Functional outcomes of fungal community shifts driven by tree genotype and spatial‐temporal factors in Mediterranean pine forests

Pérez‐Izquierdo, Leticia; Zabal‐Aguirre, Mario; Flores‐Rentería, Dulce; González‐Martínez, Santiago C.; Buée, Marc; Rincón, Ana María

doi:10.1111/1462-2920.13690

Cited by 48 publications

(43 citation statements)

References 71 publications

(91 reference statements)

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“…Differences in litter qualities have been demonstrated at interspecific (Wang et al ., ) and intraspecific levels (Madritch & Hunter, ) and recognized as a consequence of the genetic expression (Allan et al ., ). Litter quality controls litter decay and soil functioning through its effect on the belowground microbial communities (Chavez‐Vergara et al ., ), and these last act, in turn, as important controlling factors of SOM formation and nutrient mobilization (Pérez‐Izquierdo et al ., ). In fact, we observed that enzymes related to hemicellulose degradation and organic N mobilization were particularly active in soil beneath the Atlantic trees, compared with the other genotypes.…”

Section: Discussionmentioning

confidence: 99%

“…season), are among the main environmental factors in the efficiency of C use and ecosystem functioning, directly or indirectly, or both, affecting soil microorganisms (Manzoni et al ., ). Different microbial groups decompose and assimilate C compounds differently depending on their quality (Wang et al ., ), and the functional effects observed in our study might reflect cascading effects on microbial communities (Pérez‐Izquierdo et al ., ), which deserves further analysis. Potential enzyme activities were measured in optimally controlled conditions; therefore, results could vary under field conditions where complex multi‐factor interactions usually occur (Baldrian, ).…”

Section: Discussionmentioning

confidence: 99%

“…This can be particularly pronounced in Mediterranean forest ecosystems, which are characterized by hot dry summers and scarce precipitation, and where plant primary productivity, and thus the dynamics of litter and soil decomposition, are strongly affected by the climate conditions and especially the availability of water (Gallardo & Merino, ). In addition, differences in the structure of fungal communities have been reported previously between spring and autumn at the sites of the current study (Pérez‐Izquierdo et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Tree genotype and seasonal effects on soil properties and biogeochemical functioning in Mediterranean pine forests

Pérez‐Izquierdo

Saint‐André²,

Santenoise³

et al. 2018

European J Soil Science

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Summary In forests, intraspecific genetic variation in trees can affect the entire ecosystem, which in turn depends on the different processes occurring through space and time in soil. We hypothesized that, in addition to the effect of the local site, tree genotype and season would have an effect on the properties and functions of the edaphic environment. We studied soils beneath different genotypes of Pinus pinaster Ait. (Atlantic, Mediterranean and African) in 45‐year‐old common gardens in spring and autumn. The pH, organic matter, nutrients and infrared spectroscopy, together with enzyme activities, were determined and used to evaluate the soil properties and biogeochemical functioning. In addition to strong site effects, tree genotype and seasonal effects were detected on soil properties and functions. Both were major controlling factors of microbially mediated functioning, especially processes related to the carbon (C) and nitrogen (N) cycles. In general, the soil environment beneath the Atlantic trees was different from that under the Mediterranean and African genotypes, with differences in raw infrared spectra and increased activities of enzymes involved in hemicellulose degradation and N mobilization. Regarding the season, the largest soil humidity (RH), electric conductivity (EC), and N and potassium (K) concentrations, coupled with the smallest phosphorus (P) concentration and C:N ratios, were detected in autumn. Degradation of C peaked in autumn, whereas P and N mobilization usually peaked in spring. Our results showed that, beyond local site effects, there were detectable effects of tree genotype and season in Mediterranean forest soils, which governed microbially mediated processes that might have relevant functional consequences at the ecosystem level. Highlights Tree genotype and season shape the features and functioning of Mediterranean forest soils. Tree genotype, season and site effects on soil are identified separately under field conditions. Intraspecific genetic variation of trees defines soil properties and functioning. Tree genotype and season are key regulators of the edaphic environment in Mediterranean forests.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 97%

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Tree genotype and seasonal effects on soil properties and biogeochemical functioning in Mediterranean pine forests

Pérez‐Izquierdo

Saint‐André²,

Santenoise³

et al. 2018

European J Soil Science

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“…This, in combination with the sessile nature of trees, may form a “much more intimate (localized) pathogen‐host interaction”, leading to low pathogen‐induced mortality of offspring beneath unrelated conspecifics compared to those beneath their parent trees (Augspurger & Kelly, ). The disease triangle further predicts that intraspecific genetic divergence among host provenances (or “genotypes” in Pérez‐Izquierdo et al, ) and the genetic variation within pathogen populations (e.g. formae speciales in Fusarium oxysporum ; Altinok, Can, & Altinok, ) could cause differential infestation, depending on the co‐occurring genotypes of the host and pathogen.…”

