Fluctuation of ecological niches and geographic range shifts along chile pepper's domestication gradient.

Domestication is an ongoing well-described process. However, while many have studied the changes domestication causes in plant genetics, few have explored its impact on the portion of the geographic landscape in which the plants exist. Therefore, the goal of this study was to understand how the process of domestication changed the geographic space suitable for chile pepper (Capsicum annuum) in its center of origin (domestication). C. annuum is a major crop species globally whose center of domestication, Mexico, has been well-studied. It provides a unique opportunity to explore the degree to which ranges of different domestication classes diverged and how these ranges might be altered by climate change. To this end, we created ecological niche models for four domestication classes (wild, semiwild, landrace, modern cultivar) based on present climate and future climate scenarios for 2050, 2070, and 2090. Considering present environment, we found substantial overlap in the geographic niches of all the domestication classes. Yet, environmental and geographic aspects of the current ranges did vary among classes. Wild and commercial varieties could grow in desert conditions, while landraces could not. With projections into the future, habitat was lost asymmetrically, with wild, semiwild, and landraces at greater risk of territorial declines than modern cultivars. Further, we identified areas where future suitability overlap between landraces and wilds is expected to be lost. While range expansion is widely associated with domestication, we found little support of a constant niche expansion (either in environmental or geographical space) throughout the domestication gradient in chile peppers in Mexico. Instead, particular domestication transitions resulted in loss, followed by capturing or recapturing environmental or geographic space. The differences in environmental characterization among domestication gradient classes and their future potential range shifts increase the need for conservation efforts to preserve landraces and semiwild genotypes.

Crop adaptation to climate change: An evolutionary perspective.

The disciplines of evolutionary biology and plant and animal breeding have been intertwined throughout their development, with responses to artificial selection yielding insights into the action of natural selection and evolutionary biology providing statistical and conceptual guidance for modern breeding. Here we offer an evolutionary perspective on a grand challenge of the 21st century: feeding humanity in the face of climate change. We first highlight promising strategies currently under way to adapt crops to current and future climate change. These include methods to match crop varieties with current and predicted environments and to optimize breeding goals, management practices, and crop microbiomes to enhance yield and sustainable production. We also describe the promise of crop wild relatives and recent technological innovations such as speed breeding, genomic selection, and genome editing for improving environmental resilience of existing crop varieties or for developing new crops. Next, we discuss how methods and theory from evolutionary biology can enhance these existing strategies and suggest novel approaches. We focus initially on methods for reconstructing the evolutionary history of crops and their pests and symbionts, because such historical information provides an overall framework for crop-improvement efforts. We then describe how evolutionary approaches can be used to detect and mitigate the accumulation of deleterious mutations in crop genomes, identify alleles and mutations that underlie adaptation (and maladaptation) to agricultural environments, mitigate evolutionary trade-offs, and improve critical proteins. Continuing feedback between the evolution and crop biology communities will ensure optimal design of strategies for adapting crops to climate change.

Where the wild things are: genetic associations of environmental adaptation in the Oryza rufipogon species complex.

Crop wild relatives host unique adaptation strategies that enable them to thrive across a wide range of habitats. As pressures from a changing climate mount, a more complete understanding of the genetic variation that underlies this adaptation could enable broader utilization of wild materials for crop improvement. Here, we carry out environmental association analyses (EAA) in the Oryza rufipogon species complex (ORSC), the wild progenitor of cultivated Asian rice, to identify genomic regions associated with environmental adaptation characterized by variation in bioclimatic and soil variables. We further examine regions for colocalizations with phenotypic associations within the same collection. EAA results indicate that significant regions tend to associate with single environmental variables, although 2 significant loci on chromosomes 3 and 5 are detected as common across multiple variable types (i.e. precipitation, temperature, and/or soil). Distributions of allele frequencies at significant loci across subpopulations of cultivated Oryza sativa indicate that, in some cases, adaptive variation may already be present among cultivars, although evaluation in cultivated populations is needed to empirically test this. This work has implications for the potential utility of wild genetic resources in pre-breeding efforts for rice improvement.

