scholarly journals Trehalose Synthesis Contributes to Osmotic Stress Tolerance and Virulence of the Bacterial Wilt Pathogen Ralstonia solanacearum

2020 ◽  
Vol 33 (3) ◽  
pp. 462-473 ◽  
Author(s):  
April M. MacIntyre ◽  
John X. Barth ◽  
Molly C. Pellitteri Hahn ◽  
Cameron O. Scarlett ◽  
Stéphane Genin ◽  
...  
Keyword(s):  
Osmotic Stress ◽  
Bacterial Wilt ◽  
Ralstonia Solanacearum ◽  
Type Strain ◽  
Wild Type Strain ◽  
Xylem Sap ◽  
Wilt Disease ◽  
Wild Type ◽  
Tomato Plants ◽  
Trehalose Synthesis

The xylem-dwelling plant pathogen Ralstonia solanacearum changes the chemical composition of host xylem sap during bacterial wilt disease. The disaccharide trehalose, implicated in stress tolerance across all kingdoms of life, is enriched in sap from R. solanacearum–infected tomato plants. Trehalose in xylem sap could be synthesized by the bacterium, the plant, or both. To investigate the source and role of trehalose metabolism during wilt disease, we evaluated the effects of deleting the three trehalose synthesis pathways in the pathogen: TreYZ, TreS, and OtsAB, as well as its sole trehalase, TreA. A quadruple treY/treS/otsA/treA mutant produced 30-fold less intracellular trehalose than the wild-type strain missing the trehalase enzyme. This trehalose-nonproducing mutant had reduced tolerance to osmotic stress, which the bacterium likely experiences in plant xylem vessels. Following naturalistic soil-soak inoculation of tomato plants, this triple mutant did not cause disease as well as wild-type R. solanacearum. Further, the wild-type strain out-competed the trehalose-nonproducing mutant by over 600-fold when tomato plants were coinoculated with both strains, showing that trehalose biosynthesis helps R. solanacearum overcome environmental stresses during infection. An otsA (trehalose-6-phosphate synthase) single mutant behaved similarly to ΔtreY/treS/otsA in all experimental settings, suggesting that the OtsAB pathway is the dominant trehalose synthesis pathway in R. solanacearum.

scholarly journals Chemotaxis Is Required for Virulence and Competitive Fitness of the Bacterial Wilt Pathogen Ralstonia solanacearum

2006 ◽  
Vol 188 (10) ◽  
pp. 3697-3708 ◽  
Author(s):  
Jian Yao ◽  
Caitilyn Allen
Keyword(s):  
Host Plant ◽  
Plant Pathogen ◽  
Ralstonia Solanacearum ◽  
Type Strain ◽  
Wild Type Strain ◽  
Random Motion ◽  
Wild Type ◽  
Tomato Plants ◽  
Swimming Motility ◽  
Directed Motility

ABSTRACT Ralstonia solanacearum, a soilborne plant pathogen of considerable economic importance, invades host plant roots from the soil. Qualitative and quantitative chemotaxis assays revealed that this bacterium is specifically attracted to diverse amino acids and organic acids, and especially to root exudates from the host plant tomato. Exudates from rice, a nonhost plant, were less attractive. Eight different strains from this heterogeneous species complex varied significantly in their attraction to a panel of carbohydrate stimuli, raising the possibility that chemotactic responses may be differentially selected traits that confer adaptation to various hosts or ecological conditions. Previous studies found that an aflagellate mutant lacking swimming motility is significantly reduced in virulence, but the role of directed motility mediated by the chemotaxis system was not known. Two site-directed R. solanacearum mutants lacking either CheA or CheW, which are core chemotaxis signal transduction proteins, were completely nonchemotactic but retained normal swimming motility. In biologically realistic soil soak virulence assays on tomato plants, both nonchemotactic mutants had significantly reduced virulence indistinguishable from that of a nonmotile mutant, demonstrating that directed motility, not simply random motion, is required for full virulence. In contrast, nontactic strains were as virulent as the wild-type strain was when bacteria were introduced directly into the plant stem through a cut petiole, indicating that taxis makes its contribution to virulence in the early stages of host invasion and colonization. When inoculated individually by soaking the soil, both nontactic mutants reached the same population sizes as the wild type did in the stems of tomato plants just beginning to wilt. However, when tomato plants were coinoculated with a 1:1 mixture of a nontactic mutant and its wild-type parent, the wild-type strain outcompeted both nontactic mutants by 100-fold. Together, these results indicate that chemotaxis is an important trait for virulence and pathogenic fitness in this plant pathogen.

