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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 PBFC genes according to primary ecological classification of bacteria.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. Computations were made for (a) endophytes/symbionts, (b) saprophytes, (c) phytoparasites, (d) animal pathogens.
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f2: Co-occurrence network of PBFC genes according to primary ecological classification of bacteria.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. Computations were made for (a) endophytes/symbionts, (b) saprophytes, (c) phytoparasites, (d) animal pathogens.

Mentions: The genomes of 279 other sequenced Proteobacteria corresponding to saprophytes or endophytes/symbionts without established PGPR status, as well as pathogens of plants or animals, were studied as well. For the 56 endophytes/symbionts, PBFC genes were found in 0 (for phlACBD) to 36 (pqqBCDE) of the genomes (Table 1). Whereas two bacteria did not display any of the 23 PBFC genes, they were extensively found in others, with eight strains exhibiting as many as 10 PBFC genes each. Overall, the endophytes/symbionts harbored 6.1 ± 2.6 PBFC genes per strain, but the difference with PGPR was not significant (P = 0.06). Exact-Fisher pairwise tests of the co-occurrence of PBFC genes (P < 0.05) revealed four groups, i.e. hcnABC and pqqBCDE linked by pqqFG genes, as well as nifHDK/acdS and budAB/ipdC further apart (Fig. 2a).


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 PBFC genes according to primary ecological classification of bacteria.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. Computations were made for (a) endophytes/symbionts, (b) saprophytes, (c) phytoparasites, (d) animal pathogens.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Co-occurrence network of PBFC genes according to primary ecological classification of bacteria.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. Computations were made for (a) endophytes/symbionts, (b) saprophytes, (c) phytoparasites, (d) animal pathogens.
Mentions: The genomes of 279 other sequenced Proteobacteria corresponding to saprophytes or endophytes/symbionts without established PGPR status, as well as pathogens of plants or animals, were studied as well. For the 56 endophytes/symbionts, PBFC genes were found in 0 (for phlACBD) to 36 (pqqBCDE) of the genomes (Table 1). Whereas two bacteria did not display any of the 23 PBFC genes, they were extensively found in others, with eight strains exhibiting as many as 10 PBFC genes each. Overall, the endophytes/symbionts harbored 6.1 ± 2.6 PBFC genes per strain, but the difference with PGPR was not significant (P = 0.06). Exact-Fisher pairwise tests of the co-occurrence of PBFC genes (P < 0.05) revealed four groups, i.e. hcnABC and pqqBCDE linked by pqqFG genes, as well as nifHDK/acdS and budAB/ipdC further apart (Fig. 2a).

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