Genome-wide association study for carcass weight in pasture-finished beef cattle in Hawai'i.

Introduction: Genome-wide association studies (GWAS) have identified genetic markers for cattle production and reproduction traits. Several publications have reported Single Nucleotide Polymorphisms (SNPs) for carcass-related traits in cattle, but these studies were rarely conducted in pasture-finished beef cattle. Hawai'i, however, has a diverse climate, and 100% of its beef cattle are pasture-fed. Methods: Blood samples were collected from 400 cattle raised in Hawai'i islands at the commercial harvest facility. Genomic DNA was isolated, and 352 high-quality samples were genotyped using the Neogen GGP Bovine 100 K BeadChip. SNPs that did not meet the quality control standards were removed using PLINK 1.9, and 85 k high-quality SNPs from 351 cattle were used for association mapping with carcass weight using GAPIT (Version 3.0) in R 4.2. Four models were used for the GWAS analysis: General Linear Model (GLM), the Mixed Linear Model (MLM), the Fixed and Random Model Circulating Probability Unification (FarmCPU), the Bayesian-Information and Linkage-Disequilibrium Iteratively Nested Keyway (BLINK). Results and Discussion: Our results indicated that the two multi-locus models, FarmCPU and BLINK, outperformed single-locus models, GLM and MLM, in beef herds in this study. Specifically, five significant SNPs were identified using FarmCPU, while BLINK and GLM each identified the other three. Also, three of these eleven SNPs ("BTA-40510-no-rs", "BovineHD1400006853", and "BovineHD2100020346") were shared by multiple models. The significant SNPs were mapped to genes such as EIF5, RGS20, TCEA1, LYPLA1, and MRPL15, which were previously reported to be associated with carcass-related traits, growth, and feed intake in several tropical cattle breeds. This confirms that the genes identified in this study could be candidate genes for carcass weight in pasture-fed beef cattle and can be selected for further breeding programs to improve the carcass yield and productivity of pasture-finished beef cattle in Hawai'i and beyond.

State spaces for agriculture: A meta-systematic design automation framework.

Agriculture is a designed system with the largest areal footprint of any human activity. In some cases, the designs within agriculture emerged over thousands of years, such as the use of rows for the spatial organization of crops. In other cases, designs were deliberately chosen and implemented over decades, as during the Green Revolution. Currently, much work in the agricultural sciences focuses on evaluating designs that could improve agriculture's sustainability. However, approaches to agricultural system design are diverse and fragmented, relying on individual intuition and discipline-specific methods to meet stakeholders' often semi-incompatible goals. This ad-hoc approach presents the risk that agricultural science will overlook nonobvious designs with large societal benefits. Here, we introduce a state space framework, a common approach from computer science, to address the problem of proposing and evaluating agricultural designs computationally. This approach overcomes limitations of current agricultural system design methods by enabling a general set of computational abstractions to explore and select from a very large agricultural design space, which can then be empirically tested.

Regulator of Awn Elongation 3, an E3 ubiquitin ligase, is responsible for loss of awns during African rice domestication.

Two species of rice have been independently domesticated from different ancestral wild species in Asia and Africa. Comparison of mutations that underlie phenotypic and physiological alterations associated with domestication traits in these species gives insights into the domestication history of rice in both regions. Asian cultivated rice, Oryza sativa, and African cultivated rice, Oryza glaberrima, have been modified and improved for common traits beneficial for humans, including erect plant architecture, nonshattering seeds, nonpigmented pericarp, and lack of awns. Independent mutations in orthologous genes associated with these traits have been documented in the two cultivated species. Contrary to this prevailing model, selection for awnlessness targeted different genes in O. sativa and O. glaberrima. We identify Regulator of Awn Elongation 3 (RAE3) a gene that encodes an E3 ubiquitin ligase and is responsible for the awnless phenotype only in O. glaberrima. A 48-bp deletion may disrupt the substrate recognition domain in RAE3 and diminish awn elongation. Sequencing analysis demonstrated low nucleotide diversity in a ~600-kb region around the derived rae3 allele on chromosome 6 in O. glaberrima compared with its wild progenitor. Identification of RAE3 sheds light on the molecular mechanism underlying awn development and provides an example of how selection on different genes can confer the same domestication phenotype in Asian and African rice.

