Decreased Polysaccharide Feruloylation Compromises Plant Cell Wall Integrity and Increases Susceptibility to Necrotrophic Fungal Pathogens

Fungal pathogens have evolved combinations of plant cell-wall-degrading enzymes (PCWDEs) to deconstruct host plant cell walls (PCWs). An understanding of this process is hoped to create a basis for improving plant biomass conversion efficiency into sustainable biofuels and bioproducts. Here, an approach integrating enzyme activity assay, biomass pretreatment, field emission scanning electron microscopy (FESEM), and genomic analysis of PCWDEs were applied to examine digestibility or degradability of selected woody and herbaceous biomass by pathogenic fungi. Preferred hydrolysis of apple tree branch, rapeseed straw, or wheat straw were observed by the apple-tree-specific pathogen Valsa mali, the rapeseed pathogen Sclerotinia sclerotiorum, and the wheat pathogen Rhizoctonia cerealis, respectively. Delignification by peracetic acid (PAA) pretreatment increased PCW digestibility, and the increase was generally more profound with non-host than host PCW substrates. Hemicellulase pretreatment slightly reduced or had no effect on hemicellulose content in the PCW substrates tested; however, the pretreatment significantly changed hydrolytic preferences of the selected pathogens, indicating a role of hemicellulose branching in PCW digestibility. Cellulose organization appears to also impact digestibility of host PCWs, as reflected by differences in cellulose microfibril organization in woody and herbaceous PCWs and variation in cellulose-binding domain organization in cellulases of pathogenic fungi, which is known to influence enzyme access to cellulose. Taken together, this study highlighted the importance of chemical structure of both hemicelluloses and cellulose in host PCW digestibility by fungal pathogens.

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The Role of Mechanoperception in Plant Cell Wall Integrity Maintenance

Plants ◽

10.3390/plants9050574 ◽

2020 ◽

Vol 9 (5) ◽

pp. 574 ◽

Cited By ~ 6

Author(s):

Laura Bacete ◽

Thorsten Hamann

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Cell Walls ◽

Molecular Mechanisms ◽

Plant Cell Wall ◽

Cell Wall Integrity ◽

Adaptive Changes ◽

Structural Support ◽

Dynamic Structures ◽

Molecular Components

The plant cell walls surrounding all plant cells are highly dynamic structures, which change their composition and organization in response to chemical and physical stimuli originating both in the environment and in plants themselves. They are intricately involved in all interactions between plants and their environment while also providing adaptive structural support during plant growth and development. A key mechanism contributing to these adaptive changes is the cell wall integrity (CWI) maintenance mechanism. It monitors and maintains the functional integrity of cell walls by initiating adaptive changes in cellular and cell wall metabolism. Despite its importance, both our understanding of its mode of action and knowledge regarding the molecular components that form it are limited. Intriguingly, the available evidence implicates mechanosensing in the mechanism. Here, we provide an overview of the knowledge available regarding the molecular mechanisms involved in and discuss how mechanoperception and signal transduction may contribute to plant CWI maintenance.

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Plant cell wall integrity maintenance and pattern-triggered immunity modulate jointly plant stress responses in Arabidopsis thaliana

10.1101/130013 ◽

2017 ◽

Author(s):

Timo Engelsdorf ◽

Nora Gigli-Bisceglia ◽

Manikandan Veerabagu ◽

Joseph F. McKenna ◽

Frauke Augstein ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Plant Growth ◽

Plant Cell ◽

Stress Responses ◽

Cell Walls ◽

Plant Cell Wall ◽

Cell Wall Integrity ◽

Maintenance Mechanism ◽

Signaling Components

AbstractPlant cells are surrounded by walls, which must often meet opposing functional requirements during plant growth and defense. The cells meet them by modifying wall structure and composition in a tightly controlled and adaptive manner. The modifications seem to be mediated by a dedicated cell wall integrity (CWI) maintenance mechanism. Currently the mode of action of the mechanism is not understood and it is unclear how its activity is coordinated with established plant defense signaling. We investigated responses to induced cell wall damage (CWD) impairing CWI and the underlying mechanism in Arabidopsis thaliana. Interestingly inhibitor- and enzyme-derived CWD induced similar, turgor-sensitive stress responses. Genetic analysis showed that the receptor-like kinase (RLK) FEI2 and the mechano-sensitive, plasma membrane-localized Ca2+- channel MCA1 function downstream of the THE1 RLK in CWD perception. Phenotypic clustering with 27 genotypes identified a core group of RLKs and ion channels, required for activation of CWD responses. By contrast, the responses were repressed by pattern-triggered immune (PTI) signaling components including PEPR1 and 2, the receptors for the immune signaling peptide AtPep1. Interestingly AtPep1 application repressed CWD-induced phytohormone accumulation in a PEPR1/2-dependent manner. These results suggest that PTI suppresses CWD-induced defense responses through elicitor peptide-mediated signaling during defense response activation. If PTI is impaired, the suppression of CWD-induced responses is alleviated, thus compensating for defective PTI.Significance statementStress resistance and plant growth determine food crop yield and efficiency of bioenergy production from ligno-cellulosic biomass. Plant cell walls are essential elements of the biological processes, therefore functional integrity of the cell walls must be maintained throughout. Here we investigate the plant cell wall integrity maintenance mechanism. We characterize its mode of action, identify essential signaling components and show that the AtPep1 signaling peptide apparently coordinates pattern triggered immunity (PTI) and cell wall integrity maintenance in plants. These results suggest how PTI and cell wall modification coordinately regulate biotic stress responses with plants possibly compensating for PTI impairment through enhanced activation of stress responses regulated by the CWI maintenance mechanism.

