Genomic diversity and population structure of teosinte (Zea spp.) and its conservation implications.

The wild species of the genus Zea commonly named teosintes, comprise nine different taxa, distributed from northern Mexico to Costa Rica. Although this genus of plants has been extensively studied from a morphological, ecogeographical and genetic point of view, most contributions have been limited to the study of a few populations and taxa. To understand the great variability that exists between and within teosinte species, it is necessary to include the vast majority of known populations. In this context, the objective of this work was to evaluate the diversity and genomic structure of 276 teosinte populations. Molecular analyzes were performed with 3,604 plants and with data from 33,929 SNPs. The levels of genetic diversity by taxonomic group show a marked difference between species, races and sections, where the highest values of genomic diversity was found in ssp. parviglumis and ssp. mexicana. The lower values were obtained for the Luxuriantes section as well as ssp. huehuetenagensis of the section Zea. The results of structure show that there is a great genetic differentiation in all the taxonomic groups considered. For ssp. parviglumis and mexicana, which are the taxa with the largest number of populations, a marked genomic differentiation was found that is consistent with their geographic distribution patterns. These results showed a loss of diversity in several teosinte populations, making a strong case for further collection, and ex situ and in situ conservation. Also, this study highlights the importance of integrating genomic diversity and structure for the applications of conservation and management.

Incorporating evolutionary and threat processes into crop wild relatives conservation.

Crop wild relatives (CWR) intra- and interspecific diversity is essential for crop breeding and food security. However, intraspecific genetic diversity, which is central given the idiosyncratic threats to species in landscapes, is usually not considered in planning frameworks. Here, we introduce an approach to develop proxies of genetic differentiation to identify conservation areas, applying systematic conservation planning tools that produce hierarchical prioritizations of the landscape. It accounts for: (i) evolutionary processes, including historical and environmental drivers of genetic diversity, and (ii) threat processes, considering taxa-specific tolerance to human-modified habitats, and their extinction risk status. Our analyses can be used as inputs for developing national action plans for the conservation and use of CWR. Our results also inform public policy to mitigate threat processes to CWR (like crops living modified organisms or agriculture subsidies), and could advise future research (e.g. for potential germplasm collecting). Although we focus on Mesoamerican CWR within Mexico, our methodology offers opportunities to effectively guide conservation and monitoring strategies to safeguard the evolutionary resilience of any taxa, including in regions of complex evolutionary histories and mosaic landscapes.

Domestication reshaped the genetic basis of inbreeding depression in a maize landrace compared to its wild relative, teosinte.

Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to large-effect mutations versus variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load in the maize population that we predicted from sequence data. Parental breeding values were highly consistent between outcross and selfed offspring, indicating that additive effects determine most of the genetic value even in the presence of strong inbreeding depression. We developed a novel linkage scan to identify quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, small-effect partially recessive effects in linkage disequilibrium underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against some large effect variants, but polygenic load is harder to purge and overall segregating mutational burden increased in maize compared to teosinte.

A conserved genetic architecture among populations of the maize progenitor, teosinte, was radically altered by domestication.

Very little is known about how domestication was constrained by the quantitative genetic architecture of crop progenitors and how quantitative genetic architecture was altered by domestication. Yang et al. [C. J. Yang et al., Proc. Natl. Acad. Sci. U.S.A. 116, 5643-5652 (2019)] drew multiple conclusions about how genetic architecture influenced and was altered by maize domestication based on one sympatric pair of teosinte and maize populations. To test the generality of their conclusions, we assayed the structure of genetic variances, genetic correlations among traits, strength of selection during domestication, and diversity in genetic architecture within teosinte and maize. Our results confirm that additive genetic variance is decreased, while dominance genetic variance is increased, during maize domestication. The genetic correlations are moderately conserved among traits between teosinte and maize, while the genetic variance-covariance matrices (G-matrices) of teosinte and maize are quite different, primarily due to changes in the submatrix for reproductive traits. The inferred long-term selection intensities during domestication were weak, and the neutral hypothesis was rejected for reproductive and environmental response traits, suggesting that they were targets of selection during domestication. The G-matrix of teosinte imposed considerable constraint on selection during the early domestication process, and constraint increased further along the domestication trajectory. Finally, we assayed variation among populations and observed that genetic architecture is generally conserved among populations within teosinte and maize but is radically different between teosinte and maize. While selection drove changes in essentially all traits between teosinte and maize, selection explains little of the difference in domestication traits among populations within teosinte or maize.

Contemporary evolution of maize landraces and their wild relatives influenced by gene flow with modern maize varieties.

Mexico is recognized as the center of origin and domestication of maize. Introduction of modern maize varieties (MVs) into Mexico raised concerns regarding the possible effects of gene flow from MVs into maize landraces (LRs) and their wild relatives (WRs), teosintes. However, after more than 60 y from the release of the first MVs, the impact of the sympatry with LRs and their WRs has not been explored with genetic data. In this work, we assessed changes in the genomes of 7 maize LRs and 2 WR subspecies from collections spanning over 70 y. We compared the genotypes obtained by genotyping by sequencing (GBS) for LRs and WRs before and after the adoption of MVs, and observed introgression from sympatric MVs into LRs and into the WR Zea mays ssp. mexicana sampled after the year 2000. We also found a decrease in the paired divergence index (FST ) between MV-LR and MV-WR over the same time frame. Moreover, we determined that LR genetic diversity increased after 2000, probably as a result of gene flow from MVs introduced in the 1990s. Our findings allowed us to identify ongoing changes in the domesticated and wild maize genetic pools, and concur with previous works that have evaluated short-term gene flow from MVs into LRs in other crops. Our approach represents a useful tool for tracking evolutionary change in wild and domesticated genetic resources, as well as for developing strategies for their conservation.