Genomic-environmental associations in wild cranberry (Vaccinium macrocarpon Ait.).

Understanding the genetic basis of local adaptation in natural plant populations, particularly crop wild relatives, may be highly useful for plant breeding. By characterizing genetic variation for adaptation to potentially stressful environmental conditions, breeders can make targeted use of crop wild relatives to develop cultivars for novel or changing environments. This is especially appealing for improving long-lived woody perennial crops such as the American cranberry (Vaccinium macrocarpon Ait.), the cultivation of which is challenged by biotic and abiotic stresses. In this study, we used environmental association analyses in a collection of 111 wild cranberry accessions to identify potentially adaptive genomic regions for a range of bioclimatic and soil conditions. We detected 126 significant associations between SNP marker loci and environmental variables describing temperature, precipitation, and soil attributes. Many of these markers tagged genes with functional annotations strongly suggesting a role in adaptation to biotic or abiotic conditions. Despite relatively low genetic variation in cranberry, our results suggest that local adaptation to divergent environments is indeed present, and the identification of potentially adaptive genetic variation may enable a selective use of this germplasm for breeding more stress-tolerant cultivars.

Interactions between breeding system and ploidy affect niche breadth in Solanum.

Understanding the factors driving ecological and evolutionary interactions of economically important plant species is important for agricultural sustainability. The geography of crop wild relatives, including wild potatoes (Solanum section Petota), have received attention; however, such information has not been analysed in combination with phylogenetic histories, genomic composition and reproductive systems to identify potential species for use in breeding for abiotic stress tolerance. We used a combination of ordinary least-squares (OLS) and phylogenetic generalized least-squares (PGLM) analyses to identify the discrete climate classes that make up the climate niche that wild potato species inhabit in the context of breeding system and ploidy. Self-incompatible diploid or self-compatible polyploid species significantly increase the number of discrete climate classes within a climate niche inhabited. This result was sustained when correcting for phylogenetic non-independence in the linear model. Our results support the idea that specific breeding system and ploidy combinations increase niche breadth through the decoupling of geographical range and niche diversity, and therefore, these species may be of particular interest for crop adaptation to a changing climate.

Utilizing CRISPR-Cas in Tropical Crop Improvement: A Decision Process for Fitting Genome Engineering to Your Species.

Adopting modern gene-editing technologies for trait improvement in agriculture requires important workflow developments, yet these developments are not often discussed. Using tropical crop systems as a case study, we describe a workflow broken down into discrete processes with specific steps and decision points that allow for the practical application of the CRISPR-Cas gene editing platform in a crop of interest. While we present the steps of developing genome-edited plants as sequential, in practice parts can be done in parallel, which are discussed in this perspective. The main processes include 1) understanding the genetic basis of the trait along with having the crop's genome sequence, 2) testing and optimization of the editing reagents, development of efficient 3) tissue culture and 4) transformation methods, and 5) screening methods to identify edited events with commercial potential. Our goal in this perspective is to help any lab that wishes to implement this powerful, easy-to-use tool in their pipeline, thus aiming to democratize the technology.

Multi-Species Genomics-Enabled Selection for Improving Agroecosystems Across Space and Time.

Plant breeding has been central to global increases in crop yields. Breeding deserves praise for helping to establish better food security, but also shares the responsibility of unintended consequences. Much work has been done describing alternative agricultural systems that seek to alleviate these externalities, however, breeding methods and breeding programs have largely not focused on these systems. Here we explore breeding and selection strategies that better align with these more diverse spatial and temporal agricultural systems.

