Ecological trade-offs drive phenotypic and genetic differentiation of Arabidopsis thaliana in Europe.

Plant diversity is shaped by trade-offs between traits related to competitive ability, propagule dispersal, and stress resistance. However, we still lack a clear understanding of how these trade-offs influence species distribution and population dynamics. In Arabidopsis thaliana, recent genetic analyses revealed a group of cosmopolitan genotypes that successfully recolonized Europe from its center after the last glaciation, excluding older (relict) lineages from the distribution except for their north and south margins. Here, we tested the hypothesis that cosmopolitans expanded due to higher colonization ability, while relicts persisted at the margins due to higher tolerance to competition and/or stress. We compared the phenotypic and genetic differentiation between 71 European genotypes originating from the center, and the south and north margins. We showed that a trade-off between plant fecundity and seed mass shapes the differentiation of A. thaliana in Europe, suggesting that the success of the cosmopolitan groups could be explained by their high dispersal ability. However, at both north and south margins, we found evidence of selection for alleles conferring low dispersal but highly competitive and stress-resistance abilities. This study sheds light on the role of ecological trade-offs as evolutionary drivers of the distribution and dynamics of plant populations.

Can plants build their niche through modulation of soil microbial activities linked with nitrogen cycling? A test with Arabidopsis thaliana.

In natural systems, different plant species have been shown to modulate specific nitrogen (N) cycling processes so as to meet their N demand, thereby potentially influencing their own niche. This phenomenon might go beyond plant interactions with symbiotic microorganisms and affect the much less explored plant interactions with free-living microorganisms involved in soil N cycling, such as nitrifiers and denitrifiers. Here, we investigated variability in the modulation of soil nitrifying and denitrifying enzyme activities (NEA and DEA, respectively), and their ratio (NEA : DEA), across 193 Arabidopsis thaliana accessions. We studied the genetic and environmental determinants of such plant-soil interactions, and effects on plant biomass production in the next generation. We found that NEA, DEA, and NEA : DEA varied c. 30-, 15- and 60-fold, respectively, among A. thaliana genotypes and were related to genes linked with stress response, flowering, and nitrate nutrition, as well as to soil parameters at the geographic origin of the analysed genotypes. Moreover, plant-mediated N cycling activities correlated with the aboveground biomass of next-generation plants in home vs away nonautoclaved soil, suggesting a transgenerational impact of soil biotic conditioning on plant performance. Altogether, these findings suggest that nutrient-based plant niche construction may be much more widespread than previously thought.

Evolutionary pathways to lower biomass allocation to the seed coat in crops: insights from allometric scaling.

Crops generally have seeds larger than their wild progenitors´ and with reduced dormancy. In wild plants, seed mass and allocation to the seed coat (a proxy for physical dormancy) scale allometrically so that larger seeds tend to allocate less to the coats. Larger seeds and lightweight coats might thus have evolved as correlated traits in crops. We tested whether 34 crops and 22 of their wild progenitors fit the allometry described in the literature, which would indicate co-selection of both traits during crop evolution. Deviations from the allometry would suggest that other evolutionary processes contribute to explain the emergence of larger, lightweight-coated seeds in crops. Crops fitted the scaling slope but deviated from its intercept in a consistent way: Seed coats of crops were lighter than expected by their seed size. The wild progenitors of crops displayed the same trend, indicating that deviations cannot be solely attributed to artificial selection during or after domestication. The evolution of seeds with small coats in crops likely resulted from a combination of various pressures, including the selection of wild progenitors with coats smaller than other wild plants, further decreases during early evolution under cultivation, and indirect selection due to the seed coat-seed size allometry.

Why incorporate plant architecture into trait-based ecology?

Trait-based ecology has improved our understanding of the functioning of organisms, communities, ecosystems, and beyond. However, its predictive ability remains limited as long as phenotypic integration and temporal dynamics are not considered. We highlight how the morphogenetic processes that shape the 3D development of a plant during its lifetime affect its performance. We show that the diversity of architectural traits allows us to go beyond organ-level traits in capturing the temporal and spatial dimensions of ecological niches and informing community assembly processes. Overall, we argue that consideration of multilevel topological, geometrical, and ontogenetic features provides a dynamic view of the whole-plant phenotype and a relevant framework for investigating phenotypic integration, plant adaptation and performance, and community structure and dynamics.

