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Xylan Utilization Regulon in Xanthomonas citri pv. citri Strain 306: Gene Expression and Utilization of Oligoxylosides

Identifieur interne : 000375 ( Main/Exploration ); précédent : 000374; suivant : 000376

Xylan Utilization Regulon in Xanthomonas citri pv. citri Strain 306: Gene Expression and Utilization of Oligoxylosides

Auteurs : V. Chow [États-Unis] ; D. Shantharaj [États-Unis] ; Y. Guo [États-Unis] ; G. Nong [États-Unis] ; G. V. Minsavage [États-Unis] ; J. B. Jones [États-Unis] ; J. F. Preston [États-Unis]

Source :

RBID : PMC:4345395

Abstract

Xanthomonas citri pv. citri strain 306 (Xcc306), a causative agent of citrus canker, produces endoxylanases that catalyze the depolymerization of cell wall-associated xylans. In the sequenced genomes of all plant-pathogenic xanthomonads, genes encoding xylanolytic enzymes are clustered in three adjacent operons. In Xcc306, these consecutive operons contain genes encoding the glycoside hydrolase family 10 (GH10) endoxylanases Xyn10A and Xyn10C, the agu67 gene, encoding a GH67 α-glucuronidase (Agu67), the xyn43E gene, encoding a putative GH43 α-l-arabinofuranosidase, and the xyn43F gene, encoding a putative β-xylosidase. Recombinant Xyn10A and Xyn10C convert polymeric 4-O-methylglucuronoxylan (MeGXn) to oligoxylosides methylglucuronoxylotriose (MeGX3), xylotriose (X3), and xylobiose (X2). Xcc306 completely utilizes MeGXn predigested with Xyn10A or Xyn10C but shows little utilization of MeGXn. Xcc306 with a deletion in the gene encoding α-glucuronidase (Xcc306 Δagu67) will not utilize MeGX3 for growth, demonstrating the role of Agu67 in the complete utilization of GH10-digested MeGXn. Preferential growth on oligoxylosides compared to growth on polymeric MeGXn indicates that GH10 xylanases, either secreted by Xcc306 in planta or produced by the plant host, generate oligoxylosides that are processed by Xyn10 xylanases and Agu67 residing in the periplasm. Coordinate induction by oligoxylosides of xyn10, agu67, cirA, the tonB receptor, and other genes within these three operons indicates that they constitute a regulon that is responsive to the oligoxylosides generated by the action of Xcc306 GH10 xylanases on MeGXn. The combined expression of genes in this regulon may allow scavenging of oligoxylosides derived from cell wall deconstruction, thereby contributing to the tissue colonization and/or survival of Xcc306 and, ultimately, to plant disease.


Url:
DOI: 10.1128/AEM.03091-14
PubMed: 25595763
PubMed Central: 4345395


Affiliations:


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Le document en format XML

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pv. citri Strain 306: Gene Expression and Utilization of Oligoxylosides</title>
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<title xml:lang="en" level="a" type="main">Xylan Utilization Regulon in
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pv. citri Strain 306: Gene Expression and Utilization of Oligoxylosides</title>
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<name sortKey="Chow, V" sort="Chow, V" uniqKey="Chow V" first="V." last="Chow">V. Chow</name>
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<named-content content-type="genus-species">Xanthomonas citri</named-content>
pv. citri strain 306 (
<italic>Xcc</italic>
306), a causative agent of citrus canker, produces endoxylanases that catalyze the depolymerization of cell wall-associated xylans. In the sequenced genomes of all plant-pathogenic xanthomonads, genes encoding xylanolytic enzymes are clustered in three adjacent operons. In
<italic>Xcc</italic>
306, these consecutive operons contain genes encoding the glycoside hydrolase family 10 (GH10) endoxylanases Xyn10A and Xyn10C, the
<italic>agu67</italic>
gene, encoding a GH67 α-glucuronidase (Agu67), the
<italic>xyn43E</italic>
gene, encoding a putative GH43 α-
<sc>l</sc>
-arabinofuranosidase, and the
<italic>xyn43F</italic>
gene, encoding a putative β-xylosidase. Recombinant Xyn10A and Xyn10C convert polymeric 4-
<italic>O</italic>
-methylglucuronoxylan (MeGX
<sub>
<italic>n</italic>
</sub>
) to oligoxylosides methylglucuronoxylotriose (MeGX
<sub>3</sub>
), xylotriose (X
<sub>3</sub>
), and xylobiose (X
<sub>2</sub>
).
<italic>Xcc</italic>
306 completely utilizes MeGX
<sub>
<italic>n</italic>
</sub>
predigested with Xyn10A or Xyn10C but shows little utilization of MeGX
<sub>
<italic>n</italic>
</sub>
.
<italic>Xcc</italic>
306 with a deletion in the gene encoding α-glucuronidase (
<italic>Xcc</italic>
306 Δ
<italic>agu67</italic>
) will not utilize MeGX
<sub>3</sub>
for growth, demonstrating the role of Agu67 in the complete utilization of GH10-digested MeGX
<sub>
<italic>n</italic>
</sub>
. Preferential growth on oligoxylosides compared to growth on polymeric MeGX
<sub>
<italic>n</italic>
</sub>
indicates that GH10 xylanases, either secreted by
<italic>Xcc</italic>
306
<italic>in planta</italic>
or produced by the plant host, generate oligoxylosides that are processed by Xyn10 xylanases and Agu67 residing in the periplasm. Coordinate induction by oligoxylosides of
<italic>xyn10</italic>
,
<italic>agu67</italic>
,
<italic>cirA</italic>
, the
<italic>tonB</italic>
receptor, and other genes within these three operons indicates that they constitute a regulon that is responsive to the oligoxylosides generated by the action of
<italic>Xcc</italic>
306 GH10 xylanases on MeGX
<sub>
<italic>n</italic>
</sub>
. The combined expression of genes in this regulon may allow scavenging of oligoxylosides derived from cell wall deconstruction, thereby contributing to the tissue colonization and/or survival of
<italic>Xcc</italic>
306 and, ultimately, to plant disease.</p>
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</front>
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<country name="États-Unis">
<region name="Floride">
<name sortKey="Chow, V" sort="Chow, V" uniqKey="Chow V" first="V." last="Chow">V. Chow</name>
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<name sortKey="Guo, Y" sort="Guo, Y" uniqKey="Guo Y" first="Y." last="Guo">Y. Guo</name>
<name sortKey="Jones, J B" sort="Jones, J B" uniqKey="Jones J" first="J. B." last="Jones">J. B. Jones</name>
<name sortKey="Minsavage, G V" sort="Minsavage, G V" uniqKey="Minsavage G" first="G. V." last="Minsavage">G. V. Minsavage</name>
<name sortKey="Nong, G" sort="Nong, G" uniqKey="Nong G" first="G." last="Nong">G. Nong</name>
<name sortKey="Preston, J F" sort="Preston, J F" uniqKey="Preston J" first="J. F." last="Preston">J. F. Preston</name>
<name sortKey="Shantharaj, D" sort="Shantharaj, D" uniqKey="Shantharaj D" first="D." last="Shantharaj">D. Shantharaj</name>
</country>
</tree>
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