Knotweeds are known to influence microbial processes. This study aimed to unravel the clonal control of microbial nitrogen cycle activities by established knotweed patches, as function of plant growth phases and ramet positions within the patch, all according to six different soils. At six sites, we measured N-microbial activities (free-living nitrogen fixation, nitrification, and denitrification, substrate-induced respiration), soil N mineral forms, moisture and pH across five plant growth phases and at two ramet positions within the patch (centre and front). The sites were categorized as having High, Medium or Low soil functioning based on (a)biotic parameters (nitrification, denitrification, soil moisture, and pH). The influence of the patch centre on N-microbial activities varied with soil functioning during the plant growth phases. Nitrification and N fixation increased in Low functioning soils but decreased or remained unchanged in High functioning soils. Denitrification remained constant in Low functioning soils but decreased in High functioning soils. In Medium functioning soil, denitrification and N fixation were reduced, whereas nitrification remained unchanged. Significant differences in N cycle control were found between the patch centre and front, depending on the growth phase and soil functioning. During the growth period (N demand), the patch centre influences N-microbial activities differently, depending on soil functioning, leading to improved N acquisition in soils with strong competition for mineral N (High and Medium functioning soils). Ramets at the patch centre and front control the N cycle differently, with the centre likely facilitating N acquisition and the front promoting colonization.
BACKGROUND AND AIMS:The successful plant Fallopia × bohemica presents interesting capacities for control of the soil nitrogen cycle at the adult stage, termed biological inhibition of denitrification (BDI). The BDI strategy allows the plant, via the production of secondary metabolites (procyanidins), to compete with the denitrifying microbial community and to divert nitrate from the soil for its benefit. In this study, we analysed whether seedlings of F. × bohemica can implement BDI at the seedling stage. We also determined whether soil nitrogen availability influences the implementation of BDI and seedling growth. METHODS:We sowed achenes of F. × bohemica in soils representing a nitrogen gradient (six treatments) and harvested seedlings after 20 or 40 days of growth. The denitrification and related microbial communities (i.e. functional gene abundances of nirK and nirS), soil parameters (nitrate content and humidity) and plant performance (biomass, growth and root morphology) were determined. KEY RESULTS:On soil without addition of nitrogen, BDI was observed after 20 days of growth, whereas a stimulation of denitrification was found after 40 days. The increase of soil N content had few effects on the activity and structure of the soil denitrifying community and on the plant biomasses or the relative growth rates. Correlations between plant and microbial parameters were observed after 20 days of growth, reflecting early and strong chemical interactions between plants and the denitrifying community, which decreased with plant growth after 40 days. CONCLUSIONS:This study shows that an early BDI enhances the efficiency of nitrogen acquisition in the first weeks of growth, allowing for a conservative root strategy after 40 days. This switch to a conservative strategy involved resource storage, an altered allocation to above- and below-ground parts and an investment in fine roots. It now seems clear that this storage strategy starts at a very young age with early establishment of BDI, giving this clonal plant exceptional capacities for storage and multiplication.
Denitrification is considered the major pathway leading to soil gaseous (N) losses, affecting N availability for plants and consequently plant productivity. Biological denitrification inhibition (BDI) in Fallopia spp., a plant species complex with a high level of growth and competitiveness for mineral N, acts through procyanidin production. However, the soil factors governing BDI development are still unknown. Through a mesocosm experiment using two treatments – soil planted with Fallopia japonica and unplanted–, nine biologically and physically contrasting soils were studied with the aim to ascertain how each can affect BDI development. Microbial enzyme activities (respiration - SIR, denitrification - DEA), denitrifying functional gene abundance (nirK, nirS), total bacterial community abundance (rRNA 16S) and soil physicochemical parameters (N mineral forms, soil texture, moisture, pH) were measured before and after plant growth, and the DEA:SIR ratio was used as a BDI proxy. The DEA:SIR ratio decreased for six soils. BDI development is related to a small number of soil factors, mainly initial soil moisture and ammonium concentration, and unexpectedly, with the initial abundance of nirK(in), nirS(in) and rRNA 16S(in). The intensity of this decrease is positively correlated to the level of DEA in unplanted soil: the higher the DEA in unplanted soil, the more intense the BDI under F. japonica. The procyanidin concentration of the F. japonica belowground system was positively correlated to BDI intensity. These results suggest that a procyanidin assay from the plant belowground system could be a new proxy for measuring BDI intensity. Interestingly, this research shows that BDI is not systematic, and that few (a)biotic soil parameters influence its development. More importantly, this research is the first to highlight that biotic factors are relevant in explaining BDI. This paper also presents new perspectives on plant-microorganism interactions in terms of plant awareness of the soil microbial community.