A feedback loop between management, intraspecific trait variation and harvesting practices.

Intraspecific variation in plants is a major ecological mechanism whose local determinants are still poorly understood. In particular, the relationship between this variation and human practices may be key to understanding human-nature relationships. We argue that it is necessary to consider how human practices both influence and depend on the phenotypic variability of species of interest. Arnica montana (arnica) is a good model to study the complex interactions between human actions and plant phenotype, as (i) its ecological niche is shaped by human management actions and (ii) its variability has consequences for harvesters. Using a functional trait approach, we examined feedback loops linking management actions, plant phenotype and harvesting practices. In 27 sites in southeastern France, we measured vegetative and reproductive functional traits of arnica of interest for harvesters, and recorded management actions (grazing; mowing) and ecological variables (including height of surrounding vegetation and tree cover). We examined their effects on plant traits with linear mixed models and used path analysis to test if the effects of human management on traits are mediated by the height of surrounding vegetation. Management actions affected functional traits of arnica. Biomass removal practices (grazing, mowing) were associated with smaller plants producing smaller leaves with reduced specific leaf area. We uncovered the core role of the height of surrounding vegetation in determining this phenotype. Tree cover was associated with reduced flowering. The observed intraspecific variation in response to management actions differentially impacts the two main harvesting practices. Flower-head harvesting depends on reproductive traits that are not impacted by mowing (which is done in winter) but adversely affected by tree cover. In contrast, traits associated with large biomass under tree cover or with high surrounding vegetation are favourable for whole-plant harvesters. Our trait-based approach unveiled clear links between management actions and plant phenotype, with impacts on both vegetative and reproductive traits. These changes induced by management also affect the practices of harvesters. We thus demonstrated a feedback loop between human actions and plant phenotype and provided a novel perspective on human-related causes and consequences of plant intraspecific variability.

Upland rice varietal mixtures in Madagascar: evaluating the effects of varietal interaction on crop performance.

Introduction: Rice plays a critical role in human livelihoods and food security. However, its cultivation requires inputs that are not accessible to all farming communities and can have negative effects on ecosystems. simultaneously, ecological research demonstrates that biodiversity management within fields contributes to ecosystem functioning. Methods: This study aims to evaluate the mixture effect of four functionally distinct rice varieties in terms of characteristics and agronomic performance and their spatial arrangement on the upland rice performance in the highlands of Madagascar. The study was conducted during the 2021-2022 rainfall season at two close sites in Madagascar. Both site differ from each other's in soil properties and soil fertility management. The experimental design at each site included three modalities: i) plot composition, i.e., pure stand or binary mixture; ii) the balance between the varieties within a mixture; iii) and for the balanced mixture (50% of each variety), the spatial arrangement, i.e., row or checkerboard patterns. Data were collected on yields (grain and biomass), and resistance to Striga asiatica infestation, Pyricularia oryzea and bacterial leaf blight (BLB) caused by Xanthomonas oryzae-pv from each plot. Results and discussion: Varietal mixtures produced significantly higher grain and biomass yields, and significantly lower incidence of Pyricularia oryzea compared to pure stands. No significant differences were observed for BLB and striga infestation. These effects were influenced by site fertility, the less fertilized site showed stronger mixture effects with greater gains in grain yield (60%) and biomass yield (42%). The most unbalanced repartition (75% and 25% of each variety) showed the greatest mixture effect for grain yield at both sites, with a strong impact of the varietal identity within the plot. The mixture was most effective when EARLY_MUTANT_IAC_165 constituted 75% of the density associated with other varieties at 25% density. The assessment of the net effect ratio of disease, an index evaluating the mixture effect in disease reduction, indicated improved disease resistance in mixtures, regardless of site conditions. Our study in limited environments suggests that varietal mixtures can enhance rice productivity, especially in low-input situations. Further research is needed to understand the ecological mechanisms behind the positive mixture effect.

