scholarly journals Coexpression of Fungal Cell Wall-Modifying Enzymes Reveals Their Additive Impact on Arabidopsis Resistance to the Fungal Pathogen, Botrytis cinerea

Biology ◽  
2021 ◽  
Vol 10 (10) ◽  
pp. 1070
Author(s):  
Sivakumar Swaminathan ◽  
Nathan T. Reem ◽  
Vincenzo Lionetti ◽  
Olga A. Zabotina

The plant cell wall (CW) is an outer cell skeleton that plays an important role in plant growth and protection against both biotic and abiotic stresses. Signals and molecules produced during host–pathogen interactions have been proven to be involved in plant stress responses initiating signal pathways. Based on our previous research findings, the present study explored the possibility of additively or synergistically increasing plant stress resistance by stacking beneficial genes. In order to prove our hypothesis, we generated transgenic Arabidopsis plants constitutively overexpressing three different Aspergillus nidulans CW-modifying enzymes: a xylan acetylesterase, a rhamnogalacturonan acetylesterase and a feruloylesterase. The two acetylesterases were expressed either together or in combination with the feruloylesterase to study the effect of CW polysaccharide deacetylation and deferuloylation on Arabidopsis defense reactions against a fungal pathogen, Botrytis cinerea. The transgenic Arabidopsis plants expressing two acetylesterases together showed higher CW deacetylation and increased resistance to B. cinerea in comparison to wild-type (WT) Col-0 and plants expressing single acetylesterases. While the expression of feruloylesterase alone compromised plant resistance, coexpression of feruloylesterase together with either one of the two acetylesterases restored plant resistance to the pathogen. These CW modifications induced several defense-related genes in uninfected healthy plants, confirming their impact on plant resistance. These results demonstrated that coexpression of complementary CW-modifying enzymes in different combinations have an additive effect on plant stress response by constitutively priming the plant defense pathways. These findings might be useful for generating valuable crops with higher protections against biotic stresses.

Plants ◽  
2020 ◽  
Vol 9 (5) ◽  
pp. 601
Author(s):  
Silvio Tundo ◽  
Maria Chiara Paccanaro ◽  
Ibrahim Elmaghraby ◽  
Ilaria Moscetti ◽  
Renato D’Ovidio ◽  
...  

During host plant infection, pathogens produce a wide array of cell wall degrading enzymes (CWDEs) to break the plant cell wall. Among CWDEs, xylanases are key enzymes in the degradation of xylan, the main component of hemicellulose. Targeted deletion experiments support the direct involvement of the xylanase BcXyn11a in the pathogenesis of Botrytis cinerea. Since the Triticum aestivum xylanase inhibitor-I (TAXI-I) has been shown to inhibit BcXyn11a, we verified if TAXI-I could be exploited to counteract B. cinerea infections. With this aim, we first produced Nicotiana tabacum plants transiently expressing TAXI-I, observing increased resistance to B. cinerea. Subsequently, we transformed Arabidopsis thaliana to express TAXI-I constitutively, and we obtained three transgenic lines exhibiting a variable amount of TAXI-I. The line with the higher level of TAXI-I showed increased resistance to B. cinerea and the absence of necrotic lesions when infiltrated with BcXyn11a. Finally, in a droplet application experiment on wild-type Arabidopsis leaves, TAXI-I prevented the necrotizing activity of BcXyn11a. These results would confirm that the contribution of BcXyn11a to virulence is due to its necrotizing rather than enzymatic activity. In conclusion, our experiments highlight the ability of the TAXI-I xylanase inhibitor to counteract B. cinerea infection presumably by preventing the necrotizing activity of BcXyn11a.


2015 ◽  
Vol 28 (11) ◽  
pp. 1167-1180 ◽  
Author(s):  
Jani Kelloniemi ◽  
Sophie Trouvelot ◽  
Marie-Claire Héloir ◽  
Adeline Simon ◽  
Bérengère Dalmais ◽  
...  

Mature grapevine berries at the harvesting stage (MB) are very susceptible to the gray mold fungus Botrytis cinerea, while veraison berries (VB) are not. We conducted simultaneous microscopic and transcriptomic analyses of the pathogen and the host to investigate the infection process developed by B. cinerea on MB versus VB, and the plant defense mechanisms deployed to stop the fungus spreading. On the pathogen side, our genome-wide transcriptomic data revealed that B. cinerea genes upregulated during infection of MB are enriched in functional categories related to necrotrophy, such as degradation of the plant cell wall, proteolysis, membrane transport, reactive oxygen species (ROS) generation, and detoxification. Quantitative-polymerase chain reaction on a set of representative genes related to virulence and microscopic observations further demonstrated that the infection is also initiated on VB but is stopped at the penetration stage. On the plant side, genome-wide transcriptomic analysis and metabolic data revealed a defense pathway switch during berry ripening. In response to B. cinerea inoculation, VB activated a burst of ROS, the salicylate-dependent defense pathway, the synthesis of the resveratrol phytoalexin, and cell-wall strengthening. On the contrary, in infected MB, the jasmonate-dependent pathway was activated, which did not stop the fungal necrotrophic process.