scholarly journals Trehalose induces tomato defenses and increases drought tolerance and bacterial wilt disease resistance

2021 ◽  
Author(s):  
April M MacIntyre ◽  
Valerian Meline ◽  
Zachary Gorman ◽  
Steven P Augustine ◽  
Carolyn J Dye ◽  
...  
Keyword(s):  
Disease Resistance ◽  
Stomatal Conductance ◽  
Water Use ◽  
Bacterial Wilt ◽  
Xylem Sap ◽  
Wilt Disease ◽  
Tomato Plants ◽  
Bacterial Wilt Disease ◽  
Infected Tomato ◽  
Use Efficiency

Ralstonia solanacearum causes plant bacterial wilt disease, leading to severe crop losses. Xylem sap from R. solanacearum-infected tomato is enriched in host produced trehalose. Water stressed plants accumulate the disaccharide trehalose, which increases drought tolerance via abscisic acid (ABA) signaling networks. Because infected plants have reduced water flow, we hypothesized that bacterial wilt physiologically mimics drought stress, which trehalose could mitigate. Transcriptomic responses of susceptible vs. resistant tomato plants to R. solanacearum infection revealed differential expression of drought-associated genes, including those involved in ABA and trehalose metabolism. ABA was enriched in xylem sap from R. solanacearum-infected plants. Treating roots with ABA lowered stomatal conductance and reduced R. solanacearum stem colonization. Treating roots with trehalose increased ABA in xylem sap and reduced plant water use by reducing stomatal conductance and temporarily improving water use efficiency. Further, trehalose-treated plants were more resistant to bacterial wilt disease. Trehalose treatment also upregulated expression of salicylic acid (SA)-dependent defense genes, increased xylem sap levels of SA and other antimicrobial compounds, and increased wilt resistance of SA-insensitive NahG tomato plants. Additionally, trehalose treatment increased xylem concentrations of jasmonic acid and related oxylipins. Together, these data show that exogenous trehalose reduced both water stress and bacterial wilt disease and triggered systemic resistance. This suite of responses revealed unexpected linkages between plant responses to biotic and abiotic stress and suggests that that R. solanacearum-infected tomato plants produce more trehalose to improve water use efficiency and increase wilt disease resistance. In turn, R. solanacearum degrades trehalose as a counter-defense.

scholarly journals Group III Histidine Kinase Is a Positive Regulator of Hog1-Type Mitogen-Activated Protein Kinase in Filamentous Fungi

2005 ◽  
Vol 4 (11) ◽  
pp. 1820-1828 ◽  
Author(s):  
Akira Yoshimi ◽  
Kaihei Kojima ◽  
Yoshitaka Takano ◽  
Chihiro Tanaka
Keyword(s):  
Osmotic Stress ◽  
Filamentous Fungi ◽  
Histidine Kinase ◽  
Type Strain ◽  
Wild Type Strain ◽  
Wild Type ◽  
Group Iii ◽  
Positive Regulator ◽  
Mitogen Activated Protein ◽  
In The Wild

ABSTRACT We previously reported that the group III histidine kinase Dic1p in the maize pathogen Cochliobolus heterostrophus is involved in resistance to dicarboximide and phenylpyrrole fungicides and in osmotic adaptation. In addition, exposure to the phenylpyrrole fungicide fludioxonil led to improper activation of Hog1-type mitogen-activated protein kinases (MAPKs) in some phytopathogenic fungi, including C. heterostrophus. Here we report, for the first time, the relationship between the group III histidine kinase and Hog1-related MAPK: group III histidine kinase is a positive regulator of Hog1-related MAPK in filamentous fungi. The phosphorylation pattern of C. heterostrophus BmHog1p (Hog1-type MAPK) was analyzed in wild-type and dic1-deficient strains by Western blotting. In the wild-type strain, phosphorylated BmHog1p was detected after exposure to both iprodione and fludioxonil at a concentration of 1 μg/ml. In the dic1-deficient strains, phosphorylated BmHog1p was not detected after exposure to 10 μg/ml of the fungicides. In response to osmotic stress (0.4 M KCl), a trace of phosphorylated BmHog1p was found in the dic1-deficient strains, whereas the band representing active BmHog1p was clearly detected in the wild-type strain. Similar results were obtained for Neurospora crassa Os-2p MAPK phosphorylation in the mutant of the group III histidine kinase gene os-1. These results indicate that group III histidine kinase positively regulates the activation of Hog1-type MAPKs in filamentous fungi. Notably, the Hog1-type MAPKs were activated at high fungicide (100 μg/ml) and osmotic stress (0.8 M KCl) levels in the histidine kinase mutants of both fungi, suggesting that another signaling pathway activates Hog1-type MAPKs in these conditions.