Correction: The genetic identity of neighboring plants in intraspecific mixtures modulates disease susceptibility of both wheat and rice.

[This corrects the article DOI: 10.1371/journal.pbio.3002287.].

Climate change and land use threaten global hotspots of phylogenetic endemism for trees.

Across the globe, tree species are under high anthropogenic pressure. Risks of extinction are notably more severe for species with restricted ranges and distinct evolutionary histories. Here, we use a global dataset covering 41,835 species (65.1% of known tree species) to assess the spatial pattern of tree species' phylogenetic endemism, its macroecological drivers, and how future pressures may affect the conservation status of the identified hotspots. We found that low-to-mid latitudes host most endemism hotspots, with current climate being the strongest driver, and climatic stability across thousands to millions of years back in time as a major co-determinant. These hotspots are mostly located outside of protected areas and face relatively high land-use change and future climate change pressure. Our study highlights the risk from climate change for tree diversity and the necessity to strengthen conservation and restoration actions in global hotspots of phylogenetic endemism for trees to avoid major future losses of tree diversity.

Changes in crop trait plasticity with domestication history: Management practices matter.

Crop domestication has led to the development of distinct trait syndromes, a series of constrained plant trait trade-offs to maximize yield in high-input agricultural environments, and potentially constrained trait plasticity. Yet, with the ongoing transition to organic and diversified agroecosystems, which create more heterogeneous nutrient availability, this constrained plasticity, especially in root functional traits, may be undesirable for nutrient acquisition. Such agricultural systems require a nuanced understanding of the soil-crop continuum under organic amendments and with intercropping, and the role crop genetic resources play in governing nutrient management and design. In this study, we use a functional traits lens to determine if crops with a range of domestication histories express different functional trait plasticity and how this expression changes with soil amendments and intercropping. We utilize a common garden experiment including five wheat (Triticum aestivum) varietals with a range of domestication histories planted in a factorial combination with amendment type (organic and inorganic) and cropping design (monoculture or intercropped with soybean). We use bivariate, multivariate and trait space analyses to quantify trait variation and plasticity in five leaf and five root functional traits. Almost all leaf and root traits varied among varieties. Yet, amendment type was nearly inconsequential for explaining trait expression across varieties. However, intercropping was linked to significant differences in root acquisitive strategies, regardless of the varietals' distinct history. Our findings show substantial leaf and root trait plasticity, with roots expressing greater trait space occupation with domestication, but also the strong role of management in crop trait expression. We underscore the utility of a functional trait-based approach to understand plant-soil dynamics with organic amendments, as well as the role of crop genetic histories in the successful transition to low-input and diversified agroecosystems.

Plant trait relationships are maintained within a major crop species: lack of artificial selection signal and potential for improved agronomic performance.

The exploration of phenotypic spaces of large sets of plant species has considerably increased our understanding of diversification processes in the plant kingdom. Nevertheless, such advances have predominantly relied on interspecific comparisons that hold several limitations. Here, we grew in the field a unique set of 179 inbred lines of durum wheat, Triticum turgidum spp. durum, characterized by variable degrees of artificial selection. We measured aboveground and belowground traits as well as agronomic traits to explore the functional and agronomic trait spaces and to investigate trait-to-agronomic performance relationships. We showed that the wheat functional trait space shared commonalities with global cross-species spaces previously described, with two main axes of variation: a root foraging axis and a slow-fast trade-off axis. Moreover, we detected a clear signature of artificial selection on the variation of agronomic traits, unlike functional traits. Interestingly, we identified alternative phenotypic combinations that can optimize crop performance. Our work brings insightful knowledge about the structure of phenotypic spaces of domesticated plants and the maintenance of phenotypic trade-offs in response to artificial selection, with implications for trade-off-free and multi-criteria selection in plant breeding.

The ecological causes of functional distinctiveness in communities.

