Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium

Effantin, Géraldine; Rivasseau, Corinne; Gromova, Marina; Bligny, Richard; Hugouvieux‐Cotte‐Pattat, Nicole

doi:10.1111/j.1365-2958.2011.07881.x

Cited by 54 publications

(42 citation statements)

References 43 publications

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“…Consequently, direct evidence of potential substrate assimilation by epiphytes is limited to a small number of bacteria and compounds. Moreover, it has not been shown which secondary plant metabolites reach the leaf cuticle or accumulate there in response to bacterial colonization, which is in contrast to the detection of signaling compounds inside plants as a consequence of bacterial presence (Ryu et al, 2004;Effantin et al, 2011;Pieterse et al, 2014).…”

Section: Introductionmentioning

confidence: 79%

Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves

Ryffel¹,

Helfrich²,

Kiefer³

et al. 2015

The ISME Journal

124

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The phyllosphere, which is defined as the parts of terrestrial plants above the ground, is a large habitat for different microorganisms that show a high extent of adaption to their environment. A number of hypotheses were generated by culture-independent functional genomics studies to explain the competitiveness of specialized bacteria in the phyllosphere. In contrast, in situ data at the metabolome level as a function of bacterial colonization are lacking. Here, we aimed to obtain new insights into the metabolic interplay between host and epiphytes upon colonization of Arabidopsis thaliana leaves in a controlled laboratory setting using environmental metabolomics approaches. Quantitative nuclear magnetic resonance (NMR) and imaging high-resolution mass spectrometry (IMS) methods were used to identify Arabidopsis leaf surface compounds and their possible involvement in the epiphytic lifestyle by relative changes in compound pools. The dominant carbohydrates on the leaf surfaces were sucrose, fructose and glucose. These sugars were significantly and specifically altered after epiphytic leaf colonization by the organoheterotroph Sphingomonas melonis or the phytopathogen Pseudomonas syringae pv. tomato, but only to a minor extent by the methylotroph Methylobacterium extorquens. In addition to carbohydrates, IMS revealed surprising alterations in arginine metabolism and phytoalexin biosynthesis that were dependent on the presence of bacteria, which might reflect the consequences of bacterial activity and the recognition of not only pathogens but also commensals by the plant. These results highlight the power of environmental metabolomics to aid in elucidating the molecular basis underlying plantepiphyte interactions in situ.

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Section: Introductionmentioning

confidence: 79%

Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves

Ryffel¹,

Helfrich²,

Kiefer³

et al. 2015

The ISME Journal

124

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“…These conditions could vary depending on the plant but also throughout the plant infection. For instance pH varies from about 5 at the early stage of infection to nearly 7 in the macerated tissue (43). In contrast to other D. dadantii 3937 pectate lyases, which are mainly induced in the presence of pectin degradation products and plant extracts, PelN regulation is mostly connected with environmental conditions, probably under the control of global regulators.…”

Section: Discussionmentioning

confidence: 99%

PelN Is a New Pectate Lyase of Dickeya dadantii with Unusual Characteristics

et al. 2013

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The plant-pathogenic bacterium Dickeya dadantii produces several pectinolytic enzymes that play a major role in the soft-rot disease. Eight characterized endopectate lyases are secreted in the extracellular medium by the type II secretion system, Out. They cleave internal glycosidic bonds of pectin, leading to plant tissue maceration. The D. dadantii pectate lyases belong to different families, namely, PL1, PL2, PL3, and PL9. Analysis of the D. dadantii 3937 genome revealed a gene encoding a new protein of the PL9 family, which already includes the secreted endopectate lyase PelL and the periplasmic exopectate lyase PelX. We demonstrated that PelN is an additional extracellular protein secreted by the Out system. However, PelN has some unusual characteristics. Although most pectate lyases require a very alkaline pH and Ca 2؉ for their activity, the PelN activity is optimal at pH 7.4 and in the presence of Fe 2؉ as a cofactor. PelN is only weakly affected by the degree of pectin methyl esterification. The PelN structural model, constructed on the basis of the PelL structure, suggests that the PelL global topology and its catalytic amino acids are conserved in PelN. Notable differences concern the presence of additional loops at the PelN surface, and the replacement of PelL charged residues, involved in substrate binding, by aromatic residues in PelN. The pelN expression is affected by different environmental conditions, such as pH, osmolarity, and temperature. It is controlled by the repressors KdgR and PecS and by the activator GacA, three regulators of D. dadantii pectinase genes. Since a pelN mutant had reduced virulence on chicory leaves, the PelN enzyme plays a role in plant infection, despite its low specific activity and its unusual cofactor requirement.

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“…Pectobacterium and Dickeya, like many bacteria, encode the butanediol pathway, which results in the production of the potent insect attractant acetoin, suggesting that these bacteria may attract insect vectors to infected plant material through this route (37,100). Once associated with an insect, some isolates of Pectobacterium carotovorum can infect and persist in D. melanogaster and activate an immune response (8,9).…”

Section: Insects As Vectors and Alternate Hostsmentioning

confidence: 99%

The Role of Secretion Systems and Small Molecules in Soft-Rot Enterobacteriaceae Pathogenicity

Charkowski¹,

Blanco

Condemine

et al. 2012

Annu. Rev. Phytopathol.

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220

251

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Soft-rot Enterobacteriaceae (SRE), which belong to the genera Pectobacterium and Dickeya, consist mainly of broad host-range pathogens that cause wilt, rot, and blackleg diseases on a wide range of plants. They are found in plants, insects, soil, and water in agricultural regions worldwide. SRE encode all six known protein secretion systems present in gram-negative bacteria, and these systems are involved in attacking host plants and competing bacteria. They also produce and detect multiple types of small molecules to coordinate pathogenesis, modify the plant environment, attack competing microbes, and perhaps to attract insect vectors. This review integrates new information about the role protein secretion and detection and production of ions and small molecules play in soft-rot pathogenicity.

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Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium

Cited by 54 publications

References 43 publications

Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves

Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves

PelN Is a New Pectate Lyase of Dickeya dadantii with Unusual Characteristics

The Role of Secretion Systems and Small Molecules in Soft-Rot Enterobacteriaceae Pathogenicity

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