Improving the use of plant genetic resources to sustain breeding programs' efficiency.

Genetic progress of crop plants is required to face human population growth and guarantee production stability in increasingly unstable environmental conditions. Breeding is accompanied by a loss in genetic diversity, which hinders sustainable genetic gain. Methodologies based on molecular marker information have been developed to manage diversity and proved effective in increasing long-term genetic gain. However, with realistic plant breeding population sizes, diversity depletion in closed programs appears ineluctable, calling for the introduction of relevant diversity donors. Although maintained with significant efforts, genetic resource collections remain underutilized, due to a large performance gap with elite germplasm. Bridging populations created by crossing genetic resources to elite lines prior to introduction into elite programs can manage this gap efficiently. To improve this strategy, we explored with simulations different genomic prediction and genetic diversity management options for a global program involving a bridging and an elite component. We analyzed the dynamics of quantitative trait loci fixation and followed the fate of allele donors after their introduction into the breeding program. Allocating 25% of total experimental resources to create a bridging component appears highly beneficial. We showed that potential diversity donors should be selected based on their phenotype rather than genomic predictions calibrated with the ongoing breeding program. We recommend incorporating improved donors into the elite program using a global calibration of the genomic prediction model and optimal cross selection maintaining a constant diversity. These approaches use efficiently genetic resources to sustain genetic gain and maintain neutral diversity, improving the flexibility to address future breeding objectives.

Assessing the potential of genetic resource introduction into elite germplasm: a collaborative multiparental population for flint maize.

KEY MESSAGE: Implementing a collaborative pre-breeding multi-parental population efficiently identifies promising donor x elite pairs to enrich the flint maize elite germplasm. Genetic diversity is crucial for maintaining genetic gains and ensuring breeding programs' long-term success. In a closed breeding program, selection inevitably leads to a loss of genetic diversity. While managing diversity can delay this loss, introducing external sources of diversity is necessary to bring back favorable genetic variation. Genetic resources exhibit greater diversity than elite materials, but their lower performance levels hinder their use. This is the case for European flint maize, for which elite germplasm has incorporated only a limited portion of the diversity available in landraces. To enrich the diversity of this elite genetic pool, we established an original cooperative maize bridging population that involves crosses between private elite materials and diversity donors to create improved genotypes that will facilitate the incorporation of original favorable variations. Twenty donor × elite BC1S2 families were created and phenotyped for hybrid value for yield related traits. Crosses showed contrasted means and variances and therefore contrasted potential in terms of selection as measured by their usefulness criterion (UC). Average expected mean performance gain over the initial elite material was 5%. The most promising donor for each elite line was identified. Results also suggest that one more generation, i.e., 3 in total, of crossing to the elite is required to fully exploit the potential of a donor. Altogether, our results support the usefulness of incorporating genetic resources into elite flint maize. They call for further effort to create fixed diversity donors and identify those most suitable for each elite program.

Optimized breeding strategies to harness genetic resources with different performance levels.

BACKGROUND: The narrow genetic base of elite germplasm compromises long-term genetic gain and increases the vulnerability to biotic and abiotic stresses in unpredictable environmental conditions. Therefore, an efficient strategy is required to broaden the genetic base of commercial breeding programs while not compromising short-term variety release. Optimal cross selection aims at identifying the optimal set of crosses that balances the expected genetic value and diversity. We propose to consider genomic selection and optimal cross selection to recurrently improve genetic resources (i.e. pre-breeding), to bridge the improved genetic resources with elites (i.e. bridging), and to manage introductions into the elite breeding population. Optimal cross selection is particularly adapted to jointly identify bridging, introduction and elite crosses to ensure an overall consistency of the genetic base broadening strategy. RESULTS: We compared simulated breeding programs introducing donors with different performance levels, directly or indirectly after bridging. We also evaluated the effect of the training set composition on the success of introductions. We observed that with recurrent introductions of improved donors, it is possible to maintain the genetic diversity and increase mid- and long-term performances with only limited penalty at short-term. Considering a bridging step yielded significantly higher mid- and long-term genetic gain when introducing low performing donors. The results also suggested to consider marker effects estimated with a broad training population including donor by elite and elite by elite progeny to identify bridging, introduction and elite crosses. CONCLUSION: Results of this study provide guidelines on how to harness polygenic variation present in genetic resources to broaden elite germplasm.

Genomic prediction with a maize collaborative panel: identification of genetic resources to enrich elite breeding programs.

