OsPGIP1-Mediated Resistance to Bacterial Leaf Streak in Rice is Beyond Responsive to the Polygalacturonase of Xanthomonas oryzae pv. oryzicola

AbstractPolygalacturonase-inhibiting proteins (PGIPs) have been shown to recognize fungal polygalacturonases (PGs), which initiate innate immunity in various plant species. Notably, the connection between rice OsPGIPs and PGs in Xanthomonas oryzae pv. oryzicola (Xoc), which causes bacterial leaf streak (BLS), remains unclear. Here, we show that OsPGIP1 was strongly induced after inoculating rice with the Xoc strain RS105. Furthermore, OsPGIP1-overexpressing (OV) and RNA interference (RNAi) rice lines increased and decreased, respectively, the resistance of rice to RS105, indicating that OsPGIP1 contributes to BLS resistance. Subsequently, we generated the unique PG mutant RS105Δpg, the virulence of which is attenuated compared to that of RS105. Surprisingly, the lesion lengths caused by RS105Δpg were similar to those caused by RS105 in the OV lines compared with wild-type ZH11 with reduced Xoc susceptibility. However, the lesion lengths caused by RS105Δpg were still significantly shorter in the OV lines than in ZH11, implying that OsPGIP1-mediated BLS resistance could respond to other virulence factors in addition to PGs. To explore the OsPGIP1-mediated resistance, RNA-seq analysis were performed and showed that many plant cell wall-associated genes and several MYB transcription factor genes were specifically expressed or more highly induced in the OV lines compared to ZH11 postinoculation with RS105. Consistent with the expression of the differentially expressed genes, the OV plants accumulated a higher content of jasmonic acid (JA) than ZH11 postinoculation with RS105, suggesting that the OsPGIP1-mediated resistance to BLS is mainly dependent on the plant cell wall-associated immunity and the JA signaling pathway.

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Synergistic Effect of Different Plant Cell Wall–Degrading Enzymes Is Important for Virulence of Fusarium graminearum

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-07-17-0179-r ◽

2017 ◽

Vol 30 (11) ◽

pp. 886-895 ◽

Cited By ~ 26

Author(s):

Maria Chiara Paccanaro ◽

Luca Sella ◽

Carla Castiglioni ◽

Francesca Giacomello ◽

Ana Lilia Martínez-Rocha ◽

...

Keyword(s):

Cell Wall ◽

Fusarium Graminearum ◽

Plant Cell ◽

Plant Cell Wall ◽

Xylanase Activity ◽

Cellulase Activity ◽

Wild Type ◽

Cell Wall Degrading Enzymes ◽

Xylanase Production ◽

Significant Difference

Endo-polygalacturonases (PGs) and xylanases have been shown to play an important role during pathogenesis of some fungal pathogens of dicot plants, while their role in monocot pathogens is less defined. Pg1 and xyr1 genes of the wheat pathogen Fusarium graminearum encode the main PG and the major regulator of xylanase production, respectively. Single- and double-disrupted mutants for these genes were obtained to assess their contribution to fungal infection. Compared with wild-type strain, the ∆pg mutant showed a nearly abolished PG activity, slight reduced virulence on soybean seedlings, but no significant difference in disease symptoms on wheat spikes; the ∆xyr mutant was strongly reduced in xylanase activity and moderately reduced in cellulase activity but was as virulent as wild type on both soybean and wheat plants. Consequently, the ΔpgΔxyr double mutant was impaired in xylanase, PG, and cellulase activities but, differently from single mutants, was significantly reduced in virulence on both plants. These findings demonstrate that the concurrent presence of PG, xylanase, and cellulase activities is necessary for full virulence. The observation that the uronides released from wheat cell wall after a F. graminearum PG treatment were largely increased by the fungal xylanases suggests that these enzymes act synergistically in deconstructing the plant cell wall.

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Pyramiding Unmarked Deletions in Ralstonia solanacearum Shows That Secreted Proteins in Addition to Plant Cell-Wall-Degrading Enzymes Contribute to Virulence

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-18-1296 ◽

2005 ◽

Vol 18 (12) ◽

pp. 1296-1305 ◽

Cited By ~ 77

Author(s):

Huanli Liu ◽

Shuping Zhang ◽

Mark A. Schell ◽

Timothy P. Denny

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Ralstonia Solanacearum ◽

Plant Cell Wall ◽

Secreted Proteins ◽

Cellulolytic Enzymes ◽

Wild Type ◽

Cell Wall Degrading Enzymes ◽

Tomato Plants ◽

Degrading Enzymes

Ralstonia solanacearum, like many phytopathogenic bacteria, makes multiple extracellular plant cell-wall-degrading enzymes (CWDE), some of which contribute to its ability to cause wilt disease. CWDE and many other proteins are secreted to the milieu via the highly conserved type II protein secretion system (T2SS). R. solanacearum with a defective T2SS is weakly virulent, but it is not known whether this is due to absence of all the CWDE or the loss of other secreted proteins that contribute to disease. These alternatives were investigated by creating mutants of wild-type strain GMI1000 lacking either the T2SS or up to six CWDE and comparing them for virulence on tomato plants. To create unmarked deletions, genomic regions flanking the target gene were polymerase chain reaction (PCR)-amplified, were fused using splice overlap extension PCR, were cloned into a suicide plasmid harboring the sacB counter-selectable marker, and then, were site-specifically introduced into the genome. Various combinations of five deletions (δpehA, δpehB, δpehC, δpme, and δegl) and one inactivated allele (cbhA::aphA-3) resulted in 15 mutants missing one to six CWDE. In soil-drench inoculation assays, virulence of mutants lacking only pectic enzymes (PehA, PehB, PehC, and Pme) was not statistically different from GMI1000, but all the mutants lacking one or both cellulolytic enzymes (Egl or CbhA) wilted plants significantly more slowly than did the wild type. The GMI-6 mutant that lacks all six CWDE was more virulent than the mutant lacking only its two cellulolytic enzymes, and both were significantly more virulent than the T2SS mutant (GMI-D). Very similar results were observed in wounded-petiole inoculation assays, so GMI-6 and GMI-D appear to be less capable of colonizing tomato tissues after invasion. Because the T2SS mutant was much less virulent than the sixfold CWDE mutant, we conclude that other secreted proteins contribute substantially to the ability of R. solanacearum GMI1000 to systemically colonize tomato plants.

