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A TAL effector-like protein of an endofungal bacterium increases the stress tolerance and alters the transcriptome of the host.

Identifieur interne : 000236 ( Main/Exploration ); précédent : 000235; suivant : 000237

A TAL effector-like protein of an endofungal bacterium increases the stress tolerance and alters the transcriptome of the host.

Auteurs : Morgan E. Carter [États-Unis] ; Sara C D. Carpenter [États-Unis] ; Zoë E. Dubrow [États-Unis] ; Mark R. Sabol [États-Unis] ; Fabio C. Rinaldi [États-Unis] ; Olga A. Lastovetsky [États-Unis] ; Stephen J. Mondo [États-Unis] ; Teresa E. Pawlowska [États-Unis] ; Adam J. Bogdanove [États-Unis]

Source :

RBID : pubmed:32632014

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English descriptors

Abstract

Symbioses of bacteria with fungi have only recently been described and are poorly understood. In the symbiosis of Mycetohabitans (formerly Burkholderia) rhizoxinica with the fungus Rhizopus microsporus, bacterial type III (T3) secretion is known to be essential. Proteins resembling T3-secreted transcription activator-like (TAL) effectors of plant pathogenic bacteria are encoded in the three sequenced Mycetohabitans spp. genomes. TAL effectors nuclear-localize in plants, where they bind and activate genes important in disease. The Burkholderia TAL-like (Btl) proteins bind DNA but lack the N- and C-terminal regions, in which TAL effectors harbor their T3 and nuclear localization signals, and activation domain. We characterized a Btl protein, Btl19-13, and found that, despite the structural differences, it can be T3-secreted and can nuclear-localize. A btl19-13 gene knockout did not prevent the bacterium from infecting the fungus, but the fungus became less tolerant to cell membrane stress. Btl19-13 did not alter transcription in a plant-based reporter assay, but 15 R. microsporus genes were differentially expressed in comparisons both of the fungus infected with the wild-type bacterium vs. the mutant and with the mutant vs. a complemented strain. Southern blotting revealed btl genes in 14 diverse Mycetohabitans isolates. However, banding patterns and available sequences suggest variation, and the btl19-13 phenotype could not be rescued by a btl gene from a different strain. Our findings support the conclusion that Btl proteins are effectors that act on host DNA and play important but varied or possibly host genotype-specific roles in the M. rhizoxinica-R. microsporus symbiosis.

DOI: 10.1073/pnas.2003857117
PubMed: 32632014
PubMed Central: PMC7382252


Affiliations:


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<term>Burkholderia (metabolism)</term>
<term>Burkholderia (physiology)</term>
<term>Gene Expression Regulation, Fungal (genetics)</term>
<term>Rhizopus (genetics)</term>
<term>Rhizopus (metabolism)</term>
<term>Stress, Physiological (genetics)</term>
<term>Symbiosis (genetics)</term>
<term>Transcription Activator-Like Effectors (genetics)</term>
<term>Transcription Activator-Like Effectors (metabolism)</term>
<term>Transcriptome (genetics)</term>
<term>Type III Secretion Systems (genetics)</term>
<term>Type III Secretion Systems (metabolism)</term>
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<term>Burkholderia (génétique)</term>
<term>Burkholderia (métabolisme)</term>
<term>Burkholderia (physiologie)</term>
<term>Effecteurs de type activateur de transcription (génétique)</term>
<term>Effecteurs de type activateur de transcription (métabolisme)</term>
<term>Rhizopus (génétique)</term>
<term>Rhizopus (métabolisme)</term>
<term>Régulation de l'expression des gènes fongiques (génétique)</term>
<term>Stress physiologique (génétique)</term>
<term>Symbiose (génétique)</term>
<term>Systèmes de sécrétion de type III (génétique)</term>
<term>Systèmes de sécrétion de type III (métabolisme)</term>
<term>Transcriptome (génétique)</term>
</keywords>
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<term>Transcription Activator-Like Effectors</term>
<term>Type III Secretion Systems</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Burkholderia</term>
<term>Gene Expression Regulation, Fungal</term>
<term>Rhizopus</term>
<term>Stress, Physiological</term>
<term>Symbiosis</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Burkholderia</term>
<term>Effecteurs de type activateur de transcription</term>
<term>Rhizopus</term>
<term>Régulation de l'expression des gènes fongiques</term>
<term>Stress physiologique</term>
<term>Symbiose</term>
<term>Systèmes de sécrétion de type III</term>
<term>Transcriptome</term>
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<term>Rhizopus</term>
<term>Transcription Activator-Like Effectors</term>
<term>Type III Secretion Systems</term>
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<div type="abstract" xml:lang="en">Symbioses of bacteria with fungi have only recently been described and are poorly understood. In the symbiosis of
<i>Mycetohabitans</i>
(formerly
<i>Burkholderia</i>
)
<i>rhizoxinica</i>
with the fungus
<i>Rhizopus microsporus</i>
, bacterial type III (T3) secretion is known to be essential. Proteins resembling T3-secreted transcription activator-like (TAL) effectors of plant pathogenic bacteria are encoded in the three sequenced
<i>Mycetohabitans</i>
spp. genomes. TAL effectors nuclear-localize in plants, where they bind and activate genes important in disease. The Burkholderia TAL-like (Btl) proteins bind DNA but lack the N- and C-terminal regions, in which TAL effectors harbor their T3 and nuclear localization signals, and activation domain. We characterized a Btl protein, Btl19-13, and found that, despite the structural differences, it can be T3-secreted and can nuclear-localize. A
<i>btl19</i>
<i>-13</i>
gene knockout did not prevent the bacterium from infecting the fungus, but the fungus became less tolerant to cell membrane stress. Btl19-13 did not alter transcription in a plant-based reporter assay, but 15
<i>R. microsporus</i>
genes were differentially expressed in comparisons both of the fungus infected with the wild-type bacterium vs. the mutant and with the mutant vs. a complemented strain. Southern blotting revealed
<i>btl</i>
genes in 14 diverse
<i>Mycetohabitans</i>
isolates. However, banding patterns and available sequences suggest variation, and the
<i>btl19-13</i>
phenotype could not be rescued by a
<i>btl</i>
gene from a different strain. Our findings support the conclusion that Btl proteins are effectors that act on host DNA and play important but varied or possibly host genotype-specific roles in the
<i>M. rhizoxinica</i>
-
<i>R. microsporus</i>
symbiosis.</div>
</front>
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<Month>09</Month>
<Day>17</Day>
</DateRevised>
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<Abstract>
<AbstractText>Symbioses of bacteria with fungi have only recently been described and are poorly understood. In the symbiosis of
<i>Mycetohabitans</i>
(formerly
<i>Burkholderia</i>
)
<i>rhizoxinica</i>
with the fungus
<i>Rhizopus microsporus</i>
, bacterial type III (T3) secretion is known to be essential. Proteins resembling T3-secreted transcription activator-like (TAL) effectors of plant pathogenic bacteria are encoded in the three sequenced
<i>Mycetohabitans</i>
spp. genomes. TAL effectors nuclear-localize in plants, where they bind and activate genes important in disease. The Burkholderia TAL-like (Btl) proteins bind DNA but lack the N- and C-terminal regions, in which TAL effectors harbor their T3 and nuclear localization signals, and activation domain. We characterized a Btl protein, Btl19-13, and found that, despite the structural differences, it can be T3-secreted and can nuclear-localize. A
<i>btl19</i>
<i>-13</i>
gene knockout did not prevent the bacterium from infecting the fungus, but the fungus became less tolerant to cell membrane stress. Btl19-13 did not alter transcription in a plant-based reporter assay, but 15
<i>R. microsporus</i>
genes were differentially expressed in comparisons both of the fungus infected with the wild-type bacterium vs. the mutant and with the mutant vs. a complemented strain. Southern blotting revealed
<i>btl</i>
genes in 14 diverse
<i>Mycetohabitans</i>
isolates. However, banding patterns and available sequences suggest variation, and the
<i>btl19-13</i>
phenotype could not be rescued by a
<i>btl</i>
gene from a different strain. Our findings support the conclusion that Btl proteins are effectors that act on host DNA and play important but varied or possibly host genotype-specific roles in the
<i>M. rhizoxinica</i>
-
<i>R. microsporus</i>
symbiosis.</AbstractText>
<CopyrightInformation>Copyright © 2020 the Author(s). Published by PNAS.</CopyrightInformation>
</Abstract>
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<LastName>Carter</LastName>
<ForeName>Morgan E</ForeName>
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<Identifier Source="ORCID">0000-0001-5639-2013</Identifier>
<AffiliationInfo>
<Affiliation>Section of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY 14853.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Carpenter</LastName>
<ForeName>Sara C D</ForeName>
<Initials>SCD</Initials>
<AffiliationInfo>
<Affiliation>Section of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY 14853.</Affiliation>
</AffiliationInfo>
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<LastName>Dubrow</LastName>
<ForeName>Zoë E</ForeName>
<Initials>ZE</Initials>
<AffiliationInfo>
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</AffiliationInfo>
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<Initials>MR</Initials>
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</AffiliationInfo>
</Author>
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<AffiliationInfo>
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</AffiliationInfo>
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<LastName>Lastovetsky</LastName>
<ForeName>Olga A</ForeName>
<Initials>OA</Initials>
<Identifier Source="ORCID">0000-0002-3989-0915</Identifier>
<AffiliationInfo>
<Affiliation>Department of Microbiology, Cornell University, Ithaca, NY 14853.</Affiliation>
</AffiliationInfo>
</Author>
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