Significance Despite their importance in supplying nutrients, root traits related to maize domestication are scarce. We used laser ablation tomography to characterize the root architecture and anatomy of 5,300-y-old maize specimens recovered from San Marcos (Tehuacán, Mexico), revealing exquisite preservation of their cellular organization. Outer cortical cells contained thick and lignified walls typical of extant maize adapted to hard soils. By contrast, the absence of seminal roots is only found in the maize ancestor, teosinte. Two genes important for seminal root development had mutations that could relate to their absence. Our results indicate that some traits related to drought adaptation were not fully present in the earliest maize from Tehuacán, providing clues to conditions prevailing during early maize cultivation.

Native American genetic ancestry has been remarkably implicated with increased risk of diverse health issues in several Mexican populations, especially in relation to the dramatic changes in environmental, dietary, and cultural settings they have recently undergone. In particular, the effects of these ecological transitions and Westernization of lifestyles have been investigated so far predominantly on Mestizo individuals. Nevertheless, indigenous groups, rather than admixed Mexicans, have plausibly retained the highest proportions of genetic components shaped by natural selection in response to the ancient milieu experienced by Mexican ancestors during their pre-Columbian evolutionary history. These formerly adaptive variants have the potential to represent the genetic determinants of some biological traits that are peculiar to Mexican people, as well as a reservoir of loci with possible biomedical relevance. To test such a hypothesis, we used genome-wide genotype data to infer the unique adaptive evolution of Native Mexican groups selected as reasonable descendants of the main pre-Columbian Mexican civilizations. A combination of haplotype-based and gene-network analyses enabled us to detect genomic signatures ascribable to polygenic adaptive traits plausibly evolved by the main genetic clusters of Mexican indigenous populations to cope with local environmental and/or cultural conditions. Some of these adaptations were found to play a role in modulating the susceptibility/resistance of these groups to certain pathological conditions, thus providing new evidence that diverse selective pressures have contributed to shape the current biological and disease-risk patterns of present-day Native and Mestizo Mexican populations.

BackgroundThe entomopathogenic nematode Steinernema carpocapsae has been used worldwide as a biocontrol agent for insect pests, making it an interesting model for understanding parasite-host interactions. Two models propose that these interactions are co-evolutionary processes in such a way that equilibrium is never reached. In one model, known as “arms race”, new alleles in relevant genes are fixed in both host and pathogens by directional positive selection, producing recurrent and alternating selective sweeps. In the other model, known as“trench warfare”, persistent dynamic fluctuations in allele frequencies are sustained by balancing selection. There are some examples of genes evolving according to both models, however, it is not clear to what extent these interactions might alter genome-level evolutionary patterns and intraspecific diversity. Here we investigate some of these aspects by studying genomic variation in S. carpocapsae and other pathogenic and free-living nematodes from phylogenetic clades IV and V.ResultsTo look for signatures of an arms-race dynamic, we conducted massive scans to detect directional positive selection in interspecific data. In free-living nematodes, we detected a significantly higher proportion of genes with sites under positive selection than in parasitic nematodes. However, in these genes, we found more enriched Gene Ontology terms in parasites. To detect possible effects of dynamic polymorphisms interactions we looked for signatures of balancing selection in intraspecific genomic data. The observed distribution of Tajima’s D values in S. carpocapsae was more skewed to positive values and significantly different from the observed distribution in the free-living Caenorhabditis briggsae. Also, the proportion of significant positive values of Tajima’s D was elevated in genes that were differentially expressed after induction with insect tissues as compared to both non-differentially expressed genes and the global scan.ConclusionsOur study provides a first portrait of the effects that lifestyle might have in shaping the patterns of selection at the genomic level. An arms-race between hosts and pathogens seems to be affecting specific genetic functions but not necessarily increasing the number of positively selected genes. Trench warfare dynamics seem to be acting more generally in the genome, likely focusing on genes responding to the interaction, rather than targeting specific genetic functions.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0935-x) contains supplementary material, which is available to authorized users.

Archaeological cobs from Paredones and Huaca Prieta (Peru) represent some of the oldest maize known to date, yet they present relevant phenotypic traits corresponding to domesticated maize. This contrasts with the earliest Mexican macro-specimens from Guila Naquitz and San Marcos, which are phenotypically intermediate for these traits, even though they date more recently in time. To gain insights into the origins of ancient Peruvian maize, we sequenced DNA from three Paredones specimens dating ~6700–5000 calibrated years before present (BP), conducting comparative analyses with two teosinte subspecies (Zea mays ssp. mexicana and parviglumis) and extant maize, that include highland and lowland landraces from Mesoamerica and South America. We show that Paredones maize originated from the same domestication event as Mexican maize and was domesticated by ~6700 BP, implying rapid dispersal followed by improvement. Paredones maize shows no relevant gene flow from mexicana, smaller than that observed in teosinte parviglumis. Thus, Paredones samples represent the only maize without confounding mexicana variation found to date. It also harbors significantly fewer alleles previously found to be adaptive to highlands, but not of alleles adaptive to lowlands, supporting a lowland migration route. Our overall results imply that Paredones maize originated in Mesoamerica, arrived in Peru without mexicana introgression through a rapid lowland migration route, and underwent improvements in both Mesoamerica and South America.

