Ecological principles to guide the development of crop variety mixtures

Crop variety mixtures can provide many benefits, including pathogen suppression and increased yield and yield stability. However, these benefits do not necessarily occur in all mixtures, and the benefits of diversity may be compromised by disadvantages due to increased crop heterogeneity. In-field development of mixtures by assembling many combinations of crop genotypes without prior expectation about which genotypes need to be combined to produce well-performing mixtures results in prohibitively large designs. Therefore, effective tools are required to narrow down the number of promising variety mixtures, and to then identify in experiments which of these deliver the highest benefits. Here, we first review current knowledge about the mechanisms underlying effects in ecological diversity experiments and in current agricultural applications. We then discuss some of the principal difficulties arising in the application of this knowledge to develop good variety mixtures. We also discuss non-conventional approaches to solve some of these issues. In particular, we highlight the potential and limitations of trait-based methods to determine good variety mixing partners, and argue that nontraditional traits and trait-derived metrics may be needed for the trait-based approach to deliver its full potential. Specifically, we argue that good mixing partners can be identified using modern genetic and genomic approaches. Alternatively, good mixtures may be obtained by combining varieties that respond differently to environmental variation; such varieties could easily be identified in standard variety testing trials. Preliminary analyses show that niche differences underlying the different environmental responses can indicate functional complementarity and promote mixture yield and yield stability

A plant biodiversity effect resolved to a single chromosomal region

Despite extensive evidence that biodiversity promotes plant community productivity, progress towards understanding the mechanistic basis of this effect remains slow, impeding the development of predictive ecological theory and agricultural applications. Here, we analysed non-additive interactions between genetically divergent Arabidopsis accessions in experimental plant communities. By combining methods from ecology and quantitative genetics, we identify a major effect locus at which allelic differences between individuals increase the above-ground productivity of communities. In experiments with near-isogenic lines, we show that this diversity effect acts independently of other genomic regions and can be resolved to a single region representing less than 0.3% of the genome. Using plant–soil feedback experiments, we also demonstrate that allelic diversity causes genotype-specific soil legacy responses in a consecutive growing period, even after the original community has disappeared. Our work thus suggests that positive diversity effects can be linked to single Mendelian factors, and that a range of complex community properties can have a simple cause. This may pave the way to novel breeding strategies, focusing on phenotypic properties that manifest themselves beyond isolated individuals; that is, at a higher level of biological organization

Increasing plant group productivity through latent genetic variation for cooperation

Historic yield advances in the major crops have, to a large extent, been achieved by selection for improved productivity of groups of plant individuals such as high-density stands. Research suggests that such improved group productivity depends on “cooperative” traits (e.g., erect leaves, short stems) that—while beneficial to the group—decrease individual fitness under competition. This poses a problem for some traditional breeding approaches, especially when selection occurs at the level of individuals, because “selfish” traits will be selected for and reduce yield in high-density monocultures. One approach, therefore, has been to select individuals based on ideotypes with traits expected to promote group productivity. However, this approach is limited to architectural and physiological traits whose effects on growth and competition are relatively easy to anticipate. Here, we developed a general and simple method for the discovery of alleles promoting cooperation in plant stands. Our method is based on the game-theoretical premise that alleles increasing cooperation benefit the monoculture group but are disadvantageous to the individual when facing noncooperative neighbors. Testing the approach using the model plant Arabidopsis thaliana, we found a major effect locus where the rarer allele was associated with increased cooperation and productivity in high-density stands. The allele likely affects a pleiotropic gene, since we find that it is also associated with reduced root competition but higher resistance against disease. Thus, even though cooperation is considered evolutionarily unstable except under special circumstances, conflicting selective forces acting on a pleiotropic gene might maintain latent genetic variation for cooperation in nature. Such variation, once identified in a crop, could rapidly be leveraged in modern breeding programs and provide efficient routes to increase yields

Single-gene resolution of diversity-driven overyielding in plant genotype mixtures

In plant communities, diversity often increases productivity and functioning, but the specific underlying drivers are difficult to identify. Most ecological theories attribute positive diversity effects to complementary niches occupied by different species or genotypes. However, the specific nature of niche complementarity often remains unclear, including how it is expressed in terms of trait differences between plants. Here, we use a gene-centred approach to study positive diversity effects in mixtures of natural Arabidopsis thaliana genotypes. Using two orthogonal genetic mapping approaches, we find that between-plant allelic differences at the AtSUC8 locus are strongly associated with mixture overyielding. AtSUC8 encodes a proton-sucrose symporter and is expressed in root tissues. Genetic variation in AtSUC8 affects the biochemical activities of protein variants and natural variation at this locus is associated with different sensitivities of root growth to changes in substrate pH. We thus speculate that - in the particular case studied here - evolutionary divergence along an edaphic gradient resulted in the niche complementarity between genotypes that now drives overyielding in mixtures. Identifying genes important for ecosystem functioning may ultimately allow linking ecological processes to evolutionary drivers, help identify traits underlying positive diversity effects, and facilitate the development of high-performance crop variety mixtures