scholarly journals A cbb3-Type Cytochrome C Oxidase Contributes to Ralstonia solanacearum R3bv2 Growth in Microaerobic Environments and to Bacterial Wilt Disease Development in Tomato

2010 ◽  
Vol 23 (8) ◽  
pp. 1042-1052 ◽  
Author(s):  
Jennifer Colburn-Clifford ◽  
Caitilyn Allen
Keyword(s):  
Cytochrome C ◽  
Cytochrome C Oxidase ◽  
Bacterial Wilt ◽  
Ralstonia Solanacearum ◽  
Wilt Disease ◽  
Wild Type ◽  
Low Oxygen ◽  
Tomato Root ◽  
Bacterial Wilt Disease ◽  
Oxygen Conditions

Ralstonia solanacearum race 3 biovar 2 (R3bv2) is an economically important soilborne plant pathogen that causes bacterial wilt disease by infecting host plant roots and colonizing the xylem vessels. Little is known about R3bv2 behavior in the host rhizosphere and early in bacterial wilt pathogenesis. To explore this part of the disease cycle, we used a novel taxis-based promoter-trapping strategy to identify pathogen genes induced in the plant rhizosphere. This screen identified several rex (root exudate expressed) genes whose promoters were upregulated in the presence of tomato root exudates. One rex gene encodes an assembly protein for a high affinity cbb3-type cytochrome c oxidase (cbb3-cco) that enables respiration in low-oxygen conditions in other bacteria. R3bv2 cbb3-cco gene expression increased under low-oxygen conditions, and a cbb3-cco mutant strain grew more slowly in a microaerobic environment (0.5% O2). Although the cco mutant could still wilt tomato plants, symptom onset was significantly delayed relative to the wild-type parent strain. Further, the cco mutant did not colonize host stems or adhere to roots as effectively as wild type. These results suggest that R3bv2 encounters low-oxygen environments during its interactions with host plants and that the pathogen depends on this oxidase to help it succeed in planta.

scholarly journals Competition with the Wild-type Strain and a Phenotypic Conversion Strain of Ralstonia solanacearum in the Soil and Plants

2016 ◽  
Vol 28 (3) ◽  
pp. 133-141 ◽  
Author(s):  
Hiroki NAKAHARA ◽  
Taro MORI ◽  
Hiromi MATSUSAKI ◽  
Naotaka MATSUZOE
Keyword(s):  
Ralstonia Solanacearum ◽  
Type Strain ◽  
Wild Type Strain ◽  
Wild Type

scholarly journals CgHog1-Mediated CgRds2 Phosphorylation Alters Glycerophospholipid Composition To Coordinate Osmotic Stress in Candida glabrata

2019 ◽  
Vol 85 (6) ◽  
Author(s):  
Chengjin Wu ◽  
Jiali Zhang ◽  
Guoxing Zhu ◽  
Rui Yao ◽  
Xiulai Chen ◽  
...  
Keyword(s):  
Cell Growth ◽  
Osmotic Stress ◽  
Cell Survival ◽  
Type Strain ◽  
Candida Glabrata ◽  
Wild Type Strain ◽  
Membrane Integrity ◽  
Wild Type ◽  
Content Type ◽  
Zinc Cluster