2000 ◽  
Vol 13 (4) ◽  
pp. 430-438 ◽  
Author(s):  
Cecilia Norman-Setterblad ◽  
Sabina Vidal ◽  
E. Tapio Palva

We have characterized the role of salicylic acid (SA)-independent defense signaling in Arabidopsis thaliana in response to the plant pathogen Erwinia carotovora subsp. carotovora. Use of pathway-specific target genes as well as signal mutants allowed us to elucidate the role and interactions of ethylene, jasmonic acid (JA), and SA signal pathways in this response. Gene expression studies suggest a central role for both ethylene and JA pathways in the regulation of defense gene expression triggered by the pathogen or by plant cell wall-degrading enzymes (CF) secreted by the pathogen. Our results suggest that ethylene and JA act in concert in this regulation. In addition, CF triggers another, strictly JA-mediated response inhibited by ethylene and SA. SA does not appear to have a major role in activating defense gene expression in response to CF. However, SA may have a dual role in controlling CF-induced gene expression, by enhancing the expression of genes synergistically induced by ethylene and JA and repressing genes induced by JA alone.


2014 ◽  
Vol 2014 ◽  
pp. 1-9 ◽  
Author(s):  
Lyuben Zagorchev ◽  
Plamena Kamenova ◽  
Mariela Odjakova

Contemporary agriculture is facing new challenges with the increasing population and demand for food on Earth and the decrease in crop productivity due to abiotic stresses such as water deficit, high salinity, and extreme fluctuations of temperatures. The knowledge of plant stress responses, though widely extended in recent years, is still unable to provide efficient strategies for improvement of agriculture. The focus of study has been shifted to the plant cell wall as a dynamic and crucial component of the plant cell that could immediately respond to changes in the environment. The investigation of plant cell wall proteins, especially in commercially important monocot crops revealed the high involvement of this compartment in plants stress responses, but there is still much more to be comprehended. The aim of this review is to summarize the available data on this issue and to point out the future areas of interest that should be studied in detail.


2006 ◽  
Vol 19 (8) ◽  
pp. 931-936 ◽  
Author(s):  
Simone Ferrari ◽  
Roberta Galletti ◽  
Donatella Vairo ◽  
Felice Cervone ◽  
Giulia De Lorenzo

Polygalacturonases (PGs) hydrolyze the homogalacturonan of plant cell-wall pectin and are important virulence factors of several phytopathogenic fungi. In response to abiotic and biotic stress, plants accumulate PG-inhibiting proteins (PGIPs) that reduce the activity of fungal PGs. In Arabidopsis thaliana, PGIPs with comparable activity against BcPG1, an important pathogenicity factor of the necrotrophic fungus Botrytis cinerea, are encoded by two genes, AtPGIP1 and AtPGIP2. Both genes are induced by fungal infection through different signaling pathways. We show here that transgenic Arabidopsis plants expressing an antisense AtPGIP1 gene have reduced AtPGIP1 inhibitory activity and are more susceptible to B. cinerea infection. These results indicate that PGIP contributes to basal resistance to this pathogen and strongly support the vision that this protein plays a role in Arabidopsis innate immunity.


2014 ◽  
Vol 27 (8) ◽  
pp. 781-792 ◽  
Author(s):  
Majse Nafisi ◽  
Maria Stranne ◽  
Lisha Zhang ◽  
Jan A. L. van Kan ◽  
Yumiko Sakuragi

The plant cell wall is one of the first physical interfaces encountered by plant pathogens and consists of polysaccharides, of which arabinan is an important constituent. During infection, the necrotrophic plant pathogen Botrytis cinerea secretes a cocktail of plant cell-wall-degrading enzymes, including endo-arabinanase activity, which carries out the breakdown of arabinan. The roles of arabinan and endo-arabinanases during microbial infection were thus far elusive. In this study, the gene Bcara1 encoding for a novel α-1,5-L-endo-arabinanase was identified and the heterologously expressed BcAra1 protein was shown to hydrolyze linear arabinan with high efficiency whereas little or no activity was observed against the other oligo- and polysaccharides tested. The Bcara1 knockout mutants displayed reduced arabinanase activity in vitro and severe retardation in secondary lesion formation during infection of Arabidopsis leaves. These results indicate that BcAra1 is a novel endo-arabinanase and plays an important role during the infection of Arabidopsis. Interestingly, the level of Bcara1 transcript was considerably lower during the infection of Nicotiana benthamiana compared with Arabidopsis and, consequently, the ΔBcara1 mutants showed the wild-type level of virulence on N. benthamiana leaves. These results support the conclusion that the expression of Bcara1 is host dependent and is a key determinant of the disease outcome.