KEY MESSAGE: Collaborative diversity panels and genomic prediction seem relevant to identify and harness genetic resources for polygenic trait-specific enrichment of elite germplasms. In plant breeding, genetic diversity is important to maintain the pace of genetic gain and the ability to respond to new challenges in a context of climatic and social expectation changes. Many genetic resources are accessible to breeders but cannot all be considered for broadening the genetic diversity of elite germplasm. This study presents the use of genomic predictions trained on a collaborative diversity panel, which assembles genetic resources and elite lines, to identify resources to enrich an elite germplasm. A maize collaborative panel (386 lines) was considered to estimate genome-wide marker effects. Relevant predictive abilities (0.40-0.55) were observed on a large population of private elite materials, which supported the interest of such a collaborative panel for diversity management perspectives. Grain-yield estimated marker effects were used to select a donor that best complements an elite recipient at individual loci or haplotype segments, or that is expected to give the best-performing progeny with the elite. Among existing and new criteria that were compared, some gave more weight to the donor-elite complementarity than to the donor value, and appeared more adapted to long-term objective. We extended this approach to the selection of a set of donors complementing an elite population. We defined a crossing plan between identified donors and elite recipients. Our results illustrated how collaborative projects based on diversity panels including both public resources and elite germplasm can contribute to a better characterization of genetic resources in view of their use to enrich elite germplasm.

Assessment of breeding programs sustainability: application of phenotypic and genomic indicators to a North European grain maize program.

KEY MESSAGE: We review and propose easily implemented and affordable indicators to assess the genetic diversity and the potential of a breeding population and propose solutions for its long-term management. Successful plant breeding programs rely on balanced efforts between short-term goals to develop competitive cultivars and long-term goals to improve and maintain diversity in the genetic pool. Indicators of the sustainability of response to selection in breeding pools are of key importance in this context. We reviewed and proposed sets of indicators based on temporal phenotypic and genotypic data and applied them on an early maize grain program implying two breeding pools (Dent and Flint) selected in a reciprocal manner. Both breeding populations showed a significant positive genetic gain summing up to 1.43 qx/ha/year but contrasted evolutions of genetic variance. Advances in high-throughput genotyping permitted the identification of regions of low diversity, mainly localized in pericentromeric regions. Observed changes in genetic diversity were multiple, reflecting a complex breeding system. We estimated the impact of linkage disequilibrium (LD) and of allelic diversity on the additive genetic variance at a genome-wide and chromosome-wide scale. Consistently with theoretical expectation under directional selection, we found a negative contribution of LD to genetic variance, which was unevenly distributed between chromosomes. This suggests different chromosome selection histories and underlines the interest to recombine specific chromosome regions. All three sets of indicators valorize in house data and are easy to implement in the era of genomic selection in every breeding program.

Improving Short- and Long-Term Genetic Gain by Accounting for Within-Family Variance in Optimal Cross-Selection.

The implementation of genomic selection in recurrent breeding programs raises the concern that a higher inbreeding rate could compromise the long-term genetic gain. An optimized mating strategy that maximizes the performance in progeny and maintains diversity for long-term genetic gain is therefore essential. The optimal cross-selection approach aims at identifying the optimal set of crosses that maximizes the expected genetic value in the progeny under a constraint on genetic diversity in the progeny. Optimal cross-selection usually does not account for within-family selection, i.e., the fact that only a selected fraction of each family is used as parents of the next generation. In this study, we consider within-family variance accounting for linkage disequilibrium between quantitative trait loci to predict the expected mean performance and the expected genetic diversity in the selected progeny of a set of crosses. These predictions rely on the usefulness criterion parental contribution (UCPC) method. We compared UCPC-based optimal cross-selection and the optimal cross-selection approach in a long-term simulated recurrent genomic selection breeding program considering overlapping generations. UCPC-based optimal cross-selection proved to be more efficient to convert the genetic diversity into short- and long-term genetic gains than optimal cross-selection. We also showed that, using the UCPC-based optimal cross-selection, the long-term genetic gain can be increased with only a limited reduction of the short-term commercial genetic gain.

Usefulness Criterion and Post-selection Parental Contributions in Multi-parental Crosses: Application to Polygenic Trait Introgression.

Predicting the usefulness of crosses in terms of expected genetic gain and genetic diversity is of interest to secure performance in the progeny and to maintain long-term genetic gain in plant breeding. A wide range of crossing schemes are possible including large biparental crosses, backcrosses, four-way crosses, and synthetic populations. In silico progeny simulations together with genome-based prediction of quantitative traits can be used to guide mating decisions. However, the large number of multi-parental combinations can hinder the use of simulations in practice. Analytical solutions have been proposed recently to predict the distribution of a quantitative trait in the progeny of biparental crosses using information of recombination frequency and linkage disequilibrium between loci. Here, we extend this approach to obtain the progeny distribution of more complex crosses including two to four parents. Considering agronomic traits and parental genome contribution as jointly multivariate normally distributed traits, the usefulness criterion parental contribution (UCPC) enables to (i) evaluate the expected genetic gain for agronomic traits, and at the same time (ii) evaluate parental genome contributions to the selected fraction of progeny. We validate and illustrate UCPC in the context of multiple allele introgression from a donor into one or several elite recipients in maize (Zea mays L.). Recommendations regarding the interest of two-way, three-way, and backcrosses were derived depending on the donor performance. We believe that the computationally efficient UCPC approach can be useful for mate selection and allocation in many plant and animal breeding contexts.