Invasive plants may alter ecological and ecosystem processes, including the N-cycle. The Fallopia species complex is a well-studied invasive species whose N-resource acquisition traits define it as an acquisitive species. However, the study of the impacts of invasive plants on the N-cycle never considers the N-acquisition strategy as a reference for choosing another suitable plant control. The purpose of this study is to assess the impacts of an invasive species (Fallopia japonica FJ) on the N-cycle and to compare with those caused by a native acquisitive species (Dactylis glomerata DG), all compared to unplanted soils. A four-months mesocosm experiment was conducted by growing FJ and DG on nine different soils and measuring their impacts on N-cycle microbial activities (free-living nitrogen fixation FLNF, denitrification DEA, nitrification NEA), on N-mineral forms and on functional N-cycle gene abundance (nifH, AOA, AOB, nirS, nirK) as well as the total bacterial community gene (rRNA 16S). The nine soils differ in microbial enzymatic activities, N-mineral form concentrations, physico-chemical factors, texture, and gene abundances. Plant effects on FLNF, NEA and DEA are only soil dependent and no effect of invasive status was found. In addition, the native plant DG generally affected microbial parameters over a wider range of soils than the invasive plant. Stronger impacts of the native DG on microbial gene abundances were found compared to the invasive FJ. A stronger effect of the invasive plant was found for the soil NO3− concentration, with a significant decrease under the FJ than under the DG. Under both FJ and DG, NH4+ concentrations were not significantly affected. In conclusion, the invasive status in the ecosystem of the two plants studied cannot be explained through their impacts on microbial enzymatic activities and gene abundances of the soil N-cycle and the soil N mineral pools.
The Japanese knotweed ( Fallopia japonica ) is considered as highly invasive in Europe and is largely widespread in France, without any established predator. This short study first characterized the herbivory of Fallopia by the black vine weevil ( Otiorhynchus sulcatus ), a commonly encountered coleopteran in France. Through an experimental design of leaf choices, between Fragaria spp. and Fallopia spp., our results show that the insects prefer Fallopia , even if it is presented for the first time. Even if this simple observation may appear as trivial, it highlights a novel plant-insect interaction and may start new insight in plant control or invasion management.
Biotic and abiotic factors are important drivers of the introduction, dispersal and establishment of an invasive species in fluvial corridors. In this study, we propose to better understand the spatial distribution of Asian knotweeds and to model their invasibility at the river basin scale in the Rhone Mediterranean and Corsica regions, France. We implemented a multiscale analysis of biophysical and anthropogenic factors related to the presence of knotweeds. Subbasins were sampled (50-600 km(2)), a large dataset on knotweed occurrence and biotic/abiotic factors was collected, and logistic regression was applied. A robust logit model (accuracy: 90%; false positive rate: 13%) estimated the probability of the occurrence of knotweeds at the river basin scale. We found clear evidence of: i) spatial scale-dependent water availability for knotweed implantation (e.g., summer vs. winter rainfalls > 250 mm); ii) an important role of hydrogeomorphic forces in dispersal; and iii) interspecific competition in riparian areas. The occurrence of knotweeds is also closely related to human-derived pressures. The management of knotweeds on roads and railways in the vicinity of rivers may be a major source of propagules. Hydraulic infrastructures (dikes and mill weirs) may also have served as locations of knotweed introduction since the end of the nineteenth century and may play a major role in the propagule transfer of knotweed; to date, these infrastructures have provided favourable conditions for knotweed establishment. Despite local water authorities' increasing awareness of invasive plants, local management practices for flood mitigation, low awareness of roads/railway managers, and negative representations of knotweeds have probably largely contributed to their dispersion over decades. The final model intends to integrate these biophysical and human factors by providing an operational tool to help river managers determine the sensitivity of their river basins to knotweed invasion. (C) 2020 Elsevier B.V. All rights reserved.
