The Trk Potassium Transporter Is Required for RsmB-Mediated Activation of Virulence in the Phytopathogen Pectobacterium wasabiae

ABSTRACTPectobacterium wasabiae(previously known asErwinia carotovora) is an important plant pathogen that regulates the production of plant cell wall-degrading enzymes through anN-acyl homoserine lactone-based quorum sensing system and through the GacS/GacA two-component system (also known as ExpS/ExpA). At high cell density, activation of GacS/GacA induces the expression of RsmB, a noncoding RNA that is essential for the activation of virulence in this bacterium. A genetic screen to identify regulators of RsmB revealed that mutants defective in components of a putative Trk potassium transporter (trkHandtrkA) had decreasedrsmBexpression. Further analysis of these mutants showed that changes in potassium concentration influencedrsmBexpression and consequent tissue damage in potato tubers and that this regulation required an intact Trk system. Regulation ofrsmBexpression by potassium via the Trk system occurred even in the absence of the GacS/GacA system, demonstrating that these systems act independently and are both required for full activation of RsmB and for the downstream induction of virulence in potato infection assays. Overall, our results identified potassium as an essential environmental factor regulating the Rsm system, and the consequent induction of virulence, in the plant pathogenP. wasabiae.IMPORTANCECrop losses from bacterial diseases caused by pectolytic bacteria are a major problem in agriculture. By studying the regulatory pathways involved in controlling the expression of plant cell wall-degrading enzymes inPectobacterium wasabiae, we showed that the Trk potassium transport system plays an important role in the regulation of these pathways. The data presented further identify potassium as an important environmental factor in the regulation of virulence in this plant pathogen. We showed that a reduction in virulence can be achieved by increasing the extracellular concentration of potassium. Therefore, this work highlights how elucidation of the mechanisms involved in regulating virulence can lead to the identification of environmental factors that can influence the outcome of infection.

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Regulation of the Production of Plant Cell Wall Degrading Enzymes in the Bacterial Plant Pathogen, Erwinia Carotovora Subsp. Carotovora.

Biotechnology in Agriculture - Current Plant Science and Biotechnology in Agriculture ◽

10.1007/978-94-011-1779-1_83 ◽

1993 ◽

pp. 426-429

Author(s):

A. K. Chatterjee ◽

H. Murata ◽

Y. Liu ◽

A. Chatterjee

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Plant Pathogen ◽

Plant Cell Wall ◽

Erwinia Carotovora ◽

Cell Wall Degrading Enzymes ◽

Degrading Enzymes ◽

Bacterial Plant Pathogen

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The use of plant cell wall-degrading enzymes from newly isolatedPenicillium ochrochloronBiourge for viscosity reduction in ethanol production with fresh sweet potato tubers as feedstock

Biotechnology and Applied Biochemistry ◽

10.1002/bab.1190 ◽

2014 ◽

Vol 61 (4) ◽

pp. 480-491 ◽

Cited By ~ 6

Author(s):

Yuhong Huang ◽

Yanling Jin ◽

Weiliang Shen ◽

Yang Fang ◽

Guohua Zhang ◽

...

Keyword(s):

Cell Wall ◽

Ethanol Production ◽

Sweet Potato ◽

Plant Cell ◽

Plant Cell Wall ◽

Viscosity Reduction ◽

Potato Tubers ◽

Cell Wall Degrading Enzymes ◽

Degrading Enzymes

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An efficient treatment for detoxification process of cassava starch by plant cell wall-degrading enzymes

Journal of Bioscience and Bioengineering ◽

10.1016/j.jbiosc.2009.06.021 ◽

2010 ◽

Vol 109 (1) ◽

pp. 9-14 ◽

Cited By ~ 22

Author(s):

Somphit Sornyotha ◽

Khin Lay Kyu ◽

Khanok Ratanakhanokchai

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Plant Cell Wall ◽

Cassava Starch ◽

Cell Wall Degrading Enzymes ◽

Efficient Treatment ◽

Degrading Enzymes ◽

Detoxification Process

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Carbohydrate-Binding Modules in Plant Cell Wall-Degrading Enzymes

Trends in Glycoscience and Glycotechnology ◽

10.4052/tigg.1403.1e ◽

2016 ◽

Vol 28 (161) ◽

pp. E49-E53

Author(s):

Shuichi Karita

Keyword(s):

Cell Wall ◽

Plant Cell ◽

Plant Cell Wall ◽

Carbohydrate Binding ◽

Cell Wall Degrading Enzymes ◽

Degrading Enzymes ◽

Carbohydrate Binding Modules

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The regulatory and transcriptional landscape associated with carbon utilization in a filamentous fungus

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1915611117 ◽

2020 ◽

Vol 117 (11) ◽

pp. 6003-6013 ◽

Cited By ~ 5

Author(s):

Vincent W. Wu ◽

Nils Thieme ◽

Lori B. Huberman ◽

Axel Dietschmann ◽

David J. Kowbel ◽

...

Keyword(s):

Cell Wall ◽

Transcription Factors ◽

Plant Cell ◽

Plant Cell Wall ◽

Plant Biomass ◽

Carbon Sources ◽

Cell Wall Degrading Enzymes ◽

Degrading Enzymes ◽

Genes Encoding

Filamentous fungi, such asNeurospora crassa, are very efficient in deconstructing plant biomass by the secretion of an arsenal of plant cell wall-degrading enzymes, by remodeling metabolism to accommodate production of secreted enzymes, and by enabling transport and intracellular utilization of plant biomass components. Although a number of enzymes and transcriptional regulators involved in plant biomass utilization have been identified, how filamentous fungi sense and integrate nutritional information encoded in the plant cell wall into a regulatory hierarchy for optimal utilization of complex carbon sources is not understood. Here, we performed transcriptional profiling ofN. crassaon 40 different carbon sources, including plant biomass, to provide data on how fungi sense simple to complex carbohydrates. From these data, we identified regulatory factors inN. crassaand characterized one (PDR-2) associated with pectin utilization and one with pectin/hemicellulose utilization (ARA-1). Using in vitro DNA affinity purification sequencing (DAP-seq), we identified direct targets of transcription factors involved in regulating genes encoding plant cell wall-degrading enzymes. In particular, our data clarified the role of the transcription factor VIB-1 in the regulation of genes encoding plant cell wall-degrading enzymes and nutrient scavenging and revealed a major role of the carbon catabolite repressor CRE-1 in regulating the expression of major facilitator transporter genes. These data contribute to a more complete understanding of cross talk between transcription factors and their target genes, which are involved in regulating nutrient sensing and plant biomass utilization on a global level.

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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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