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Analysis of genes contributing to plant-beneficial functions in Plant Growth-Promoting Rhizobacteria and related Proteobacteria.

Bruto M, Prigent-Combaret C, Muller D, Moënne-Loccoz Y - Sci Rep (2014)

Bottom Line: Here, this issue was targeted using 23 genes contributing directly or indirectly to established PGPR effects, based on genome sequence analysis of 304 contrasted Alpha- Beta- and Gammaproteobacteria.Most of the 23 genes studied were also found in non-PGPR Proteobacteria and none of them were common to all 25 PGPR genomes studied.However, ancestral character reconstruction indicated that gene transfers -predominantly ancient- resulted in characteristic gene combinations according to taxonomic subgroups of PGPR strains.

View Article: PubMed Central - PubMed

Affiliation: 1] Université de Lyon, F-69622, Lyon, France [2] Université Lyon 1, Villeurbanne, France [3] CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France.

ABSTRACT
The positive effects of root-colonizing bacteria cooperating with plants lead to improved growth and/or health of their eukaryotic hosts. Some of these Plant Growth-Promoting Rhizobacteria (PGPR) display several plant-beneficial properties, suggesting that the accumulation of the corresponding genes could have been selected in these bacteria. Here, this issue was targeted using 23 genes contributing directly or indirectly to established PGPR effects, based on genome sequence analysis of 304 contrasted Alpha- Beta- and Gammaproteobacteria. Most of the 23 genes studied were also found in non-PGPR Proteobacteria and none of them were common to all 25 PGPR genomes studied. However, ancestral character reconstruction indicated that gene transfers -predominantly ancient- resulted in characteristic gene combinations according to taxonomic subgroups of PGPR strains. This suggests that the PGPR-plant cooperation could have established separately in various taxa, yielding PGPR strains that use different gene assortments. The number of genes contributing to plant-beneficial functions increased along the continuum -animal pathogens, phytopathogens, saprophytes, endophytes/symbionts, PGPR- indicating that the accumulation of these genes (and possibly of different plant-beneficial traits) might be an intrinsic PGPR feature. This work uncovered preferential associations occurring between certain genes contributing to phytobeneficial traits and provides new insights into the emergence of PGPR bacteria.

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Co-occurrence network of the PBFC genes for the 304 genomes.The genes are depicted with a colored circle according to their encoded function. Each co-occurrence is represented by an edge linking the corresponding genes and materialized by a line. nirK does not appear in the figure because this gene did not shown any significant co-occurrence with other PBFC gene(s).
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f4: Co-occurrence network of the PBFC genes for the 304 genomes.The genes are depicted with a colored circle according to their encoded function. Each co-occurrence is represented by an edge linking the corresponding genes and materialized by a line. nirK does not appear in the figure because this gene did not shown any significant co-occurrence with other PBFC gene(s).

Mentions: The comparison of the 304 genomes showed that, unexpectedly, PBFC genes previously described as clustered (even forming operons in many cases) were not necessarily found together in a same genome (Fig. 4). For instance, pqqFG were close to pqqBCDE in Pseudomonas (and a few other genera), whereas pqqBCDE occurred without pqqG (encoding a family-S9 peptidase) and especially pqqF (encoding a family-M16 peptidase) in most other Proteobacteria. Similar observations were made for phlD and phlACB, as well as budAB and budC. Yet, the groups revealed by exact-Fisher pairwise tests (P < 0.01) corresponded mainly to genes involved in a same function (Fig. 3). This analysis showed that hcnABC and phlD linked the other phl genes with the six pqq genes, themselves linked to budABC/ipdC via nirK and to nifHDK. nifHDK were also linked, separately, to ppdC and to acdS.


Analysis of genes contributing to plant-beneficial functions in Plant Growth-Promoting Rhizobacteria and related Proteobacteria.

Bruto M, Prigent-Combaret C, Muller D, Moënne-Loccoz Y - Sci Rep (2014)

Co-occurrence network of the PBFC genes for the 304 genomes.The genes are depicted with a colored circle according to their encoded function. Each co-occurrence is represented by an edge linking the corresponding genes and materialized by a line. nirK does not appear in the figure because this gene did not shown any significant co-occurrence with other PBFC gene(s).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4151105&req=5

f4: Co-occurrence network of the PBFC genes for the 304 genomes.The genes are depicted with a colored circle according to their encoded function. Each co-occurrence is represented by an edge linking the corresponding genes and materialized by a line. nirK does not appear in the figure because this gene did not shown any significant co-occurrence with other PBFC gene(s).
Mentions: The comparison of the 304 genomes showed that, unexpectedly, PBFC genes previously described as clustered (even forming operons in many cases) were not necessarily found together in a same genome (Fig. 4). For instance, pqqFG were close to pqqBCDE in Pseudomonas (and a few other genera), whereas pqqBCDE occurred without pqqG (encoding a family-S9 peptidase) and especially pqqF (encoding a family-M16 peptidase) in most other Proteobacteria. Similar observations were made for phlD and phlACB, as well as budAB and budC. Yet, the groups revealed by exact-Fisher pairwise tests (P < 0.01) corresponded mainly to genes involved in a same function (Fig. 3). This analysis showed that hcnABC and phlD linked the other phl genes with the six pqq genes, themselves linked to budABC/ipdC via nirK and to nifHDK. nifHDK were also linked, separately, to ppdC and to acdS.

Bottom Line: Here, this issue was targeted using 23 genes contributing directly or indirectly to established PGPR effects, based on genome sequence analysis of 304 contrasted Alpha- Beta- and Gammaproteobacteria.Most of the 23 genes studied were also found in non-PGPR Proteobacteria and none of them were common to all 25 PGPR genomes studied.However, ancestral character reconstruction indicated that gene transfers -predominantly ancient- resulted in characteristic gene combinations according to taxonomic subgroups of PGPR strains.

View Article: PubMed Central - PubMed

Affiliation: 1] Université de Lyon, F-69622, Lyon, France [2] Université Lyon 1, Villeurbanne, France [3] CNRS, UMR5557, Ecologie Microbienne, Villeurbanne, France.

ABSTRACT
The positive effects of root-colonizing bacteria cooperating with plants lead to improved growth and/or health of their eukaryotic hosts. Some of these Plant Growth-Promoting Rhizobacteria (PGPR) display several plant-beneficial properties, suggesting that the accumulation of the corresponding genes could have been selected in these bacteria. Here, this issue was targeted using 23 genes contributing directly or indirectly to established PGPR effects, based on genome sequence analysis of 304 contrasted Alpha- Beta- and Gammaproteobacteria. Most of the 23 genes studied were also found in non-PGPR Proteobacteria and none of them were common to all 25 PGPR genomes studied. However, ancestral character reconstruction indicated that gene transfers -predominantly ancient- resulted in characteristic gene combinations according to taxonomic subgroups of PGPR strains. This suggests that the PGPR-plant cooperation could have established separately in various taxa, yielding PGPR strains that use different gene assortments. The number of genes contributing to plant-beneficial functions increased along the continuum -animal pathogens, phytopathogens, saprophytes, endophytes/symbionts, PGPR- indicating that the accumulation of these genes (and possibly of different plant-beneficial traits) might be an intrinsic PGPR feature. This work uncovered preferential associations occurring between certain genes contributing to phytobeneficial traits and provides new insights into the emergence of PGPR bacteria.

Show MeSH