ABSTRACT Under stress conditions, Hog1 is required for cell survival through transiently phosphorylating downstream targets and reprogramming gene expression. Here, we report that Candida glabrata Hog1 (CgHog1) interacts with and phosphorylates CgRds2, a zinc cluster transcription factor, in response to osmotic stress. Additionally, we found that deletion of CgRDS2 led to decreases in cell growth and cell survival by 23.4% and 39.6%, respectively, at 1.5 M NaCl, compared with levels of the wild-type strain. This is attributed to significant downregulation of the expression levels of glycerophospholipid metabolism genes. As a result, the content of total glycerophospholipid decreased by 30.3%. Membrane integrity also decreased 47.6% in the Cgrds2Δ strain at 1.5 M NaCl. In contrast, overexpression of CgRDS2 increased the cell growth and cell survival by 10.2% and 6.3%, respectively, owing to a significant increase in the total glycerophospholipid content and increased membrane integrity by 27.2% and 12.1%, respectively, at 1.5 M NaCl, compared with levels for the wild-type strain. However, a strain in which the CgRDS2 gene encodes the replacement of Ser64 and Thr97 residues with alanines (Cgrds22A), harboring a CgRds2 protein that was not phosphorylated by CgHog1, failed to promote glycerophospholipid metabolism and membrane integrity at 1.5 M NaCl. Thus, the above results demonstrate that CgHog1-mediated CgRds2 phosphorylation enhanced glycerophospholipid composition and membrane integrity to resist osmotic stress in C. glabrata. IMPORTANCE This study explored the role of CgHog1-mediated CgRds2 phosphorylation in response to osmotic stress in Candida glabrata. CgHog1 interacts with and phosphorylates CgRds2, a zinc cluster transcription factor, under osmotic stress. Phosphorylated CgRds2 plays an important role in increasing glycerophospholipid composition and membrane integrity, thereby enhancing cell growth and survival.

scholarly journals Bacterial Tomato Pathogen Ralstonia solanacearum Invasion Modulates Rhizosphere Compounds and Facilitates the Cascade Effect of Fungal Pathogen Fusarium solani

2020 ◽  
Vol 8 (6) ◽  
pp. 806
Author(s):  
Lv Su ◽  
Lifan Zhang ◽  
Duoqian Nie ◽  
Eiko E. Kuramae ◽  
Biao Shen ◽  
...  
Keyword(s):  
Phenolic Acids ◽  
Bacterial Wilt ◽  
Fusarium Solani ◽  
Ralstonia Solanacearum ◽  
High Throughput Sequencing ◽  
Rhizosphere Soil ◽  
Wilt Disease ◽  
Tomato Plants ◽  
Bacterial Wilt Disease ◽  
Pathogen Invasion

Soil-borne pathogen invasions can significantly change the microbial communities of the host rhizosphere. However, whether bacterial Ralstonia solanacearum pathogen invasion influences the abundance of fungal pathogens remains unclear. In this study, we combined high-throughput sequencing, qPCR, liquid chromatography and soil culture experiments to analyze the rhizosphere fungal composition, co-occurrence of fungal communities, copy numbers of functional genes, contents of phenolic acids and their associations in healthy and bacterial wilt-diseased tomato plants. We found that R. solanacearum invasion increased the abundance of the soil-borne pathogen Fusarium solani. The concentrations of three phenolic acids in the rhizosphere soil of bacterial wilt-diseased tomato plants were significantly higher than those in the rhizosphere soil of healthy tomato plants. In addition, the increased concentrations of phenolic acids significantly stimulated F. solani growth in the soil. Furthermore, a simple fungal network with fewer links, nodes and hubs (highly connected nodes) was found in the diseased tomato plant rhizosphere. These results indicate that once the symptom of bacterial wilt disease is observed in tomato, the roots of the wilt-diseased tomato plants need to be removed in a timely manner to prevent the enrichment of other fungal soil-borne pathogens. These findings provide some ecological clues for the mixed co-occurrence of bacterial wilt disease and other fungal soil-borne diseases.

scholarly journals Diffusible Signal Factor–Repressed Extracellular Traits Enable Attachment of Xylella fastidiosa to Insect Vectors and Transmission

2014 ◽  
Vol 104 (1) ◽  
pp. 27-33 ◽  
Author(s):  
Clelia Baccari ◽  
Nabil Killiny ◽  
Michael Ionescu ◽  
Rodrigo P. P. Almeida ◽  
Steven E. Lindow
Keyword(s):  
Type Strain ◽  
Host Plants ◽  
Wild Type Strain ◽  
Culture Supernatant ◽  
Culture Media ◽  
Xylella Fastidiosa ◽  
Xylem Sap ◽  
Wild Type ◽  
Diffusible Signal Factor ◽  
Type Strains