Intensive agriculture uses increasingly large amounts of nitrogen fertilizers to increase yields because nitrogen is one of the limiting factor of plant growth. Plants are in direct competition with denitrifying bacteria for nitrate, but biological denitrification inhibition (BDI) is a strategy developed by some plants in which procyanidins are produced that inhibit denitrification. This phenomenon increases the available nitrate in the soil. Previous results showed that the addition of procyanidins to lettuce fields allowed effective BDI and increased soil nitrate and plant growth. However, agriculture is performed in different soils, and the action of procyanidins could depend on the type of soil. In this study, we tested the effect of procyanidin amendment on lettuce growth in two types of soils: loamy sand and sandy clay loam. Our results show that in both soils, the addition of procyanidins causes inhibition of denitrification, an increase in available nitrate, counter-selection of denitrification communities and a gain in plant mass without modification of the soil structure. This study highlights a sustainable agricultural method effective in a variety of soils.
Metal trace elements accumulate in soils mainly because of anthropic activities, leading living organisms to develop strategies to handle metal toxicity. Plants often associate with root endophytic fungi, including nonmycorrhizal fungi, and some of these organisms are associated with metal tolerance. The lack of synthetic analyses of plant-endophyte-metal tripartite systems and the scant consideration for taxonomy led to this review aiming (1) to inventory non-mycorrhizal root fungal endophytes described with respect to their taxonomic diversity and (2) to determine the mutualistic roles of these plant-fungus associations under metal stress. More than 1500 species in 100 orders (mainly Hypocreales and Pleosporales) were reported from a wide variety of environments and hosts. Most reported endophytes had a positive effect on their host under metal stress, but with various effects on metal uptake or translocation and no clear taxonomic consistency. Future research considering the functional patterns and dynamics of these associations is thus encouraged. ? 2020 British Mycological Society. Published by Elsevier Ltd. All rights reserved.
Some plant secondary metabolites, such as procyanidins, have been demonstrated to cause biological denitrification inhibition (BDI) of denitrifiers in soils concomitantly with a gain in plant biomass. The present work evaluated whether procyanidins had an impact on the diversity of nontarget microbial communities that are probably involved in soil fertility and ecosystem services. Lettuce plants were grown in two contrasting soils, namely Manziat (a loamy sand soil) and Serail (a sandy clay loam soil) with and without procyanidin amendment. Microbial diversity was assessed using Illumina sequencing of prokaryotic 16S rRNA gene and fungal ITS regions. We used a functional inference to evaluate the putative microbial functions present in both soils and reconstructed the microbial interaction network. The results showed a segregation of soil microbiomes present in Serail and Manziat that were dependent on specific soil edaphic variables. For example, Deltaproteobacteria was related to total nitrogen content in Manziat, while Leotiomycetes and Firmicutes were linked to Ca2+ in Serail. Procyanidin amendment did not affect the diversity and putative activity of microbial communities. In contrast, microbial interactions differed according to procyanidin amendment, with the results showing an enrichment of Entotheonellaeota and Mucoromycota in Serail soil and of Dependentiae and Rozellomycetes in Manziat soil.