Meta-analysis of yield and nitrous oxide outcomes for nitrogen management in agriculture.

Improved nitrogen (N) use is key to future food security and environmental sustainability. While many regions still experience N shortages, agriculture is the leading global emitter of N2 O due to losses exacerbated by N surpluses in other regions. In order to sustainably maintain or increase food production, farmers and their advisors need a comprehensive and actionable understanding of how nutrient management affects both yield and N2 O emissions, particularly in tropical and subtropical agroecosystems. We performed a meta-analysis to determine the effect of N management and other factors on N2 O emissions, plant N uptake, and yield. Our analysis demonstrates that performance indicators-partial N balance and partial factor productivity-predicted N2 O emissions as well as or better than N rate. While we observed consistent production and environmental benefits with enhanced-efficiency fertilizers, we noted potential trade-offs between yield and N2 O emissions for fertilizer placement. Furthermore, we observed confounding effects due to management dynamics that co-vary with nutrient application practices, thus challenging the interpretation of the effect of specific practices such as fertilization frequency. Therefore, rather than providing universally prescriptive management for N2 O emission reduction, our evidence supports mitigation strategies based upon tailored nutrient management approaches that keep N balances within safe limits, so as to minimize N2 O emissions while still achieving high crop yields. The limited evidence available suggests that these relationships hold for temperate, tropical, and subtropical regions, but given the potential for expansion of N use in crop production, further N2 O data collection should be prioritized in under-represented regions such as Sub-Saharan Africa.

Tapping Diversity From the Wild: From Sampling to Implementation.

The diversity observed among crop wild relatives (CWRs) and their ability to flourish in unfavorable and harsh environments have drawn the attention of plant scientists and breeders for many decades. However, it is also recognized that the benefit gained from using CWRs in breeding is a potential rose between thorns of detrimental genetic variation that is linked to the trait of interest. Despite the increased interest in CWRs, little attention was given so far to the statistical, analytical, and technical considerations that should guide the sampling design, the germplasm characterization, and later its implementation in breeding. Here, we review the entire process of sampling and identifying beneficial genetic variation in CWRs and the challenge of using it in breeding. The ability to detect beneficial genetic variation in CWRs is strongly affected by the sampling design which should be adjusted to the spatial and temporal variation of the target species, the trait of interest, and the analytical approach used. Moreover, linkage disequilibrium is a key factor that constrains the resolution of searching for beneficial alleles along the genome, and later, the ability to deplete linked deleterious genetic variation as a consequence of genetic drag. We also discuss how technological advances in genomics, phenomics, biotechnology, and data science can improve the ability to identify beneficial genetic variation in CWRs and to exploit it in strive for higher-yielding and sustainable crops.

Toward Unifying Global Hotspots of Wild and Domesticated Biodiversity.

Global biodiversity hotspots are areas containing high levels of species richness, endemism and threat. Similarly, regions of agriculturally relevant diversity have been identified where many domesticated plants and animals originated, and co-occurred with their wild ancestors and relatives. The agro-biodiversity in these regions has, likewise, often been considered threatened. Biodiversity and agro-biodiversity hotspots partly overlap, but their geographic intricacies have rarely been investigated together. Here we review the history of these two concepts and explore their geographic relationship by analysing global distribution and human use data for all plants, and for major crops and associated wild relatives. We highlight a geographic continuum between agro-biodiversity hotspots that contain high richness in species that are intensively used and well known by humanity (i.e., major crops and most viewed species on Wikipedia) and biodiversity hotspots encompassing species that are less heavily used and documented (i.e., crop wild relatives and species lacking information on Wikipedia). Our contribution highlights the key considerations needed for further developing a unifying concept of agro-biodiversity hotspots that encompasses multiple facets of diversity (including genetic and phylogenetic) and the linkage with overall biodiversity. This integration will ultimately enhance our understanding of the geography of human-plant interactions and help guide the preservation of nature and its contributions to people.

Taro Genome Assembly and Linkage Map Reveal QTLs for Resistance to Taro Leaf Blight.