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Proteomic analysis of rice leaves following treatment of Xanthomonas oryzae pv. oryzae secreted cell wall degrading enzyme

10.1101/2021.11.17.469048 ◽

2021 ◽

Author(s):

Anirudh Kumar ◽

Kamal Kumar Malukani ◽

Ramya Pamidimukkala ◽

Hitendra K. Patel ◽

Ramesh V Sonti

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Redox Regulation ◽

Plant Cell Wall ◽

Regulatory Elements ◽

Xanthomonas Oryzae ◽

Differentially Expressed ◽

Differentially Expressed Proteins ◽

Proteomics Data ◽

Cell Wall Degrading Enzymes

Bacterial Blight (BB) disease caused by Xanthomonas oryzae pv. oryzae (Xoo), is one of the most devastating diseases in various rice cultivating countries. Xoo secretes a mixture of plant cell wall degrading enzymes (CWDEs) such as cellulases, lipases, xylanases, and proteases to degrade different components of the plant cell wall. LipA; a lipase/esterase, is one such Xoo secreted CWDE and is an important virulence factor of Xoo. Treatment of rice tissue with purified LipA induces immune responses. In this study, a LC-MS based proteomics study was performed to identify the differentially expressed proteins (DEPs) in rice following LipA treatment. A total of 212 proteins were identified in control and 201 proteins in LipA treated samples. There were 151 proteins common between control and treatment. Fold change analysis of these common proteins through SIEVE identified 26 upregulated and 49 downregulated proteins by at least ≥1.5 fold in the LipA treated sample. Pathway analysis indicated that many proteins related to redox regulation, photosynthesis, and translation are differentially expressed after LipA treatment. We also observed that some of the differentially expressed proteins contain translation regulatory elements that may regulate translation after LipA treatment. The comparison of proteomics data with previously performed transcriptome analysis indicated that different sets of genes and pathways are altered in both the analyses.

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Production of plant cell wall degrading enzymes by the exo-1 mutant and wild type Neurospora crassa

Journal of Biotechnology ◽

10.1016/j.jbiotec.2010.09.815 ◽

2010 ◽

Vol 150 ◽

pp. 513-514

Author(s):

A.M. Polizeli ◽

M.A. Moraes ◽

J.A. Jorge ◽

H.F. Terenzi ◽

M.L.T.M. Polizeli

Keyword(s):

Cell Wall ◽

Neurospora Crassa ◽

Plant Cell ◽

Plant Cell Wall ◽

Wild Type ◽

Cell Wall Degrading Enzymes ◽

Degrading Enzymes

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Arabidopsis Response Regulator 6 (ARR6) Modulates Plant Cell-Wall Composition and Disease Resistance

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-12-19-0341-r ◽

2020 ◽

Vol 33 (5) ◽

pp. 767-780 ◽

Cited By ~ 7

Author(s):

Laura Bacete ◽

Hugo Mélida ◽

Gemma López ◽

Patrick Dabos ◽

Dominique Tremousaygue ◽

...

Keyword(s):

Cell Wall ◽

Disease Resistance ◽

Immune Responses ◽

Plant Cell ◽

Plant Cell Wall ◽

Response Regulator ◽

Cell Wall Composition ◽

Wild Type ◽

Molecular Patterns

The cytokinin signaling pathway, which is mediated by Arabidopsis response regulator (ARR) proteins, has been involved in the modulation of some disease-resistance responses. Here, we describe novel functions of ARR6 in the control of plant disease-resistance and cell-wall composition. Plants impaired in ARR6 function (arr6) were more resistant and susceptible, respectively, to the necrotrophic fungus Plectosphaerella cucumerina and to the vascular bacterium Ralstonia solanacearum, whereas Arabidopsis plants that overexpress ARR6 showed the opposite phenotypes, which further support a role of ARR6 in the modulation of disease-resistance responses against these pathogens. Transcriptomics and metabolomics analyses revealed that, in arr6 plants, canonical disease-resistance pathways, like those activated by defensive phytohormones, were not altered, whereas immune responses triggered by microbe-associated molecular patterns were slightly enhanced. Cell-wall composition of arr6 plants was found to be severely altered compared with that of wild-type plants. Remarkably, pectin-enriched cell-wall fractions extracted from arr6 walls triggered more intense immune responses than those activated by similar wall fractions from wild-type plants, suggesting that arr6 pectin fraction is enriched in wall-related damage-associated molecular patterns, which trigger immune responses. This work supports a novel function of ARR6 in the control of cell-wall composition and disease resistance and reinforces the role of the plant cell wall in the modulation of specific immune responses.

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