Wheat dwarfing reshapes plant and fungal development in arbuscular mycorrhizal symbiosis.

The introduction of Reduced height (Rht) dwarfing genes into elite wheat varieties has contributed to enhanced yield gain in high input agrosystems by preventing lodging. Yet, how modern selection for dwarfing has affected symbiosis remains poorly documented. In this study, we evaluated the response of both the plant and the arbuscular mycorrhizal fungus to plant genetic variation at a major Quantitative Trait Locus called QTL 4B2, known to harbor a Rht dwarfing gene, when forming the symbiosis. We used twelve inbred genotypes derived from a diversity base broadened durum wheat Evolutionary Pre-breeding Population and genotyped with a high-throughput Single Nucleotide Polymorphism (SNP) genotyping array. In a microcosm setup segregating roots and the extra-radical mycelium, each wheat genotype was grown with or without the presence of Rhizophagus irregularis. To characterize arbuscular mycorrhizal symbiosis, we assessed hyphal density, root colonization, spore production, and plant biomass. Additionally, we split the variation of these variables due either to genotypes or to the Rht dwarfing genes alone. The fungus exhibited greater development in the roots of Dwarf plants compared to non-Dwarf plants, showing increases of 27%, 37% and 51% in root colonization, arbuscules, and vesicles, respectively. In addition, the biomass of the extra-radical fungal structures increased by around 31% in Dwarf plants. The biomass of plant roots decreased by about 43% in mycorrhizal Dwarf plants. Interestingly, extraradical hyphal production was found to be partly genetically determined with no significant effect of Rht, as for plant biomasses. In contrast, variations in root colonization, arbuscules and extraradical spore production were explained by Rht dwarfing genes. Finally, when mycorrhizal, Dwarf plants had significantly lower total P content, pointing towards a less beneficial symbiosis for the plant and increased profit for the fungus. These results highlight the effect of Rht dwarfing genes on both root and fungal development. This calls for further research into the molecular mechanisms governing these effects, as well as changes in plant physiology, and their implications for fostering arbuscular mycorrhizal symbiosis in sustainable agrosystems.

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.

Diversity matters in wheat mixtures: A genomic survey of the impact of genetic diversity on the performance of 12 way durum wheat mixtures grown in two contrasted and controlled environments.

In ecology, an increase in genetic diversity within a community in natural ecosystems increases its productivity, while in evolutionary biology, kinship selection predicts that relatedness on social traits improves fitness. Varietal mixtures, where different genotypes are grown together, show contrasting results, especially for grain yield where both positive and negative effects of mixtures have been reported. To understand the effect of diversity on field performance, we grew 96 independent mixtures each composed with 12 durum wheat (Triticum turgidum ssp. durum Thell.) inbred lines, under two contrasting environmental conditions for water availability. Using dense genotyping, we imputed allelic frequencies and a genetic diversity index on more than 96000 loci for each mixture. We then analyzed the effect of genetic diversity on agronomic performance using a genome-wide approach. We explored the stress gradient hypothesis, which proposes that the greater the unfavourable conditions, the more beneficial the effect of diversity on mixture performance. We found that diversity on average had a negative effect on yield and its components while it was beneficial on grain weight. There was little support for the stress gradient theory. We discuss how to use genomic data to improve the assembly of varietal mixtures.

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.

Preferential helping to relatives: A potential mechanism responsible for lower yield of crop variety mixtures?

Variety mixtures, the cultivation of different genotypes within a field, have been proposed as a way to increase within-crop diversity, allowing the development of more sustainable agricultural systems with reduced environmental costs. Although mixtures have often been shown to over-yield the average of component varieties in pure stands, decreased yields in mixtures have also been documented. Kin selection may explain such pattern, whenever plants direct helping behaviors preferentially toward relatives and thus experience stronger competition when grown with less related neighbors, lowering seed production of mixtures. Using varieties of durum wheat originating from traditional Moroccan agrosystems, we designed a greenhouse experiment to address whether plants reduced competition for light by limiting stem elongation when growing with kin and whether such phenotypic response resulted in higher yield of kin groups. Seeds were sown in groups of siblings and nonkin, each group containing a focal plant surrounded by four neighbors. At the group level, mean plant height and yield did not depend upon relatedness among competing plants. At the individual level, plant height was not affected by genetic relatedness to neighbors, after accounting for direct genetic effects that might induce among-genotype differences in the ability to capture resources that do not depend on relatedness. Moreover, in contrast to our predictions, shorter plants had lower inclusive fitness. Phenotypic plasticity in height was very limited in response to neighbor genotypes. This suggests that human selection in crops may have attenuated shade-avoidance responses to competition for light. Future research on preferential helping to relatives in crops might thus target social traits that drive competition for other resources than light. Overall, our study illustrates the relevance of tackling agricultural issues from an evolutionary standpoint and calls for extending such approaches to a larger set of crop species.