The genetic architecture of teosinte catalyzed and constrained maize domestication.

The process of evolution under domestication has been studied using phylogenetics, population genetics-genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance-covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.

Ecogeography of teosinte.

Adaptation of crops to climate change has motivated an increasing interest in the potential value of novel traits from wild species; maize wild relatives, the teosintes, harbor traits that may be useful to maize breeding. To study the ecogeographic distribution of teosinte we constructed a robust database of 2363 teosinte occurrences from published sources for the period 1842-2016. A geographical information system integrating 216 environmental variables was created for Mexico and Central America and was used to characterize the environment of each teosinte occurrence site. The natural geographic distribution of teosinte extends from the Western Sierra Madre of the State of Chihuahua, Mexico to the Pacific coast of Nicaragua and Costa Rica, including practically the entire western part of Mesoamerica. The Mexican annuals Zea mays ssp. parviglumis and Zea mays ssp. mexicana show a wide distribution in Mexico, while Zea diploperennis, Zea luxurians, Zea perennis, Zea mays ssp. huehuetenangensis, Zea vespertilio and Zea nicaraguensis had more restricted and distinct ranges, representing less than 20% of the total occurrences. Only 11.2% of teosinte populations are found in Protected Natural Areas in Mexico and Central America. Ecogeographical analysis showed that teosinte can cope with extreme levels of precipitation and temperatures during growing season. Modelling teosinte geographic distribution demonstrated congruence between actual and potential distributions; however, some areas with no occurrences appear to be within the range of adaptation of teosintes. Field surveys should be prioritized to such regions to accelerate the discovery of unknown populations. Potential areas for teosintes Zea mays ssp. mexicana races Chalco, Nobogame, and Durango, Zea mays ssp. huehuetenangensis, Zea luxurians, Zea diploperennis and Zea nicaraguensis are geographically separated; however, partial overlapping occurs between Zea mays ssp. parviglumis and Zea perennis, between Zea mays ssp. parviglumis and Zea diploperennis, and between Zea mays ssp. mexicana race Chalco and Zea mays ssp. mexicana race Central Plateau. Assessing priority of collecting for conservation showed that permanent monitoring programs and in-situ conservation projects with participation of local farmer communities are critically needed; Zea mays ssp. mexicana (races Durango and Nobogame), Zea luxurians, Zea diploperennis, Zea perennis and Zea vespertilio should be considered as the highest priority taxa.

Genomic estimation of complex traits reveals ancient maize adaptation to temperate North America.

By 4000 years ago, people had introduced maize to the southwestern United States; full agriculture was established quickly in the lowland deserts but delayed in the temperate highlands for 2000 years. We test if the earliest upland maize was adapted for early flowering, a characteristic of modern temperate maize. We sequenced fifteen 1900-year-old maize cobs from Turkey Pen Shelter in the temperate Southwest. Indirectly validated genomic models predicted that Turkey Pen maize was marginally adapted with respect to flowering, as well as short, tillering, and segregating for yellow kernel color. Temperate adaptation drove modern population differentiation and was selected in situ from ancient standing variation. Validated prediction of polygenic traits improves our understanding of ancient phenotypes and the dynamics of environmental adaptation.

Efficiency of RAPD, ISSR, AFLP and ISTR markers for the detection of polymorphisms and genetic relationships in camote de cerro (Dioscorea spp. )

Background At present, species known as camote de cerro (Dioscorea spp.) are found only in the wilderness in Mexico, but their populations are extremely depleted because they are indiscriminately collected, it is urgent to evaluate the conservation status of these plants in order to design conservation genetics programs. In this study, genetic diversity parameters along with cluster analysis based on Jaccard's coefficient were estimated with the objective to assess the efficiency of Random Amplified Polymorphic DNA (RAPD), Inter Simple Sequence Repeat (ISSR), Amplified Fragment Length Polymorphism (AFLP) and Inverse Sequence Tagged Repeat (ISTR) molecular DNA markers in the Dioscorea genus. Results The polymorphic information contents were quite similar for all markers (≈0.48). Genetic variation of Dioscorea spp., in terms of average heterozygosity was lower with ISTR (0.36), and higher when other markers were used (RAPD = 0.43; ISSR = 0.45 and AFLP = 0.47). Conclusion This indicates an important level of genetic differences despite the fact that the plant is asexually propagated. Based on the diversity statistics, any marker tested in present work can be recommended for use in large-scale genetic studies of populations. However, the low correlations among different molecular marker systems show the importance of the complementarity of the information that is generated by different markers for genetic studies involving estimation of polymorphism and relationships.

Major regulatory genes in maize contribute to standing variation in teosinte (Zea mays ssp. parviglumis).

In plants, many major regulatory genes that control plant growth and development have been identified and characterized. Despite a detailed knowledge of the function of these genes little is known about how they contribute to the natural variation for complex traits. To determine whether major regulatory genes of maize contribute to standing variation in Balsas teosinte we conducted association mapping in 584 Balsas teosinte individuals. We tested 48 markers from nine candidate regulatory genes against 13 traits for plant and inflorescence architecture. We identified significant associations using a mixed linear model that controls for multiple levels of relatedness. Ten associations involving five candidate genes were significant after correction for multiple testing, and two survive the conservative Bonferroni correction. zfl2, the maize homolog of FLORICAULA of Antirrhinum, was associated with plant height. zap1, the maize homolog of APETALA1 of Arabidopsis, was associated with inflorescence branching. Five SNPs in the maize domestication gene, teosinte branched1, were significantly associated with either plant or inflorescence architecture. Our data suggest that major regulatory genes in maize do play a role in the natural variation for complex traits in teosinte and that some of the minor variants we identified may have been targets of selection during domestication.