Taro (Colocasia esculenta) is a food staple widely cultivated in the humid tropics of Asia, Africa, Pacific and the Caribbean. One of the greatest threats to taro production is Taro Leaf Blight caused by the oomycete pathogen Phytophthora colocasiae Here we describe a de novo taro genome assembly and use it to analyze sequence data from a Taro Leaf Blight resistant mapping population. The genome was assembled from linked-read sequences (10x Genomics; ∼60x coverage) and gap-filled and scaffolded with contigs assembled from Oxford Nanopore Technology long-reads and linkage map results. The haploid assembly was 2.45 Gb total, with a maximum contig length of 38 Mb and scaffold N50 of 317,420 bp. A comparison of family-level (Araceae) genome features reveals the repeat content of taro to be 82%, >3.5x greater than in great duckweed (Spirodela polyrhiza), 23%. Both genomes recovered a similar percent of Benchmarking Universal Single-copy Orthologs, 80% and 84%, based on a 3,236 gene database for monocot plants. A greater number of nucleotide-binding leucine-rich repeat disease resistance genes were present in genomes of taro than the duckweed, ∼391 vs. ∼70 (∼182 and ∼46 complete). The mapping population data revealed 16 major linkage groups with 520 markers, and 10 quantitative trait loci (QTL) significantly associated with Taro Leaf Blight disease resistance. The genome sequence of taro enhances our understanding of resistance to TLB, and provides markers that may accelerate breeding programs. This genome project may provide a template for developing genomic resources in other understudied plant species.

The home field advantage of modern plant breeding.

Since the mid-20th century, crop breeding has driven unprecedented yield gains. Breeders generally select for broadly- and reliably-performing varieties that display little genotype-by-environment interaction (GxE). In contrast, ecological theory predicts that across environments that vary spatially or temporally, the most productive population will be a mixture of narrowly adapted specialists. We quantified patterns of broad and narrow adaptation in modern, commercial maize (Zea mays L.) hybrids planted across 216 site-years, from 1999-2018, for the University of Illinois yield trials. We found that location was the dominant source of yield variation (44.5%), and yearly weather was the smallest (1.7%), which suggested a benefit for reliable performance in narrow biophysical environments. Varieties displayed a large "home field advantage" when growing in the location of best performance relative to other varieties. Home field advantage accounted for 19% of GxE and provided a yield increase of 1.01 ± 0.04 Mg ∙ ha-1 (7.6% relative to mean yield), yet was both smaller than predicted by a null model and unchanged across time. This counterfactual suggests that commercial breeding programs have missed an opportunity to further increase yields by leveraging local adaptation. Public breeding programs may pursue this opportunity by releasing specialist varieties that perform reliably in narrow environments. As seed sources are increasingly privatized and consolidated, this alternate strategy may compliment private breeding to support global food security.

A Target Capture-Based Method to Estimate Ploidy From Herbarium Specimens.

Whole genome duplication (WGD) events are common in many plant lineages, but the ploidy status and possible occurrence of intraspecific ploidy variation are unknown for most species. Standard methods for ploidy determination are chromosome counting and flow cytometry approaches. While flow cytometry approaches typically use fresh tissue, an increasing number of studies have shown that recently dried specimens can be used to yield ploidy data. Recent studies have started to explore whether high-throughput sequencing (HTS) data can be used to assess ploidy levels by analyzing allelic frequencies from single copy nuclear genes. Here, we compare different approaches using a range of yam (Dioscorea) tissues of varying ages, drying methods and quality, including herbarium tissue. Our aims were to: (1) explore the limits of flow cytometry in estimating ploidy level from dried samples, including herbarium vouchers collected between 1831 and 2011, and (2) optimize a HTS-based method to estimate ploidy by considering allelic frequencies from nuclear genes obtained using a target-capture method. We show that, although flow cytometry can be used to estimate ploidy levels from herbarium specimens collected up to fifteen years ago, success rate is low (5.9%). We validated our HTS-based estimates of ploidy using 260 genes by benchmarking with dried samples of species of known ploidy (Dioscorea alata, D. communis, and D. sylvatica). Subsequently, we successfully applied the method to the 85 herbarium samples analyzed with flow cytometry, and successfully provided results for 91.7% of them, comprising species across the phylogenetic tree of Dioscorea. We also explored the limits of using this HTS-based approach for identifying high ploidy levels in herbarium material and the effects of heterozygosity and sequence coverage. Overall, we demonstrated that ploidy diversity within and between species may be ascertained from historical collections, allowing the determination of polyploidization events from samples collected up to two centuries ago. This approach has the potential to provide insights into the drivers and dynamics of ploidy level changes during plant evolution and crop domestication.