Archaeological cobs from Paredones and Huaca Prieta (Peru) are phenotypically indistinguishable from modern maize. This contrasts with the earliest Mexican macro-specimens from Guila Naquitz and San Marcos, which are phenotypically intermediate even though they date more recently in time. These observations suggest at least two alternative scenarios, one in which maize was domesticated earlier than previously thought in the lowland Mesoamerica, followed by rapid lowland dispersal to Peru, and another in which maize was independently domesticated in South America and subsequently lost, as current evidence supports a single origin for all modern maize. To gain insights into the origins of ancient Peruvian maize, we sequenced DNA from three Paredones specimens dating 6775 to 5000 calibrated years before present (BP) and conducted comparative analyses with two teosinte subspecies (Zea mays ssp. mexicana and parviglumis) and extant maize, including highland and lowland landraces from Mesoamerica and South America. We show that Paredones maize originated from the same domestication event as Mexican maize and was domesticated by 6775 BP, implying rapid dispersal followed by improvement. Paredones maize show minimal levels of gene flow from mexicana, smaller than those observed in teosinte parviglumis. It also harbors significantly fewer alleles previously found to be adaptive to highlands, but not of alleles adaptive to lowlands, supporting a lowland migration route. Our overall results imply that Paredones maize originated in Mesoamerica, arrived in Peru without mexicana introgression through a rapid lowland migration route, and underwent improvements in both Mesoamerica and South America.

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Native American genetic ancestry has been remarkably implicated with increased risk of diverse health issues in several Mexican populations, especially in relation to the dramatic changes in environmental, dietary and cultural settings they have recently undergone. In particular, the effects of these ecological transitions and Westernization of lifestyles have been investigated so far predominantly on Admixed individuals. Nevertheless, indigenous groups, rather than admixed Mexicans, have plausibly retained the highest proportions of genetic components shaped by natural selection in response to the ancient milieu experienced by Mexican ancestors during their pre-Columbian evolutionary history. These formerly adaptive alleles/haplotypes have the potential to represent the genetic determinants of some biological traits peculiar to the Mexican people and a reservoir of loci with potential biomedical relevance. To test such a hypothesis, we used high-resolution genomic data to infer the unique adaptive evolution of 15 Native Mexican groups selected as reasonable descendants of the main pre-Columbian Mexican civilizations. A combination of haplotype-based and gene-network analyses enabled us to detect genomic signatures ascribable to polygenic adaptive traits evolved by the main genetic clusters of indigenous Mexican populations to cope with local environmental and/or cultural conditions. Some of them were also found to play a role in modulating the susceptibility/resistance of these groups to certain pathological conditions, thus providing new evidence for diverse selective pressures having contributed to shape current biological and disease-risk patterns in present-day Native and Mestizo Mexican populations.

IntroductionAlthough DNA methylation patterns are generally considered to be faithfully inherited in Arabidopsis thaliana (Arabidopsis), there is evidence of reprogramming during both male and female gametogenesis. The gynoecium is the floral reproductive organ from which the ovules develop and generate meiotically derived cells that give rise to the female gametophyte. It is not known whether the gynoecium can condition genomic methylation in the ovule or the developing female gametophyte.MethodsWe performed whole genome bisulfite sequencing to characterize the methylation patterns that prevail in the genomic DNA of pre-meiotic gynoecia of wild-type and three mutants defective in genes of the RNA-directed DNA methylation pathway (RdDM): ARGONAUTE4 (AGO4), ARGONAUTE9 (AGO9), and RNA-DEPENDENT RNA POLYMERASE6 (RDR6). ResultsBy globally analyzing transposable elements (TEs) and genes located across the Arabidopsis genome, we show that DNA methylation levels are similar to those of gametophytic cells rather than those of sporophytic organs such as seedlings and rosette leaves. We show that none of the mutations completely abolishes RdDM, suggesting strong redundancy within the methylation pathways. Among all, ago4 mutation has the strongest effect on RdDM, causing more CHH hypomethylation than ago9 and rdr6. We identify 22 genes whose DNA methylation is significantly reduced in ago4, ago9 and rdr6 mutants, revealing potential targets regulated by the RdDM pathway in premeiotic gyneocia. DiscussionOur results indicate that drastic changes in methylation levels in all three contexts occur in female reproductive organs at the sporophytic level, prior to the alternation of generations within the ovule primordium, offering a possibility to start identifying the function of specific genes acting in the establishment of the female gametophytic phase of the Arabidopsis life cycle.