A plant biodiversity effect resolved to a single genetic locus - datasets

Despite extensive evidence that biodiversity promotes plant community productivity, progress towards understanding the mechanistic basis of this effect remains slow, impeding the development of predictive ecological theory and agricultural applications. Here, we analysed non-additive interactions between genetically divergent Arabidopsis accessions in experimental plant communities. By combining methods from ecology and genetics, we identified a major effect locus that promotes complementarity amongst genotypes and above-ground productivity in mixed communities. In experiments with near-isogenic lines, we show that this diversity effect can act independently of other genomic regions and be resolved to a single locus representing less than 0.3% of the genome. Using plant-soil-feedback experiments, we demonstrate that allelic diversity also causes genotype-specific soil legacy responses in a subsequent growing period. Our work thus shows that positive diversity effects can be linked to single Mendelian factors, and that a range of complex community properties, some of which manifest themselves even after the original community has disappeared, can have a simple, single cause. This may pave the way to novel breeding strategies, focussing on phenotypic properties that manifest themselves beyond isolated individuals, i.e. at a higher level of biological organisation.</p

A plant biodiversity effect resolved to a single genetic locus

SummaryDespite extensive evidence that biodiversity promotes plant community productivity, progress towards understanding the mechanistic basis of this effect remains slow, impeding the development of predictive ecological theory and agricultural applications. Here, we analysed non-additive interactions between genetically divergent Arabidopsis accessions in experimental plant communities. By combining methods from ecology and genetics, we identified a major effect locus at which allelic differences between individuals increases above-ground productivity of communities. In experiments with near-isogenic lines, we show that this diversity effect acts independently of other genomic regions and can be resolved to a single region representing less than 0.3% of the genome. Using plant-soil-feedback experiments, we also demonstrate that allelic diversity causes genotype-specific soil legacy responses in a consecutive growing period, even after the original community has disappeared. Our work thus suggests that positive diversity effects can be linked to single Mendelian factors, and that a range of complex community properties can have a simple cause. This may pave the way to a better understanding of diversity effects, and to novel breeding strategies, focussing on phenotypic properties that manifest themselves beyond isolated individuals, i.e. at a higher level of biological organisation.</jats:p

Ecological and evolutionary approaches to improving crop variety mixtures

Variety mixtures can provide a range of benefits for both the crop and the environment. Their utility for the suppression of pathogens, especially in small grain crops, is well established and has seen some remarkable successes. However, despite decades of academic interest in the topic, commercial efforts to develop, release and promote variety mixtures remain peripheral to normal breeding activities. Here we argue that this is because simple but general design principles that allow for the optimization of multiple mixture benefits are currently lacking. We therefore review the practical and conceptual challenges inherent in the development of variety mixtures, and discuss common approaches to overcome these. We further consider three domains in which they might be particularly beneficial: pathogen resistance, yield stability and yield enhancement. We demonstrate that combining evolutionary and ecological concepts with data typically available from breeding and variety testing programmes could make mixture development easier and more economic. Identifying synergies between the breeding for monocultures and mixtures may even be key to the widespread adoption of mixtures-to the profit of breeders, farmers and society as a whole

Increasing plant group productivity through latent genetic variation for cooperation

Technologies for crop breeding have become increasingly sophisticated, yet it remains unclear whether these advances are sufficient to meet future demands. A major challenge with current crop selection regimes is that they are often based on individual performance. This tends to select for plants with “selfish” traits, which leads to a yield loss when they compete in high-density stands. In traditional breeding, this well-known “tragedy of the commons” has been addressed by anticipating ideotypes with presumably preferential characteristics. However, this approach is limited to obvious architectural and physiological traits, and it depends on a mechanistic understanding of how these modulate growth and competition. Here, we developed a general and simple method for the discovery of alleles promoting cooperation of plants in stands; it is based on the game-theoretical premise that alleles increasing cooperation incur a cost to the individual but benefit the monoculture group. Testing the approach using the model plant Arabidopsis thaliana, we found a single major effect locus where the rarer allele was associated with increased levels of cooperation and superior monoculture productivity. We show that the allele likely affects a pleiotropic regulator of growth and defense, since it is also associated with reduced root competition but higher race-specific resistance against a specialized parasite. Even though cooperation is considered evolutionarily unstable, conflicting selective forces acting on a pleiotropic gene might thus maintain latent genetic variation for it in nature. Such variation, once identified in a crop, could be rapidly leveraged in modern breeding programs and provide efficient routes to increase yields