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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

General histological features and biochemical exchanges of the phylloplane. The schematic leaf cross section shows interactive exchanges (solid arrows) involving epiphytic microorganisms (gray ellipsoids with black edge) or endophytic microorganisms (gray ellipsoids with green edge) and leaf structures. It also shows the potential fluxes of plant (open green arrows) and microbial (open gray arrows) chemicals (green or black hexagons) that can occur through excretion, exudation, guttation, wounding, leaching, or infiltration. Blue arrows indicate the dynamics of the epiphyte communities with sweeping of bacteria from plant leaves and colonization from airborne microorganisms (gray ellipsoids with blue edge).
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Figure 1: General histological features and biochemical exchanges of the phylloplane. The schematic leaf cross section shows interactive exchanges (solid arrows) involving epiphytic microorganisms (gray ellipsoids with black edge) or endophytic microorganisms (gray ellipsoids with green edge) and leaf structures. It also shows the potential fluxes of plant (open green arrows) and microbial (open gray arrows) chemicals (green or black hexagons) that can occur through excretion, exudation, guttation, wounding, leaching, or infiltration. Blue arrows indicate the dynamics of the epiphyte communities with sweeping of bacteria from plant leaves and colonization from airborne microorganisms (gray ellipsoids with blue edge).

Mentions: Among the different above-ground portions of plants found in the phyllosphere such as the caulosphere (stems), the anthosphere (flowers) and the carposphere (fruits), the phyllophane (surface of leaves; Figure 1) presents many peculiar features for microbial life (Kowalchuk et al., 2010; Vorholt, 2012; Rastogi et al., 2013; Turner et al., 2013; Müller and Ruppel, 2014). Leaf surfaces are by themselves a complex architecture of microenvironments showing bidimensionally and tridimensionally heterogeneous structures. The characteristics of upper or lower phylloplane (Eglinton and Hamilton, 1967; Schreiber et al., 2004; Reisberg et al., 2013) affect the interactions between epiphytic microorganisms, which live on plant surfaces, in particular by modulating the access to nutrients from leaf tissues (Ruinen, 1961; Bulgarelli et al., 2013), by providing more or less protection from incoming sunlight (Atamna-Ismaeel et al., 2012a), or by presenting gateways for penetration within the plant endosphere (Hirano and Upper, 2000; Schreiber et al., 2004). Epiphytic microorganisms must adjust to multiple fluctuations involving the season cycle, the day/night cycle, and the developmental, morphological and anatomical dynamics of the plant, from the bud to the senescing leaf, or from the flower to the fruit. Plant photoassimilates like sucrose, fructose, and glucose are present on leaf surfaces (Trouvelot et al., 2014), but day/night fluctuations result in important modifications of the plant metabolite profile, and therefore of nutrient availability for the growth of epiphytic microorganisms. Moreover, plant metabolic status, especially carbohydrate status, is highly responsive to conditions of abiotic or biotic stresses (Couée et al., 2006; Trouvelot et al., 2014). Plant metabolites, such as soluble sugars, polyols, amino acids, amines, VOCs such as isoprenoids, halogenated compounds or alcohols, as well as plant water and salts, are not freely and directly available for epiphytic microorganisms. Plant leaf surfaces are generally protected by lipidic and waxy cuticles that greatly limit water and metabolite fluxes, and biochemical exchanges therefore depend on multiple pathways including excretion, exudation, guttation, wounding, leaching, or infiltration (Figure 1). All of these characteristics result in an oligotrophic habitat with limitations in carbon and nitrogen resources.


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

Bringel F, Couée I - Front Microbiol (2015)

General histological features and biochemical exchanges of the phylloplane. The schematic leaf cross section shows interactive exchanges (solid arrows) involving epiphytic microorganisms (gray ellipsoids with black edge) or endophytic microorganisms (gray ellipsoids with green edge) and leaf structures. It also shows the potential fluxes of plant (open green arrows) and microbial (open gray arrows) chemicals (green or black hexagons) that can occur through excretion, exudation, guttation, wounding, leaching, or infiltration. Blue arrows indicate the dynamics of the epiphyte communities with sweeping of bacteria from plant leaves and colonization from airborne microorganisms (gray ellipsoids with blue edge).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: General histological features and biochemical exchanges of the phylloplane. The schematic leaf cross section shows interactive exchanges (solid arrows) involving epiphytic microorganisms (gray ellipsoids with black edge) or endophytic microorganisms (gray ellipsoids with green edge) and leaf structures. It also shows the potential fluxes of plant (open green arrows) and microbial (open gray arrows) chemicals (green or black hexagons) that can occur through excretion, exudation, guttation, wounding, leaching, or infiltration. Blue arrows indicate the dynamics of the epiphyte communities with sweeping of bacteria from plant leaves and colonization from airborne microorganisms (gray ellipsoids with blue edge).
Mentions: Among the different above-ground portions of plants found in the phyllosphere such as the caulosphere (stems), the anthosphere (flowers) and the carposphere (fruits), the phyllophane (surface of leaves; Figure 1) presents many peculiar features for microbial life (Kowalchuk et al., 2010; Vorholt, 2012; Rastogi et al., 2013; Turner et al., 2013; Müller and Ruppel, 2014). Leaf surfaces are by themselves a complex architecture of microenvironments showing bidimensionally and tridimensionally heterogeneous structures. The characteristics of upper or lower phylloplane (Eglinton and Hamilton, 1967; Schreiber et al., 2004; Reisberg et al., 2013) affect the interactions between epiphytic microorganisms, which live on plant surfaces, in particular by modulating the access to nutrients from leaf tissues (Ruinen, 1961; Bulgarelli et al., 2013), by providing more or less protection from incoming sunlight (Atamna-Ismaeel et al., 2012a), or by presenting gateways for penetration within the plant endosphere (Hirano and Upper, 2000; Schreiber et al., 2004). Epiphytic microorganisms must adjust to multiple fluctuations involving the season cycle, the day/night cycle, and the developmental, morphological and anatomical dynamics of the plant, from the bud to the senescing leaf, or from the flower to the fruit. Plant photoassimilates like sucrose, fructose, and glucose are present on leaf surfaces (Trouvelot et al., 2014), but day/night fluctuations result in important modifications of the plant metabolite profile, and therefore of nutrient availability for the growth of epiphytic microorganisms. Moreover, plant metabolic status, especially carbohydrate status, is highly responsive to conditions of abiotic or biotic stresses (Couée et al., 2006; Trouvelot et al., 2014). Plant metabolites, such as soluble sugars, polyols, amino acids, amines, VOCs such as isoprenoids, halogenated compounds or alcohols, as well as plant water and salts, are not freely and directly available for epiphytic microorganisms. Plant leaf surfaces are generally protected by lipidic and waxy cuticles that greatly limit water and metabolite fluxes, and biochemical exchanges therefore depend on multiple pathways including excretion, exudation, guttation, wounding, leaching, or infiltration (Figure 1). All of these characteristics result in an oligotrophic habitat with limitations in carbon and nitrogen resources.

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