Intensive agriculture uses a lot of nitrogen fertilizers to increase crop productivity. These crops are in competition with soil-denitrifying microorganisms that assimilate nitrogen in the form of nitrate and transform it into N2O, a greenhouse gas, or N2. However, certain plant species exude secondary metabolites, called procyanidins, which inhibit denitrifiers and increase the nitrate pool in the soil available for plant nutrition. This phenomenon is called biological denitrification inhibition. Previously, we showed that the addition of exogenous procyanidins to a lettuce crop induces denitrifier inhibition and increases nitrate content in the soil, affecting lettuce morphological traits. Here, the effects of procyanidin amendments in the field on a more long-term and nitrogen-consuming crop species such as celery were tested. The effects of procyanidin amendment on celery growth with those of conventional ammonium nitrate amendments were, therefore, compared. Denitrification activity, nitrate concentration, the abundance of denitrifying bacteria in the soil, and traits related to celery growth were measured. It was shown that the addition of procyanidins inhibits denitrifiers and increases the soil nitrate level, inducing an improvement in celery morphological traits. In addition, procyanidin amendment induces the lowest nitrogen concentration in tissues and reduces N2O emissions.
The effects of invasive species at the ecosystem level remain an important component required to assess their impacts. Here, we conducted an experimental study with labeled nitrogen in two types of soil (low and high nitrate conditions), investigating the effects of (1) the presence of Fallopia x bohemica on the traits of three native species (Humulus lupulus, Sambucus ebulus, and Urtica dioica) and (2) interspecific competition (monoculture of the invasive species, monoculture of the native species, and a mixture of invasive/native species) on nitrification, denitrification, and related microbial communities (i.e., functional gene abundances). We found that the species with the higher nitrate assimilation rate (U. dioica) was affected differently by the invasive species, with no effect or even an increase in aboveground biomass and number of leaves. F. x bohemica also decreased denitrification, but only in the soil with high nitrate concentrations. The impacts of the invasive species on nitrification and soil microorganisms depended on the native species and the soil type, suggesting that competition for nitrogen between plants and between plants and microorganisms is highly dependent on species traits and environmental conditions. This research highlights that studies looking at the impacts of invasive species on ecosystems should consider the plant–soil–microorganism complex as a whole.
Plant responses to heavy metals and their storage constitute a crucial step to understand the environmental impacts of metallic trace elements (MTEs). In controlled experiments, we previously demonstrated the tolerance and resilience of Japanese knotweed to soil artificial polymetallic contamination. Using the same experimental design, we tested here the effect of three individual MTEs on Fallopia × bohemica performance traits. Rhizome fragments from three different sites (considered as distinct morphotypes) were grown in a greenhouse for 1 month on a prairial soil artificially contaminated with either Cd, Cr (VI) or Zn at concentrations corresponding to relatively highly polluted soils. Our results confirmed the high tolerance of Bohemian knotweed to metal stress, though, plant response to MTE pollution was dependant on MTE identity. Bohemian knotweed was stimulated by Cr (VI) (increased root and aerial masses), did not display any measurable change in performance traits under Cd at the high dose of 10 mg kg-1, and uptook all MTEs in its rhizome, but only Zn was transferred to its aerial parts. We also highlighted changes in root secondary metabolism that were more accentuated with Zn, including the increase of anthraquinone, stilbene and biphenyl derivatives. These results compared to multi-contamination experiments previously published suggest complex interactions between metals and plant, depending principally on metal identity and also suggest a potential role of soil microbes in the interactions.
Japanese Knotweeds were introduced by man during the 19th century in Europe, where they hybridized and formed a species complex now considered as "invasive". On the basis of many herbarium specimens, the literature and archive documents, we describe the history of their discovery and introduction in France. The circumstances of their hybridization are given, as well as the reasons for the spread of the complex composed of both taxa and their polyploid hybrids. We show that after its discovery by Von Siebold, Reynoutria japonica was introduced as a single male-sterile clone in Lorraine during the early 1850s, whereas R. sachalinensis was discovered by both the French and Russians and subject to successive introductions. Our study reveals that at the end of the 19th century, these Asiatic Knotweeds became very popular among horticulturists and botanical gardens. Their cultivation in sympatry has led to the production of their hybrid R. x bohemica, as well as interspecific hybridizations and introgressions with parental species, leading to considerable genetic diversity, escape and naturalisation.
