletion leads to more noticeable responses, supporting this nutrient's primary role in plant development and metabolism. The consequential compensatory mechanisms highlight the pivotal role of CW in rearranging under environmental stresses.

Dataset Information

Constitutive expression of a grapevine polygalacturonase-inhibiting protein affects gene expression and cell wall properties in uninfected tobacco.

Publications

Constitutive expression of a grapevine polygalacturonase-inhibiting protein affects gene expression and cell wall properties in uninfected tobacco.

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