Recent work has shown that evaluating functional trait distinctiveness, the average trait distance of a species to other species in a community offers promising insights into biodiversity dynamics and ecosystem functioning. However, the ecological mechanisms underlying the emergence and persistence of functionally distinct species are poorly understood. Here, we address the issue by considering a heterogeneous fitness landscape whereby functional dimensions encompass peaks representing trait combinations yielding positive population growth rates in a community. We identify four ecological cases contributing to the emergence and persistence of functionally distinct species. First, environmental heterogeneity or alternative phenotypic designs can drive positive population growth of functionally distinct species. Second, sink populations with negative population growth can deviate from local fitness peaks and be functionally distinct. Third, species found at the margin of the fitness landscape can persist but be functionally distinct. Fourth, biotic interactions (positive or negative) can dynamically alter the fitness landscape. We offer examples of these four cases and guidelines to distinguish between them. In addition to these deterministic processes, we explore how stochastic dispersal limitation can yield functional distinctiveness. Our framework offers a novel perspective on the relationship between fitness landscape heterogeneity and the functional composition of ecological assemblages.

Nonlinear Effects Induced by Interactions among Functional Groups of Bacteria and Fungi Regulate the Priming Effect in Malagasy Soils.

The priming effect (PE) occurs when fresh organic matter (FOM) supplied to soil alters the rate of decomposition of older soil organic matter (SOM). The PE can be generated by different mechanisms driven by interactions between microorganisms with different live strategies and decomposition abilities. Among those, stoichiometric decomposition results from FOM decomposition, which induces the decomposition of SOM by the release of exoenzymes by FOM-decomposers. Nutrient mining results from the co-metabolism of energy-rich FOM with nutrient-rich SOM by SOM-decomposers. While existing statistical approaches enable measurement of the effect of community composition (linear effect) on the PE, the effect of interactions among co-occurring populations (non-linear effect) is more difficult to grasp. We compare a non-linear, clustering approach with a strictly linear approach to separately and comprehensively capture all linear and non-linear effects induced by soil microbial populations on the PE and to identify the species involved. We used an already published data set, acquired from two climatic transects of Madagascar Highlands, in which the high-throughput sequencing of soil samples was applied parallel to the analysis of the potential capacity of microbial communities to generate PE following a 13C-labeled wheat straw input. The linear and clustering approaches highlight two different aspects of the effects of microbial biodiversity on SOM decomposition. The comparison of the results enabled identification of bacterial and fungal families, and combinations of families, inducing either a linear, a non-linear, or no effect on PE after incubation. Bacterial families mainly favoured a PE proportional to their relative abundances in soil (linear effect). Inversely, fungal families induced strong non-linear effects resulting from interactions among them and with bacteria. Our findings suggest that bacteria support stoichiometric decomposition in the first days of incubation, while fungi support mainly the nutrient mining of soil's organic matter several weeks after the beginning of incubation. Used together, the clustering and linear approaches therefore enable the estimation of the relative importance of linear effects related to microbial relative abundances, and non-linear effects related to interactions among microbial populations on soil properties. Both approaches also enable the identification of key microbial families that mainly regulate soil properties.

Plant-herbivore interactions: Experimental demonstration of genetic variability in plant-plant signalling.

Plant-herbivore interactions mediated by plant-plant signalling have been documented in different species but its within-species variability has hardly been quantified. Here, we tested if herbivore foraging activity on plants was influenced by a prior contact with a damaged plant and if the effect of such plant-plant signalling was variable across 113 natural genotypes of Arabidopsis thaliana. We filmed the activity of the generalist herbivore Cornu aspersum during 1 h on two plants differing only in a prior contact with a damaged plant or not. We recorded each snails' first choice, and measured its first duration on a plant, the proportion of time spent on both plants and leaf consumption. Overall, plant-plant signalling modified the foraging activity of herbivores in A. thaliana. On average, snails spent more time and consumed more of plants that experienced a prior contact with a damaged plant. However, the effects of plant-plant signalling on snail behaviour was variable: depending on genotype identity, plant-plant signalling made undamaged plants more repellant or attractive to snails. Genome-wide associations revealed that genes related to stress coping ability and jasmonate pathway were associated to this variation. Together, our findings highlight the adaptive significance of plant-plant signalling for plant-herbivore interactions.