The management of some invasive plant species is difficult because species can exhibit high productivity despite control measures.Inefficient control methods may even produce unwanted side effects.We conducted an experimental study on Fallopia spp., a major invasive plant in Europe.We tested the effects of two different stem-cutting frequencies on the aboveground and belowground traits of several genotypes in a greenhouse experiment against control plants (no cuts).Plants receiving one cut per month for a total of 4 cuts experienced 30% mortality of the individuals, surviving plants had greatly reduced values of the measured traits, especially for biomass and height.In contrast, plants in the treatment group, consisting of a single cut in five months, were eventually able to compensate for the loss of aboveground parts despite reduced length and biomass of the rhizome.Our results indicate that minimal mechanical intervention has limited effects on Fallopia spp.During the vegetative season, managers can increase control efficacy through regular cutting rather than a one-time intervention for these species.
La surveillance des renouées du Japon le long des cours d'eau représente un volet de gestion important pour les collectivités. Son objectif est d'identifier précocement les premières taches de renouées avant leur dissémination dans le milieu. Lorsque celles-ci sont déjà bien implantées, un suivi cartographique exhaustif de sa propagation le long du corridor est souvent nécessaire pour mieux la contenir. Des techniques de télédétection ont été récemment proposées dans la littérature scientifique , elles permettraient de réduire significativement les coûts liés à sa surveillance. Cet article présente un travail d'évaluation de cet outil de télédétection sur l'Azergues, affluent de la basse Saône déjà fortement colonisé par ces plantes. Une détection des renouées à l'aide d'orthophotos aériennes de l'IGN dans le visible et l'infra-rouge a été menée et évaluée à deux échelles spatiales : quelques centaines de mètres de cours d'eau puis à l'échelle du cours d'eau, soit plusieurs dizaines de kilomètres. Cette analyse nous a permis d'identifier les avantages et les limites actuelles liées à l'utilisation de cet outil par les scientifiques et les gestionnaires.
Introduites en France à la fin du dix-neuvième siècle, les renouées asiatiques sont classées au niveau mondial parmi les espèces exotiques envahissantes les plus menaçantes pour la biodiversité. Dans cet article, écologues, géographes, historiens et gestionnaires font le point des éléments de connaissances sur ces espèces, objets de nombreux travaux de recherches et d'essais de gestion en France, en Europe et dans le monde.
Chez les renouées asiatiques (complexe Reynoutria), l’eau des rivières est un des principaux vecteurs naturels de dispersion des propagules sexuées (akènes ailés) et végétatives (fragments de tiges et de rhizomes). Les auteurs de cet article ont étudié la flottaison et la viabilité de ces trois types de propagules en conditions expérimentales pour différentes taches de renouées. De leurs études, il en ressort une grande variabilité entre les taches pour un grand nombre de traits impliqués dans la dispersion par le cours d’eau et la colonisation des berges.
Basées sur l'utilisation des effets compétitifs des végétaux indigènes, les techniques de génie écologique visent à la fois le contrôle du développement des renouées asiatiques et la restauration d'une communauté végétale diversifiée dans les zones envahies. Ces méthodes alternatives intéressent de plus en plus de gestionnaires. Cet article s'intéresse ici à ces techniques, mobilisant des ligneux comme des herbacées, parfois associées à des prétraitements, mais obligatoirement à des mesures d'accompagnement. Après une synthèse des mécanismes écologiques sur lesquels elles reposent, une description de différentes méthodes est proposée, appliquées au cas des renouées asiatiques avec un focus particulier sur les milieux rivulaires. Enfin, la conclusion insiste sur la nécessité de partager et mutualiser les expériences afin de mieux comprendre les déterminants des succès et des échecs et avancer faire une meilleure mise en œuvre de ces méthodes prometteuses.
Une des pistes de recherche les plus récentes concernant la gestion des espèces végétales invasives porte sur les capacités des plantes à produire des composés chimiques inhibant la croissance ou le développement d’autres végétaux. Cet article décrit les enjeux, quelques recherches menées en France et les défis posés par cette démarche.