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Plant Cell Wall as a Key Player During Resistant and Susceptible Plant-Virus Interactions

Frontiers in Microbiology ◽

10.3389/fmicb.2021.656809 ◽

2021 ◽

Vol 12 ◽

Cited By ~ 1

Author(s):

Edmund Kozieł ◽

Katarzyna Otulak-Kozieł ◽

Józef Julian Bujarski

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Plant Virus ◽

Defense Mechanisms ◽

Fungal Pathogens ◽

Plant Cell Wall ◽

Viral Infections ◽

Structural Element ◽

Biotic Stresses ◽

New Research

The cell wall is a complex and integral part of the plant cell. As a structural element it sustains the shape of the cell and mediates contact among internal and external factors. We have been aware of its involvement in both abiotic (like drought or frost) and biotic stresses (like bacteria or fungi) for some time. In contrast to bacterial and fungal pathogens, viruses are not mechanical destructors of host cell walls, but relatively little is known about remodeling of the plant cell wall in response to viral biotic stress. New research results indicate that the cell wall represents a crucial active component during the plant’s response to different viral infections. Apparently, cell wall genes and proteins play key roles during interaction, having a direct influence on the rebuilding of the cell wall architecture. The plant cell wall is involved in both susceptibility as well as resistance reactions. In this review we summarize important progress made in research on plant virus impact on cell wall remodeling. Analyses of essential defensive wall associated proteins in susceptible and resistant responses demonstrate that the components of cell wall metabolism can affect the spread of the virus as well as activate the apoplast- and symplast-based defense mechanisms, thus contributing to the complex network of the plant immune system. Although the cell wall reorganization during the plant-virus interaction remains a challenging task, the use of novel tools and methods to investigate its composition and structure will greatly contribute to our knowledge in the field.

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Plant cell wall integrity maintenance in model plants and crop species-relevant cell wall components and underlying guiding principles

Cellular and Molecular Life Sciences ◽

10.1007/s00018-019-03388-8 ◽

2019 ◽

Vol 77 (11) ◽

pp. 2049-2077 ◽

Cited By ~ 8

Author(s):

Nora Gigli-Bisceglia ◽

Timo Engelsdorf ◽

Thorsten Hamann

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Cell Walls ◽

Plant Cell Wall ◽

Current Knowledge ◽

Cell Wall Integrity ◽

Plant Cell Walls ◽

Maintenance Mechanism ◽

Regulatory Processes ◽

Composition And Structure

AbstractThe walls surrounding the cells of all land-based plants provide mechanical support essential for growth and development as well as protection from adverse environmental conditions like biotic and abiotic stress. Composition and structure of plant cell walls can differ markedly between cell types, developmental stages and species. This implies that wall composition and structure are actively modified during biological processes and in response to specific functional requirements. Despite extensive research in the area, our understanding of the regulatory processes controlling active and adaptive modifications of cell wall composition and structure is still limited. One of these regulatory processes is the cell wall integrity maintenance mechanism, which monitors and maintains the functional integrity of the plant cell wall during development and interaction with environment. It is an important element in plant pathogen interaction and cell wall plasticity, which seems at least partially responsible for the limited success that targeted manipulation of cell wall metabolism has achieved so far. Here, we provide an overview of the cell wall polysaccharides forming the bulk of plant cell walls in both monocotyledonous and dicotyledonous plants and the effects their impairment can have. We summarize our current knowledge regarding the cell wall integrity maintenance mechanism and discuss that it could be responsible for several of the mutant phenotypes observed.

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The Plant Cell Wall Integrity Maintenance Mechanism—Concepts for Organization and Mode of Action

Plant and Cell Physiology ◽

10.1093/pcp/pcu164 ◽

2014 ◽

Vol 56 (2) ◽

pp. 215-223 ◽

Cited By ~ 46

Author(s):

Thorsten Hamann

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Mode Of Action ◽

Plant Cell Wall ◽

Cell Wall Integrity ◽

Maintenance Mechanism

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Functional characterization of genes mediating cell wall metabolism and responses to plant cell wall integrity impairment

10.1101/552893 ◽

2019 ◽

Author(s):

Timo Engelsdorf ◽

Lars Kjaer ◽

Nora Gigli-Bisceglia ◽

Lauri Vaahtera ◽

Stefan Bauer ◽

...

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Plant Cell Wall ◽

Functional Characterization ◽

Cell Wall Composition ◽

Cell Wall Integrity ◽

Cell Wall Metabolism ◽

Altered Expression ◽

Plant Environment ◽

The Impact

AbstractPlant cell walls participate in all plant-environment interactions. Maintaining cell wall integrity (CWI) during these interactions is essential. This realization led to increased interest in CWI and resulted in knowledge regarding early perception and signalling mechanisms active during CWI maintenance. By contrast, knowledge regarding processes mediating changes in cell wall metabolism upon CWI impairment is very limited. To identify genes involved and to investigate their contributions to the processes we selected 23 genes with altered expression in response to CWI impairment and characterized the impact of T-DNA insertions in these genes on cell wall composition using Fourier-Transform Infrared Spectroscopy (FTIR) in Arabidopsis thaliana seedlings. Insertions in 14 genes led to cell wall phenotypes detectable by FTIR. A detailed analysis of four genes found that their altered expression upon CWI impairment is dependent on THE1 activity, a key component of CWI maintenance. Phenotypic characterizations of insertion lines suggest that the four genes are required for particular aspects of CWI maintenance, cell wall composition or resistance to Plectosphaerella cucumerina infection in adult plants. Taken together, the results implicate the genes in responses to CWI impairment, cell wall metabolism and/or pathogen defence, thus identifying new molecular components and processes relevant for CWI maintenance.

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