AraDiv: a dataset of functional traits and leaf hyperspectral reflectance of Arabidopsis thaliana.

Data from functional trait databases have been increasingly used to address questions related to plant diversity and trait-environment relationships. However, such databases provide intraspecific data that combine individual records obtained from distinct populations at different sites and, hence, environmental conditions. This prevents distinguishing sources of variation (e.g., genetic-based variation vs. phenotypic plasticity), a necessary condition to test for adaptive processes and other determinants of plant phenotypic diversity. Consequently, individual traits measured under common growing conditions and encompassing within-species variation across the occupied geographic range have the potential to leverage trait databases with valuable data for functional and evolutionary ecology. Here, we recorded 16 functional traits and leaf hyperspectral reflectance (NIRS) data for 721 widely distributed Arabidopsis thaliana natural accessions grown in a common garden experiment. These data records, together with meteorological variables obtained during the experiment, were assembled to create the AraDiv dataset. AraDiv is a comprehensive dataset of A. thaliana's intraspecific variability that can be explored to address questions at the interface of genetics and ecology.

Global beta-diversity of angiosperm trees is shaped by Quaternary climate change.

As Earth's climate has varied strongly through geological time, studying the impacts of past climate change on biodiversity helps to understand the risks from future climate change. However, it remains unclear how paleoclimate shapes spatial variation in biodiversity. Here, we assessed the influence of Quaternary climate change on spatial dissimilarity in taxonomic, phylogenetic, and functional composition among neighboring 200-kilometer cells (beta-diversity) for angiosperm trees worldwide. We found that larger glacial-interglacial temperature change was strongly associated with lower spatial turnover (species replacements) and higher nestedness (richness changes) components of beta-diversity across all three biodiversity facets. Moreover, phylogenetic and functional turnover was lower and nestedness higher than random expectations based on taxonomic beta-diversity in regions that experienced large temperature change, reflecting phylogenetically and functionally selective processes in species replacement, extinction, and colonization during glacial-interglacial oscillations. Our results suggest that future human-driven climate change could cause local homogenization and reduction in taxonomic, phylogenetic, and functional diversity of angiosperm trees worldwide.

Links to rare climates do not translate into distinct traits for island endemics.

Current models of island biogeography treat endemic and non-endemic species as if they were functionally equivalent, focussing primarily on species richness. Thus, the functional composition of island biotas in relation to island biogeographical variables remains largely unknown. Using plant trait data (plant height, leaf area and flower length) for 895 native species in the Canary Islands, we related functional trait distinctiveness and climate rarity for endemic and non-endemic species and island ages. Endemics showed a link to climatically rare conditions that is consistent with island geological change through time. However, functional trait distinctiveness did not differ between endemics and non-endemics and remained constant with island age. Thus, there is no obvious link between trait distinctiveness and occupancy of rare climates, at least for the traits measured here, suggesting that treating endemic and non-endemic species as functionally equivalent in island biogeography is not fundamentally wrong.

Growth-defence trade-off in rice: fast-growing and acquisitive genotypes have lower expression of genes involved in immunity.

Plant ecologists and molecular biologists have long considered the hypothesis of a trade-off between plant growth and defence separately. In particular, how genes thought to control the growth-defence trade-off at the molecular level relate to trait-based frameworks in functional ecology, such as the slow-fast plant economics spectrum, is unknown. We grew 49 phenotypically diverse rice genotypes in pots under optimal conditions and measured growth-related functional traits and the constitutive expression of 11 genes involved in plant defence. We also quantified the concentration of silicon (Si) in leaves to estimate silica-based defences. Rice genotypes were aligned along a slow-fast continuum, with slow-growing, late-flowering genotypes versus fast-growing, early-flowering genotypes. Leaf dry matter content and leaf Si concentrations were not aligned with this axis and negatively correlated with each other. Live-fast genotypes exhibited greater expression of OsNPR1, a regulator of the salicylic acid pathway that promotes plant defence while suppressing plant growth. These genotypes also exhibited greater expression of SPL7 and GH3.2, which are also involved in both stress resistance and growth. Our results do not support the hypothesis of a growth-defence trade-off when leaf Si and leaf dry matter content are considered, but they do when hormonal pathway genes are considered. We demonstrate the benefits of combining ecological and molecular approaches to elucidate the growth-defence trade-off, opening new avenues for plant breeding and crop science.

