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The Xylella fastidosa RTX operons: evidence for the evolution of protein mosaics through novel genetic exchanges.

Identifieur interne : 000223 ( Main/Exploration ); précédent : 000222; suivant : 000224

The Xylella fastidosa RTX operons: evidence for the evolution of protein mosaics through novel genetic exchanges.

Auteurs : Gregory A. Gambetta [France] ; Mark A. Matthews [États-Unis] ; Michael Syvanen [États-Unis]

Source :

RBID : pubmed:29728072

Descripteurs français

English descriptors

Abstract

BACKGROUND

Xylella fastidiosa (Xf) is a gram negative bacterium inhabiting the plant vascular system. In most species this bacterium lives as a benign symbiote, but in several agriculturally important plants (e.g. coffee, citrus, grapevine) Xf is pathogenic. Xf has four loci encoding homologues to hemolysin RTX proteins, virulence factors involved in a wide range of plant pathogen interactions.

RESULTS

We show that all four genes are expressed during pathogenesis in grapevine. The sequences from these four genes have a complex repetitive structure. At the C-termini, sequence diversity between strains is what would be expected from orthologous genes. However, within strains there is no N-terminal homology, indicating these loci encode RTXs of different functions and/or specificities. More striking is that many of the orthologous loci between strains share this extreme variation at the N-termini. Thus these RTX orthologues are most easily visualized as fusions between the orthologous C-termini and different N-termini. Further, the four genes are found in operons having a peculiar structure with an extensively duplicated module encoding a small protein with homology to the N-terminal region of the full length RTX. Surprisingly, some of these small peptides are most similar not to their corresponding full length RTX, but to the N-termini of RTXs from other Xf strains, and even other remotely related species.

CONCLUSIONS

These results demonstrate that these genes are expressed in planta during pathogenesis. Their structure suggests extensive evolutionary restructuring through horizontal gene transfers and heterologous recombination mechanisms. The sum of the evidence suggests these repetitive modules are a novel kind of mobile genetic element.


DOI: 10.1186/s12864-018-4731-9
PubMed: 29728072
PubMed Central: PMC5935956


Affiliations:


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Le document en format XML

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<term>Amino Acid Sequence (MeSH)</term>
<term>Bacterial Proteins (classification)</term>
<term>Bacterial Proteins (genetics)</term>
<term>Base Sequence (MeSH)</term>
<term>Evolution, Molecular (MeSH)</term>
<term>Gene Transfer, Horizontal (MeSH)</term>
<term>Genome, Bacterial (MeSH)</term>
<term>Hemolysin Proteins (classification)</term>
<term>Hemolysin Proteins (genetics)</term>
<term>Operon (genetics)</term>
<term>Phylogeny (MeSH)</term>
<term>Plant Diseases (microbiology)</term>
<term>Plant Leaves (genetics)</term>
<term>Plant Leaves (metabolism)</term>
<term>Plant Leaves (microbiology)</term>
<term>Sequence Alignment (MeSH)</term>
<term>Vitis (genetics)</term>
<term>Vitis (metabolism)</term>
<term>Vitis (microbiology)</term>
<term>Xylella (genetics)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Alignement de séquences (MeSH)</term>
<term>Feuilles de plante (génétique)</term>
<term>Feuilles de plante (microbiologie)</term>
<term>Feuilles de plante (métabolisme)</term>
<term>Génome bactérien (MeSH)</term>
<term>Hémolysines (classification)</term>
<term>Hémolysines (génétique)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Opéron (génétique)</term>
<term>Phylogenèse (MeSH)</term>
<term>Protéines bactériennes (classification)</term>
<term>Protéines bactériennes (génétique)</term>
<term>Séquence d'acides aminés (MeSH)</term>
<term>Séquence nucléotidique (MeSH)</term>
<term>Transfert horizontal de gène (MeSH)</term>
<term>Vitis (génétique)</term>
<term>Vitis (microbiologie)</term>
<term>Vitis (métabolisme)</term>
<term>Xylella (génétique)</term>
<term>Évolution moléculaire (MeSH)</term>
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<term>Bacterial Proteins</term>
<term>Hemolysin Proteins</term>
</keywords>
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<term>Bacterial Proteins</term>
<term>Hemolysin Proteins</term>
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<term>Hémolysines</term>
<term>Protéines bactériennes</term>
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<term>Operon</term>
<term>Plant Leaves</term>
<term>Vitis</term>
<term>Xylella</term>
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<term>Feuilles de plante</term>
<term>Hémolysines</term>
<term>Opéron</term>
<term>Protéines bactériennes</term>
<term>Vitis</term>
<term>Xylella</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en">
<term>Plant Leaves</term>
<term>Vitis</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Feuilles de plante</term>
<term>Maladies des plantes</term>
<term>Vitis</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
<term>Plant Leaves</term>
<term>Vitis</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr">
<term>Feuilles de plante</term>
<term>Vitis</term>
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<term>Amino Acid Sequence</term>
<term>Base Sequence</term>
<term>Evolution, Molecular</term>
<term>Gene Transfer, Horizontal</term>
<term>Genome, Bacterial</term>
<term>Phylogeny</term>
<term>Sequence Alignment</term>
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<term>Alignement de séquences</term>
<term>Génome bactérien</term>
<term>Phylogenèse</term>
<term>Séquence d'acides aminés</term>
<term>Séquence nucléotidique</term>
<term>Transfert horizontal de gène</term>
<term>Évolution moléculaire</term>
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<p>
<b>BACKGROUND</b>
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<p>Xylella fastidiosa (Xf) is a gram negative bacterium inhabiting the plant vascular system. In most species this bacterium lives as a benign symbiote, but in several agriculturally important plants (e.g. coffee, citrus, grapevine) Xf is pathogenic. Xf has four loci encoding homologues to hemolysin RTX proteins, virulence factors involved in a wide range of plant pathogen interactions.</p>
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<b>RESULTS</b>
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<p>We show that all four genes are expressed during pathogenesis in grapevine. The sequences from these four genes have a complex repetitive structure. At the C-termini, sequence diversity between strains is what would be expected from orthologous genes. However, within strains there is no N-terminal homology, indicating these loci encode RTXs of different functions and/or specificities. More striking is that many of the orthologous loci between strains share this extreme variation at the N-termini. Thus these RTX orthologues are most easily visualized as fusions between the orthologous C-termini and different N-termini. Further, the four genes are found in operons having a peculiar structure with an extensively duplicated module encoding a small protein with homology to the N-terminal region of the full length RTX. Surprisingly, some of these small peptides are most similar not to their corresponding full length RTX, but to the N-termini of RTXs from other Xf strains, and even other remotely related species.</p>
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<b>CONCLUSIONS</b>
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<p>These results demonstrate that these genes are expressed in planta during pathogenesis. Their structure suggests extensive evolutionary restructuring through horizontal gene transfers and heterologous recombination mechanisms. The sum of the evidence suggests these repetitive modules are a novel kind of mobile genetic element.</p>
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<AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Xylella fastidiosa (Xf) is a gram negative bacterium inhabiting the plant vascular system. In most species this bacterium lives as a benign symbiote, but in several agriculturally important plants (e.g. coffee, citrus, grapevine) Xf is pathogenic. Xf has four loci encoding homologues to hemolysin RTX proteins, virulence factors involved in a wide range of plant pathogen interactions.</AbstractText>
<AbstractText Label="RESULTS" NlmCategory="RESULTS">We show that all four genes are expressed during pathogenesis in grapevine. The sequences from these four genes have a complex repetitive structure. At the C-termini, sequence diversity between strains is what would be expected from orthologous genes. However, within strains there is no N-terminal homology, indicating these loci encode RTXs of different functions and/or specificities. More striking is that many of the orthologous loci between strains share this extreme variation at the N-termini. Thus these RTX orthologues are most easily visualized as fusions between the orthologous C-termini and different N-termini. Further, the four genes are found in operons having a peculiar structure with an extensively duplicated module encoding a small protein with homology to the N-terminal region of the full length RTX. Surprisingly, some of these small peptides are most similar not to their corresponding full length RTX, but to the N-termini of RTXs from other Xf strains, and even other remotely related species.</AbstractText>
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