The hypothesis that a wild-type strain of Xylella fastidiosa would restore the ability of rpfF mutants blocked in diffusible signal factor production to be transmitted to new grape plants by the sharpshooter vector Graphocephala atropunctata was tested. While the rpfF mutant was very poorly transmitted by vectors irrespective of whether they had also fed on plants infected with the wild-type strain, wild-type strains were not efficiently transmitted if vectors had fed on plants infected with the rpfF mutant. About 100-fewer cells of a wild-type strain attached to wings of a vector when suspended in xylem sap from plants infected with an rpfF mutant than in sap from uninfected grapes. The frequency of transmission of cells suspended in sap from plants that were infected by the rpfF mutant was also reduced over threefold. Wild-type cells suspended in a culture supernatant of an rpfF mutant also exhibited 10-fold less adherence to wings than when suspended in uninoculated culture media. A factor released into the xylem by rpfF mutants, and to a lesser extent by the wild-type strain, thus inhibits their attachment to, and thus transmission by, sharpshooter vectors and may also enable them to move more readily through host plants.

scholarly journals Ralstonia solanacearum Requires PopS, an Ancient AvrE-Family Effector, for Virulence and To Overcome Salicylic Acid-Mediated Defenses during Tomato Pathogenesis

mBio ◽  
2013 ◽  
Vol 4 (6) ◽  
Author(s):  
Jonathan M. Jacobs ◽  
Annett Milling ◽  
Raka M. Mitra ◽  
Clifford S. Hogan ◽  
Florent Ailloud ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Bacterial Wilt ◽  
Ralstonia Solanacearum ◽  
Species Complex ◽  
Plant Defenses ◽  
Natural Infection ◽  
Wild Type ◽  
Tomato Plants ◽  
Content Type ◽  
Type Iii

ABSTRACTDuring bacterial wilt of tomato, the plant pathogen Ralstonia solanacearum upregulates expression ofpopS, which encodes a type III-secreted effector in the AvrE family. PopS is a core effector present in all sequenced strains in theR. solanacearumspecies complex. The phylogeny ofpopSmirrors that of the species complex as a whole, suggesting that this is an ancient, vertically inherited effector needed for association with plants. ApopSmutant ofR. solanacearumUW551 had reduced virulence on agriculturally importantSolanumspp., including potato and tomato plants. However, thepopSmutant had wild-type virulence on a weed host,Solanum dulcamara, suggesting that some species can avoid the effects of PopS. ThepopSmutant was also significantly delayed in colonization of tomato stems compared to the wild type. Some AvrE-type effectors from gammaproteobacteria suppress salicylic acid (SA)-mediated plant defenses, suggesting that PopS, a betaproteobacterial ortholog, has a similar function. Indeed, thepopSmutant induced significantly higher expression of tomato SA-triggered pathogenesis-related (PR) genes than the wild type. Further, pretreatment of roots with SA exacerbated thepopSmutant virulence defect. Finally, thepopSmutant had no colonization defect on SA-deficient NahG transgenic tomato plants. Together, these results indicate that this conserved effector suppresses SA-mediated defenses in tomato roots and stems, which areR. solanacearum’s natural infection sites. Interestingly, PopS did not trigger necrosis when heterologously expressed inNicotianaleaf tissue, unlike the AvrE homolog DspEPccfrom the necrotrophPectobacterium carotovorumsubsp.carotovorum. This is consistent with the differing pathogenesis modes of necrosis-causing gammaproteobacteria and biotrophicR. solanacearum.IMPORTANCEThe type III-secreted AvrE effector family is widely distributed in high-impact plant-pathogenic bacteria and is known to suppress plant defenses for virulence. We characterized the biology of PopS, the only AvrE homolog made by the bacterial wilt pathogenRalstonia solanacearum. To our knowledge, this is the first study ofR. solanacearumeffector function in roots and stems, the natural infection sites of this pathogen. Unlike the functionally redundantR. solanacearumeffectors studied to date, PopS is required for full virulence and wild-type colonization of two natural crop hosts.R. solanacearumis a biotrophic pathogen that causes a nonnecrotic wilt. Consistent with this, PopS suppressed plant defenses but did not elicit cell death, unlike AvrE homologs from necrosis-causing plant pathogens. We propose that AvrE family effectors have functionally diverged to adapt to the necrotic or nonnecrotic lifestyle of their respective pathogens.

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