Section: Introductionmentioning

confidence: 99%

Incorporating the disease triangle framework for testing the effect of soil‐borne pathogens on tree species diversity

Liu

2019

Functional Ecology

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The enemy‐induced Janzen–Connell (JC) effect, a classic model invoking conspecific negative density dependence (CNDD) and distance dependence, is a primary biodiversity maintenance hypothesis. Yet, conflicting evidence for the JC effect leads to disagreement about its role in maintaining forest diversity. We focus this review on soil‐borne pathogens, which are the primary agent inducing the JC effect in many forest ecosystems. Although the test of the pathogen‐induced JC effect in ecology critically rests on the seedling mortality caused by soil pathogens, what has not been explicitly explored in the early literature but has increasingly received attention is the long‐recognized fact that the environment can alter virulence of pathogens and host susceptibility (thus pathogen–host interactions), as predicted by the classic disease triangle framework enlightened by pathology research in agricultural systems. Here, following the disease triangle framework we review evidence on how the pathogen‐induced JC effect may be contingent on context (e.g. environmental conditions, pathogen inoculum load and genetic divergence in host and pathogen populations). The reviewed evidence reveals and clarifies the conditions where pathogens may or may not cause disease to hosts, thus contributing to reconciling the inconsistent results about the pathogen‐induced JC effect in the literature. The context dependence of the disease triangle predicts that the pathogen‐induced JC effect would change under global change. Gaining insights from evidence that the pathogen‐induced JC effect is context‐dependent, we suggest that future tests on the JC hypothesis be conducted under the framework of disease triangle, and we stress the necessity by controlling the effect of context factors on plant–pathogen interactions when testing for the JC effect. We conclude the review by proposing three lines of future research for testing the importance of the JC effect in maintaining global forest tree species diversity, with a particular emphasis on testing the effect of global warming on the strength of pathogen–host interactions for better predicting changes of forest biodiversity under climate change. A plain language summary is available for this article.

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“…Pines are obligatory ectomycorrhizal (ECM) plants and this intimate relationship strongly influences the surrounding environment (Tarkka, Drigo, & Deveau, ). The effects of the plant genotype on below‐ground microbial communities can be ideally studied through the symbiosis between pines and ECM fungi (Patterson, Flores‐Rentería, Whipple, Whitham, & Gehring, ; Pérez‐Izquierdo et al, ; Piculell, Eckhardt, & Hoeksema, ). Patterson et al () have recently shown that ECM community composition is under strong plant genetic control in Pinus edulis .…”

Section: Introductionmentioning

confidence: 99%

Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome

et al. 2019

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Plant genetic variation, through its phenotypic display, can determine the composition of below ground microbial communities. Variation within a species is increasingly acknowledged to have substantial ecological consequences, particularly through trophic cascades. We hypothesized that the intraspecific genotypic variation of the tree host might impact the phylogenetic composition of its rhizospheric microbial communities, by favouring particular clades, that might be further reflected in ecosystem process rates. We tested whether the intraspecific genotypic variation of Pinus pinaster modulates nutrient cycling by determining the phylogenetic structure of its symbiotic ectomycorrhizal fungi and rhizospheric bacteria. We sequenced fungal and bacterial molecular markers and reconstructed phylogenies in the rhizosphere of P. pinaster trees belonging to three genotypic variants (Mediterranean, Atlantic, African) in three 45‐year‐old common garden experiments, and measured seven soil enzymatic activities. Local effects, based on differences in elevation and soil conditions across sites, were strong predictors of the ectomycorrhizal and bacterial communities thriving in tree’s rhizosphere. Across‐site variation also explained differences in phosphorus cycling. We detected, however, a significant effect of the plant genotype on the phylogenetic structure of the root‐associated microbiota that was consistent across sites. The most productive Mediterranean plant genotype sheltered the most distinct root microbiome, with the dominant Basidiomycetes and Proteobacteria having a strong influence on the phylogenetic microbial community structure and associating with an enhanced hydrolysis of celluloses, hemicelluloses and chitin. Beneath the less productive Atlantic genotype, the less abundant Ascomycetes and up to thirteen bacterial phyla shaped the phylogenetic microbial structure, and predicted the rates of peptidase. Ectomycorrhizal fungi explained the activity of cellulases and protease, and bacteria that of hemicellulases and chitinase, suggesting functional complementarity. Synthesis. This is the first report using three‐replicated long‐term common gardens in mature forests to disentangle plant genotype‐ and site‐specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance.

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Functional outcomes of fungal community shifts driven by tree genotype and spatial‐temporal factors in Mediterranean pine forests

Cited by 48 publications

References 71 publications

Tree genotype and seasonal effects on soil properties and biogeochemical functioning in Mediterranean pine forests

Tree genotype and seasonal effects on soil properties and biogeochemical functioning in Mediterranean pine forests

Incorporating the disease triangle framework for testing the effect of soil‐borne pathogens on tree species diversity

Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome

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