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Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics.

Bringel F, Couée I - Front Microbiol (2015)

Bottom Line: Phyllosphere microbiota are related to original and specific processes at the interface between plants, microorganisms and the atmosphere.Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere.This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Genetics, Genomics, and Microbiology, Université de Strasbourg/CNRS, UNISTRA UMR 7156 Strasbourg, France.

ABSTRACT
The phyllosphere, which lato sensu consists of the aerial parts of plants, and therefore primarily, of the set of photosynthetic leaves, is one of the most prevalent microbial habitats on earth. Phyllosphere microbiota are related to original and specific processes at the interface between plants, microorganisms and the atmosphere. Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere. This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere. Highlights • The phyllosphere is one of the most prevalent microbial habitats on earth. • Phyllosphere microbiota colonize extreme, stressful, and changing environments. • Plants, phyllosphere microbiota and the atmosphere present a dynamic continuum. • Phyllosphere microbiota interact with the dynamics of volatile organic compounds and atmospheric trace gasses.

No MeSH data available.


Related in: MedlinePlus

High-throughput molecular analysis of microbial communities of the phyllosphere: from direct DNA sequencing to sequencing of prokaryotic and eukaryotic taxonomical markers. The present range of published studies covers a significant number of plant host species in various developmental and spatio-temporal contexts and under the influence of different environmental factors. The articles presented in Supplementary Table S1 represent a selection of studies that were performed in the last years using NGS technologies. Further studies can be found in tables of other recent reviews (Rastogi et al., 2013; Knief, 2014; Müller and Ruppel, 2014). Taken together, these studies give a dynamic view of phyllosphere microbiota biodiversity, metabolisms, and environmental plasticity.
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Figure 2: High-throughput molecular analysis of microbial communities of the phyllosphere: from direct DNA sequencing to sequencing of prokaryotic and eukaryotic taxonomical markers. The present range of published studies covers a significant number of plant host species in various developmental and spatio-temporal contexts and under the influence of different environmental factors. The articles presented in Supplementary Table S1 represent a selection of studies that were performed in the last years using NGS technologies. Further studies can be found in tables of other recent reviews (Rastogi et al., 2013; Knief, 2014; Müller and Ruppel, 2014). Taken together, these studies give a dynamic view of phyllosphere microbiota biodiversity, metabolisms, and environmental plasticity.

Mentions: The structural analysis of phyllosphere microbial communities (Ruinen, 1961; Hirano and Upper, 2000; Schreiber et al., 2004) has been deeply renewed by the development of culture-independent mass sequencing in a growing number of plant species and cultivars of agricultural or ecological interest (Figure 2). Supplementary Table S1 gives a list of phyllosphere microbiota that have been characterized by high-throughput molecular analysis and summarizes the main findings of these studies. It must be noted that up to now most of these studies are based mainly on sequencing of PCR-amplified DNA-level conserved taxonomic markers (16S rRNA for bacterial taxonomy; 18S rRNA and Internal Transcribed Spacer ribosomal regions for yeasts and fungi) and, less frequently, on markers of biological functions, such as key genes related to a given metabolism, to a regulatory process or to an adaptive mechanism (Figure 2; Supplementary Table S1). A potential bias resulting from primer design and PCR reaction conditions has been described (Mao et al., 2012). Most 16S rRNA universal primers also amplify chloroplast and mitochondrial sequences that result in less rRNA sequences of interest matched to bacteria (Santhanam et al., 2014; Jo et al., 2015). To minimize the amplification of host plant DNA, primer 799F was designed to exclude chloroplast DNA, and the mtDNA sequences can be separated from the PCR-amplified bacterial sequences by size fractionation (Chelius and Triplett, 2001). Primer 799F has become a “standard” forward primer in recent phyllosphere microbiota analysis (Redford et al., 2010; Bodenhausen et al., 2013, 2014; Horton et al., 2014; Kembel et al., 2014; Maignien et al., 2014; Perazzolli et al., 2014; Santhanam et al., 2014; Williams and Marco, 2014; Copeland et al., 2015). Nevertheless, using primer 799F leads to systematic non-detection or underestimation of a few taxa such as cyanobacteria (Chelius and Triplett, 2001). Such bias can typically be avoided by direct mass sequencing and analysis of metagenomic DNA, which has been used so far only in a few studies of phyllosphere microbiota studies (Supplementary Table S1), but which is in constant increase as a result of ever lower sequencing costs and of ever improving bioinformatics tools.


Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics.