A customized nuclear target enrichment approach for developing a phylogenomic baseline for Dioscorea yams (Dioscoreaceae).

PREMISE: We developed a target enrichment panel for phylogenomic studies of Dioscorea, an economically important genus with incompletely resolved relationships. METHODS: Our bait panel comprises 260 low- to single-copy nuclear genes targeted to work in Dioscorea, assessed here using a preliminary taxon sampling that includes both distantly and closely related taxa, including several yam crops and potential crop wild relatives. We applied coalescent-based and maximum likelihood phylogenomic inference approaches to the pilot taxon set, incorporating new and published transcriptome data from additional species. RESULTS: The custom panel retrieved ~94% of targets and >80% of full gene length from 88% and 68% of samples, respectively. It has minimal gene overlap with existing panels designed for angiosperm-wide studies and generally recovers longer and more variable targets. Pilot phylogenomic analyses consistently resolve most deep and recent relationships with strong support across analyses and point to revised relationships between the crop species D. alata and candidate crop wild relatives. DISCUSSION: Our customized panel reliably retrieves targeted loci from Dioscorea, is informative for resolving relationships in denser samplings, and is suitable for refining our understanding of the independent origins of cultivated yam species; the panel likely has broader promise for phylogenomic studies across Dioscoreales.

The genomics of domestication special issue editorial.

Domestication has been of major interest to biologists for centuries, whether for creating new plants and animal types or more formally exploring the principles of evolution. Such studies have long used combinations of phenotypic and genetic evidence. Recently, the advent of a large number of genomes and genomic tools across a wide array of domesticated plant and animal species has reinvigorated the study of domestication. These genomic data, which can be easily generated for nearly any species, often provide great insight with or without a reference genome. The comparison of genome wide data from domestic and wild species has ignited a wave of insight into human, plant, and animal history with a new range of questions becoming accessible. With this in mind, this issue of Evolutionary Applications includes eleven papers covering a wide range of perspectives and methodologies relevant to understanding genomic variation under domestication.

Neo-Domestication of an Interspecific Tetraploid Helianthus annuus × Helianthus tuberous Population That Segregates for Perennial Habit.

Perennial agriculture has been proposed as an option to improve the sustainability of cropping systems, by increasing the efficiency of resource use, while also providing ecosystem services. Neo-domestication, the contemporary domestication of plants that have not previously been used in agriculture, can be used to generate new crops for these systems. Here we explore the potential of a tetraploid (2n = 4x = 68) interspecific hybrid sunflower as a perennial oilseed for use in multifunctional agricultural systems. A population of this novel tetraploid was obtained from crosses between the annual diploid oilseed crop Helianthus annuus (2n = 2x = 34) and the perennial hexaploid tuber crop Helianthus tuberosus (2n = 6x = 102). We selected for classic domestication syndrome traits for three generations. Substantial phenotypic gains were made, in some cases approaching 320%. We also analyzed the genetic basis of tuber production (i.e., perenniality), with the goal of obtaining molecular markers that could be used to facilitate future breeding in this system. Results from quantitative trait locus (QTL) mapping suggest that tuber production has an oligogenic genetic basis. Overall, this study indicates that substantial gains towards domestication goals can be achieved over contemporary time scales.