Two teosintes made modern maize

Crop domestication and the subsequent expansion of crops have long been thought of as a linear process from a wild ancestor to a domesticate. However, evidence of gene flow from locally adapted wild relatives that provided adaptive alleles into crops has been identified in multiple species. Yet, little is known about the evolutionary consequences of gene flow during domestication and the interaction of gene flow and genetic load in crop populations. We study the pseudo-cereal grain amaranth that has been domesticated three times in different geographic regions of the Americas. We quantify the amount and distribution of gene flow along the genome of the three grain amaranth species and their two wild relatives. Our results show ample gene low between crop species and between crops and their wild relatives. Genetic load in introgressed regions from different donors suggest the potential of evolutionary rescue through decreased genetic load in genomic regions contributed by wild relatives with larger population size. To assess fitness of early hybrids we performed experimental crosses between the three crop species and found genetic incompatibilities between one Central American grain amaranth and the other two crop species. These incompatibilities might have created recent reproductive barriers, and maintain species integrity today. Together, our results show that gene flow played an important role in the domestication and expansion of grain amaranth, despite genetic species barriers. The domestication of plants was likely not linear and created a genomic mosaic by multiple contributors with varying fitness effects for today's crops.

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“…Recent work even suggests a prevalent role of Zea mays spp. mexicana in the domestication of maize (Yang et al . 2023).…”

Section: Discussionmentioning

confidence: 99%

“…Recent work even suggests a prevalent role of Zea mays spp. mexicana in the domestication of maize (Yang et al 2023). While we cannot associate gene flow from wild relatives with positive selection, we find decreased genetic load in regions that were introgressed from wild relatives (Figure 4).…”

Section: Discussionmentioning

confidence: 99%

Genetic incompatibilities and evolutionary rescue by wild relatives shaped grain amaranth domestication

Gonçalves-Dias

Singh

Graf

et al. 2023

Preprint

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“…Instead of aiming to find a single variant over a recombination block, which is unlikely due to low coverage, it detects other variants within the same recombination block, providing a better framework for genome-wide diversity patterns. Additionally, the inclusion of the dataset of Mexican landrace accessions (N. Yang et al, 2023) increases the representation of the diversity close to the center of origin, balancing the variance of the discovery dataset. The balanced HapMap presented here provides a context for investigating evolutionary questions in maize across the Americas.…”

Section: Discussionmentioning

confidence: 99%

“…Data was obtained from public sources (Chia et al, 2012;Gault et al, 2018), including data from the following SRA Bioprojects: PRJEB31061 (Hufford et al, 2021), PRJNA300309 (Wang et al, 2017), PRJNA381642 (J. Yang et al, 2017), PRJNA389800 (Bukowski et al, 2018), PRJNA479960 (Kistler et al, 2018), PRJNA641489 (Chen et al, 2022), PRJNA783885 (N. Yang et al, 2023). Based on the parameters identified in the Downsampled diversity dataset, the full maize variant call set was then built using UME Discovery by calling variants over the previously described 818 accessions, using the union of four different callers (GATK, Samtools, Freebayes and DeepVar; see Materials and methods) filtered with the max error summary statistic.…”

Section: Ume For Calling Genotypes For a Diverse Maize Hapmap Databasementioning

confidence: 99%

Unified Multi-caller Ensemble (UME) generates an unbiased maize haplotype map for variable coverage whole genome data

Vallebueno-Estrada,

Swarts

2023

Preprint

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We present a novel diversity-focused haplotype map (HapMap) that characterizes over 64.5 million maize (Zea maysssp. mays) single nucleotide polymorphisms (SNPs) genotyped across 818 individuals from diverse backgrounds. This HapMap aims to balance the variation obtained from domesticated landraces and inbred lines, outgroupZea spp.and more distantTripsacum spp.in order to minimize ascertainment bias for diversity studies. Included individuals derive from public data from various experimental setups and coverages, which is challenging for standard SNP callers to accommodate. We provide evidence of coverage biases associated with standard callers that influence resulting variation and introduce a novel approach called Unified Multi-Caller Ensemble (UME), which enhances variant calling accuracy in low-coverage and mixed-coverage genomic datasets. UME corrects for coverage bias resulting from inter-sample coverage heterogeneity by leveraging evidence from variant callers with orthogonal strategies, re-calibrating the error probabilities across callers to minimize the impact of error biases inherent to a given caller. It outperforms individual strategies and excels inde novovariant calling, taking advantage of instances of higher depth reads, even in low coverage individuals, while preserving biologically informative variant relationships across coverage levels. An important feature of UME is the independence from population allele frequencies in the discovery panel, thus avoiding ascertainment bias resulting from unbalanced input genetic diversity. Discovered variants are unbiased because no population filtering is used, and the full diversity of SNPs is retained in the final variant call set to maximize the utility of the dataset for production calling newly sequenced samples. We present a strategy for filtering the recalibrated error profiles that relies on maximizing demographic signals to retain genetic relationships within the population while reducing sequencing error. After the variant discovery phase, we employ the UME production stage, which enriches genotype calling across all coverage levels, benefiting low-coverage samples. Error introduced in this process is removed through subsequent filtering. Using this approach, we generated a coverage bias-controlled maize HapMap database, providing a comprehensive representation of maize accessions and emphasizing landrace diversity. This diverse panel of domesticated maize and outgroups from across the Americas enables accurate genotyping in low-coverage samples while offering crucial context for interpreting diversity, particularly for natural diversity and paleogenomic analyses.

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“…iHS is suitable for identifying selection in a single population and relies on the presence of ongoing sweeps and a signal of selection from unusually long-range linkage disequilibrium. We also used VCFtools v0.1.16 140 Phased SNPs for modern temperate maize lines, teosinte and Tripsacum dactyloides were obtained from Grzybowski et al 85 and SNPs for 265 CIMMYT landraces were obtained from Yang et al 86 and phased with Beagle v5.4 141 . A phased and imputed set of 42,387,706 genome-wide concatenated SNPs was used for the analysis of selection.…”

Section: Detection Of Selective Sweeps In Candidate Regions Associate...mentioning

confidence: 99%

Teosinte Pollen Driveguides maize diversification and domestication by RNAi

Berube,

Ernst,

Cahn

et al. 2023

Preprint

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Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Using single molecule and single-pollen genome sequencing, we describe Teosinte Pollen Drive, an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi). 22nt small RNAs from a non-coding RNA hairpin in mexicana depend on Dicer-Like 2 (Dcl2) and target Teosinte Drive Responder 1 (Tdr1), which encodes a lipase required for pollen viability. Dcl2, Tdr1, and the hairpin are in tight pseudolinkage on chromosome 5, but only when transmitted through the male. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas, and a tightly linked inversion in mexicana spans a major domestication sweep in modern maize. A survey of maize landraces and sympatric populations of teosinte mexicana reveals correlated patterns of admixture among unlinked genes required for RNAi on at least 3 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication and evolution, and offers an explanation for the widespread abundance of "self" small RNAs in the germlines of plants and animals.

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Two teosintes made modern maize

Cited by 16 publications

References 122 publications

Genetic incompatibilities and evolutionary rescue by wild relatives shaped grain amaranth domestication

Genetic incompatibilities and evolutionary rescue by wild relatives shaped grain amaranth domestication

Unified Multi-caller Ensemble (UME) generates an unbiased maize haplotype map for variable coverage whole genome data

Teosinte Pollen Driveguides maize diversification and domestication by RNAi

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