Bringel F, Couée I - Front Microbiol (2015)

High-throughput molecular analysis of microbial communities of the phyllosphere: from direct DNA sequencing to sequencing of prokaryotic and eukaryotic taxonomical markers. The present range of published studies covers a significant number of plant host species in various developmental and spatio-temporal contexts and under the influence of different environmental factors. The articles presented in Supplementary Table S1 represent a selection of studies that were performed in the last years using NGS technologies. Further studies can be found in tables of other recent reviews (Rastogi et al., 2013; Knief, 2014; Müller and Ruppel, 2014). Taken together, these studies give a dynamic view of phyllosphere microbiota biodiversity, metabolisms, and environmental plasticity.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4440916&req=5

Figure 2: High-throughput molecular analysis of microbial communities of the phyllosphere: from direct DNA sequencing to sequencing of prokaryotic and eukaryotic taxonomical markers. The present range of published studies covers a significant number of plant host species in various developmental and spatio-temporal contexts and under the influence of different environmental factors. The articles presented in Supplementary Table S1 represent a selection of studies that were performed in the last years using NGS technologies. Further studies can be found in tables of other recent reviews (Rastogi et al., 2013; Knief, 2014; Müller and Ruppel, 2014). Taken together, these studies give a dynamic view of phyllosphere microbiota biodiversity, metabolisms, and environmental plasticity.
Mentions: The structural analysis of phyllosphere microbial communities (Ruinen, 1961; Hirano and Upper, 2000; Schreiber et al., 2004) has been deeply renewed by the development of culture-independent mass sequencing in a growing number of plant species and cultivars of agricultural or ecological interest (Figure 2). Supplementary Table S1 gives a list of phyllosphere microbiota that have been characterized by high-throughput molecular analysis and summarizes the main findings of these studies. It must be noted that up to now most of these studies are based mainly on sequencing of PCR-amplified DNA-level conserved taxonomic markers (16S rRNA for bacterial taxonomy; 18S rRNA and Internal Transcribed Spacer ribosomal regions for yeasts and fungi) and, less frequently, on markers of biological functions, such as key genes related to a given metabolism, to a regulatory process or to an adaptive mechanism (Figure 2; Supplementary Table S1). A potential bias resulting from primer design and PCR reaction conditions has been described (Mao et al., 2012). Most 16S rRNA universal primers also amplify chloroplast and mitochondrial sequences that result in less rRNA sequences of interest matched to bacteria (Santhanam et al., 2014; Jo et al., 2015). To minimize the amplification of host plant DNA, primer 799F was designed to exclude chloroplast DNA, and the mtDNA sequences can be separated from the PCR-amplified bacterial sequences by size fractionation (Chelius and Triplett, 2001). Primer 799F has become a “standard” forward primer in recent phyllosphere microbiota analysis (Redford et al., 2010; Bodenhausen et al., 2013, 2014; Horton et al., 2014; Kembel et al., 2014; Maignien et al., 2014; Perazzolli et al., 2014; Santhanam et al., 2014; Williams and Marco, 2014; Copeland et al., 2015). Nevertheless, using primer 799F leads to systematic non-detection or underestimation of a few taxa such as cyanobacteria (Chelius and Triplett, 2001). Such bias can typically be avoided by direct mass sequencing and analysis of metagenomic DNA, which has been used so far only in a few studies of phyllosphere microbiota studies (Supplementary Table S1), but which is in constant increase as a result of ever lower sequencing costs and of ever improving bioinformatics tools.

Bottom Line: Phyllosphere microbiota are related to original and specific processes at the interface between plants, microorganisms and the atmosphere.Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere.This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Genetics, Genomics, and Microbiology, Université de Strasbourg/CNRS, UNISTRA UMR 7156 Strasbourg, France.

ABSTRACT
The phyllosphere, which lato sensu consists of the aerial parts of plants, and therefore primarily, of the set of photosynthetic leaves, is one of the most prevalent microbial habitats on earth. Phyllosphere microbiota are related to original and specific processes at the interface between plants, microorganisms and the atmosphere. Recent -omics studies have opened fascinating opportunities for characterizing the spatio-temporal structure of phyllosphere microbial communities in relation with structural, functional, and ecological properties of host plants, and with physico-chemical properties of the environment, such as climate dynamics and trace gas composition of the surrounding atmosphere. This review will analyze recent advances, especially those resulting from environmental genomics, and how this novel knowledge has revealed the extent of the ecosystemic impact of the phyllosphere at the interface between plants and atmosphere. Highlights • The phyllosphere is one of the most prevalent microbial habitats on earth. • Phyllosphere microbiota colonize extreme, stressful, and changing environments. • Plants, phyllosphere microbiota and the atmosphere present a dynamic continuum. • Phyllosphere microbiota interact with the dynamics of volatile organic compounds and atmospheric trace gasses.

No MeSH data available.


Related in: MedlinePlus