A major genetic locus in neighbours controls changes of gene expression and susceptibility in intraspecific rice mixtures.

Reports indicate that intraspecific neighbours alter the physiology of focal plants, and with a few exceptions, their molecular responses to neighbours are unknown. Recently, changes in susceptibility to pathogen resulting from such interactions were demonstrated, a phenomenon called neighbour-modulated susceptibility (NMS). However, the genetics of NMS and the associated molecular responses are largely unexplored. Here, we analysed in rice the modification of biomass and susceptibility to the blast fungus pathogen in the Kitaake focal genotype in the presence of 280 different neighbours. Using genome-wide association studies, we identified the loci in the neighbour that determine the response in Kitaake. Using a targeted transcriptomic approach, we characterized the molecular responses in focal plants co-cultivated with various neighbours inducing a reduction in susceptibility. Our study demonstrates that NMS is controlled by one major locus in the rice genome of its neighbour. Furthermore, we show that this locus can be associated with characteristic patterns of gene expression in focal plant. Finally, we propose an hypothesis where Pi could play a role in explaining this case of NMS. Our study sheds light on how plants affect the physiology in their neighbourhood and opens perspectives for understanding plant-plant interactions.

Domestication provides durum wheat with protection from locust herbivory.

Lower plant resistance to herbivores following domestication has been suggested as the main cause for higher feeding damage in crops than in wild progenitors. While herbivore compensatory feeding has also been proposed as a possible mechanism for raised damage in crops with low nutritional quality, predictions regarding the effects of plant domestication on nutritional quality for herbivores remain unclear. In particular, data on primary metabolites, even major macronutrients, measured in the organs consumed by herbivores, are scarce. In this study, we used a collection of 10 accessions of wild ancestors and 10 accessions of modern progenies of Triticum turgidum to examine whether feeding damage and selectivity by nymphs of Locusta migratoria primarily depended on five leaf traits related to structural resistance or nutrient profiles. Our results unexpectedly showed that locusts favored wild ancestors over domesticated accessions and that leaf toughness and nitrogen and soluble protein contents increased with the domestication process. Furthermore, the quantitative relationship between soluble protein and digestible carbohydrates was found to poorly meet the specific requirements of the herbivore, in all wheat accessions, both wild and modern. The increase in leaf structural resistance to herbivores in domesticated tetraploid wheat accessions suggested that resource allocation trade-offs between growth and herbivory resistance may have been disrupted by domestication in the vegetative organs of this species. Since domestication did not result in a loss of nutritional quality in the leaves of the tetraploid wheat, our results rather provides evidence for a role of the content of plants in nonnutritive nitrogenous secondary compounds, possibly deterrent or toxic, at least for grasshopper herbivores.

How to improve scaling from traits to ecosystem processes.

Scaling approaches in ecology assume that traits are the main attributes by which organisms influence ecosystem functioning. However, several recent empirical papers have found only weak links between traits and ecosystem functioning, questioning the usefulness of trait-based ecology (TBE). We argue that these studies often suffer from one or more widespread misconceptions. Specifically, these studies often (i) conflict with the conceptual foundations of TBE, (ii) lack theory- or hypothesis-driven selection and use of traits, (iii) tend to ignore intraspecific variation, and (iv) use experimental or study designs that are not well suited to make strong tests of TBE assumptions. Addressing these aspects could significantly improve our ability to scale from traits to ecosystem functioning.