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.].

Phenotypic limits of crop diversity: a data exploration of functional trait space.

Relationships between crop genetic and functional diversity are key to addressing contemporary agricultural challenges. Yet, there are few approaches for quantifying the relationship between genetic diversity and crop functional trait expression. Here, we introduce 'functional space accumulation curves' to analyze how trait space increases with the number of crop genotypes within a species. We explore the potential for functional space accumulating curves to quantify genotype-trait space relationships in four common annual crop species: barley (Hordeum vulgare), rice (Oryza sativa), soybean (Glycine max), and durum wheat (Triticum durum). We also employ these curves to describe genotype-trait space relationships in the wild annual Arabidopsis thaliana, which has not been subjected to artificial selection. All five species exhibited asymptotic functional space accumulation curves, suggesting a limit to intraspecific functional crop diversity, likely due to: dominant phenotypes represented by several genotypes; or functional redundancy that might exist among genotypes. Our findings indicate that there is a diminishing return of functional diversity with increasing number of genotypes. Our analysis demonstrates the efficacy of functional space accumulation curves in quantifying trait space occupancy of crops, with implications for managing crop diversity in agroecosystems, and genetic diversity in crop breeding programs.

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.

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.

From cultivar mixtures to allelic mixtures: opposite effects of allelic richness between genotypes and genotype richness in wheat.

Agroecosystem diversification through increased crop genetic diversity could provide multiple services such as improved disease control or increased productivity. However, we still poorly understand how genetic diversity affects agronomic performance. We grew 179 inbred lines of durum wheat in pure stands and in 202 binary mixtures in field conditions. We then tested the effect of allelic richness between genotypes and genotype richness on grain yield and Septoria tritici blotch disease. Allelic richness was tested at 19K single nucleotide polymorphisms distributed along the durum wheat genome. Both genotype richness and allelic richness could be equal to 1 or 2. Mixtures were overall more productive and less diseased than their pure stand components. Yet, we identified one locus at which allelic richness between genotypes was associated with increased disease severity and decreased grain yield. The effect of allelic richness at this locus was stronger than the effect of genotype richness on grain yield (-7.6% vs +5.7%). Our results suggest that positive effects of crop diversity can be reversed by unfavourable allelic associations. This highlights the need to integrate genomic data into crop diversification strategies. More generally, investigating plant-plant interactions at the genomic level is promising to better understand biodiversity-ecosystem functioning relationships.

Plant neighbour-modulated susceptibility to pathogens in intraspecific mixtures.

As part of a trend towards diversifying cultivated areas, varietal mixtures are subject to renewed interest as a means to manage diseases. Besides the epidemiological effects of varietal mixtures on pathogen propagation, little is known about the effect of intraspecific plant-plant interactions and their impact on responses to disease. In this study, genotypes of rice (Oryza sativa) or durum wheat (Triticum turgidum) were grown with different conspecific neighbours and manually inoculated under conditions preventing pathogen propagation. Disease susceptibility was measured together with the expression of basal immunity genes as part of the response to intra-specific neighbours. The results showed that in many cases for both rice and wheat susceptibility to pathogens and immunity was modified by the presence of intraspecific neighbours. This phenomenon, which we term 'neighbour-modulated susceptibility' (NMS), could be caused by the production of below-ground signals and does not require the neighbours to be infected. Our results suggest that the mechanisms responsible for reducing disease in varietal mixtures in the field need to be re-examined.

Farming plant cooperation in crops.

Selection of the fittest can promote individual competitiveness but often results in the erosion of group performance. Recently, several authors revisited this idea in crop production and proposed new practices based on selection for cooperative phenotypes, i.e. phenotypes that increase crop yield through decreased competitiveness. These recommendations, however, remain difficult to evaluate without a formal description of crop evolutionary dynamics under different selection strategies. Here, we develop a theoretical framework to investigate the evolution of cooperation-related traits in crops, using plant height as a case study. Our model is tailored to realistic agricultural practices and shows that combining high plant density, high relatedness and selection among groups favours the evolution of shorter plants that maximize grain yield. Our model allows us to revisit past and current breeding practices in light of kin selection theory, and yields practical recommendations to increase cooperation among crops and promote sustainable agriculture.

Allocation, morphology, physiology, architecture: the multiple facets of plant above- and below-ground responses to resource stress.

Plants respond to resource stress by changing multiple aspects of their biomass allocation, morphology, physiology and architecture. To date, we lack an integrated view of the relative importance of these plastic responses in alleviating resource stress and of the consistency/variability of these responses among species. We subjected nine species (legumes, forbs and graminoids) to nitrogen and/or light shortages and measured 11 above-ground and below-ground trait adjustments critical in the alleviation of these stresses (plus several underlying traits). Nine traits out of 11 showed adjustments that improved plants' potential capacity to acquire the limiting resource at a given time. Above ground, aspects of plasticity in allocation, morphology, physiology and architecture all appeared important in improving light capture, whereas below ground, plasticity in allocation and physiology were most critical to improving nitrogen acquisition. Six traits out of 11 showed substantial heterogeneity in species plasticity, with little structuration of these differences within trait covariation syndromes. Such comprehensive assessment of the complex nature of phenotypic responses of plants to multiple stress factors, and the comparison of plant responses across multiple species, makes a clear case for the high (but largely overlooked) diversity of potential plastic responses of plants, and for the need to explore the potential rules structuring them.

Climate as a driver of adaptive variations in ecological strategies in Arabidopsis thaliana.

Background and aims: The CSR classification categorizes plants as stress tolerators (S), ruderals (R) and competitors (C). Initially proposed as a general framework to describe ecological strategies across species, this scheme has recently been used to investigate the variation of strategies within species. For instance, ample variation along the S-R axis was found in Arabidopsis thaliana, with stress-tolerator accessions predominating in hot and dry regions, which was interpreted as a sign of functional adaptation to climate within the species. Methods: In this study the range of CSR strategies within A. thaliana was evaluated across 426 accessions originating from North Africa to Scandinavia. A position in the CSR strategy space was allocated for every accession based on three functional traits: leaf area, leaf dry matter content (LDMC) and specific leaf area (SLA). Results were related to climate at origin and compared with a previous study performed on the same species. Furthermore, the role of natural selection in phenotypic differentiation between lineages was investigated with QST-FST comparisons, using the large amount of genetic information available for this species. Key Results: Substantial variation in ecological strategies along the S-R axis was found in A. thaliana. By contrast with previous findings, stress-tolerator accessions predominated in cold climates, notably Scandinavia, where late flowering was associated with traits related to resource conservation, such as high LDMC and low SLA. Because of trait plasticity, variations in CSR classification in relation to growth conditions were also observed for the same genotypes. Conclusions: There is a latitudinal gradient of ecological strategies in A. thaliana as a result of within-species adaptation to climate. Our study also underlines the importance of growth conditions and of the methodology used for trait measurement, notably age versus stage measurement, to infer the strength and direction of trait-environment relationships. This highlights the potential and limitations of the CSR classification in explaining functional adaptation to the environment.

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.