2008 ◽  
Vol 21 (2) ◽  
pp. 171-177 ◽  
Author(s):  
Michela Janni ◽  
Luca Sella ◽  
Francesco Favaron ◽  
Ann E. Blechl ◽  
Giulia De Lorenzo ◽  
...  

A possible strategy to control plant pathogens is the improvement of natural plant defense mechanisms against the tools that pathogens commonly use to penetrate and colonize the host tissue. One of these mechanisms is represented by the host plant's ability to inhibit the pathogen's capacity to degrade plant cell wall polysaccharides. Polygalacturonase-inhibiting proteins (PGIP) are plant defense cell wall glycoproteins that inhibit the activity of fungal endopolygalacturonases (endo-PGs). To assess the effectiveness of these proteins in protecting wheat from fungal pathogens, we produced a number of transgenic wheat lines expressing a bean PGIP (PvPGIP2) having a wide spectrum of specificities against fungal PGs. Three independent transgenic lines were characterized in detail, including determination of the levels of PvPGIP2 accumulation and its subcellular localization and inhibitory activity. Results show that the transgene-encoded protein is correctly secreted into the apoplast, maintains its characteristic recognition specificities, and endows the transgenic wheat with new PG recognition capabilities. As a consequence, transgenic wheat tissue showed increased resistance to digestion by the PG of Fusarium moniliforme. These new properties also were confirmed at the plant level during interactions with the fungal pathogen Bipolaris sorokiniana. All three lines showed significant reductions in symptom progression (46 to 50%) through the leaves following infection with this pathogen. Our results illustrate the feasibility of improving wheat's defenses against pathogens by expression of proteins with new capabilities to counteract those produced by the pathogens.


2015 ◽  
Vol 28 (10) ◽  
pp. 1091-1101 ◽  
Author(s):  
Chenghua Zhang ◽  
Yifan He ◽  
Pinkuan Zhu ◽  
Lu Chen ◽  
Yiwen Wang ◽  
...  

Botrytis cinerea is a necrotrophic pathogen that causes gray mold disease in a broad range of plants. Dihydroxynaphthalene (DHN) melanin is a major component of the extracellular matrix of B. cinerea, but knowledge of the exact role of melanin biosynthesis in this pathogen is unclear. In this study, we characterize two genes in B. cinerea, bcpks13 and bcbrn1, encoding polyketide synthase and tetrahydroxynaphthalene (THN) reductases, respectively, and both have predicted roles in DHN melanin biosynthesis. The ∆bcpks13 and ∆bcbrn1 mutants show white and orange pigmentation, respectively, and the mutants are also deficient in conidiation in vitro but show enhanced growth rates and virulence on hosts. Moreover, the mutants display elevated acidification of the complete medium (CM), probably due to oxalic acid secretion and secretion of cell wall–degrading enzymes, and preferably utilize plant cell-wall components as carbon sources for mycelium growth in vitro. In contrast, overexpression of bcbrn1 (OE::bcbrn1 strain) results in attenuated hydrolytic enzyme secretion, acidification ability, and virulence. Taken together, these results indicate that bcpks13 and bcbrn1 participate in diverse cellular and developmental processes, such as melanization and conidiation in B. cinerea in vitro, but they negatively regulate the virulence of this pathogen.


Author(s):  
D. Reis ◽  
B. Vian ◽  
J. C. Roland

Wall morphogenesis in higher plants is a problem still open to controversy. Until now the possibility of a transmembrane control and the involvement of microtubules were mostly envisaged. Self-assembly processes have been observed in the case of walls of Chlamydomonas and bacteria. Spontaneous gelling interactions between xanthan and galactomannan from Ceratonia have been analyzed very recently. The present work provides indications that some processes of spontaneous aggregation could occur in higher plants during the formation and expansion of cell wall.Observations were performed on hypocotyl of mung bean (Phaseolus aureus) for which growth characteristics and wall composition have been previously defined.In situ, the walls of actively growing cells (primary walls) show an ordered three-dimensional organization (fig. 1). The wall is typically polylamellate with multifibrillar layers alternately transverse and longitudinal. Between these layers intermediate strata exist in which the orientation of microfibrils progressively rotates. Thus a progressive change in the morphogenetic activity occurs.


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