Domestication and crop evolution of wheat andbarley: Genes,genomics, and future directions

Wheat and barley are two of the founder crops of the agricultural revolution that took place 10,000 years ago in the Fertile Crescent and both crops remain among the world's most important crops. Domestication of these crops from their wild ancestors required the evolution of traits useful to humans, rather than survival in their natural environment. Of these traits, grain retention and threshability, yield improvement, changes to photoperiod sensitivity and nutritional value are most pronounced between wild and domesticated forms. Knowledge about the geographical origins of these crops and the genes responsible for domestication traits largely pre-dates the era of nextgeneration sequencing, although sequencing will lead to new insights. Molecular markers were initially used to calculate distance(relatedness), genetic diversity and to generate genetic maps which were useful in cloning major domestication genes. Both crops are characterized by large,complex genomes which were long thought to be beyond the scope of whole-genome sequencing. However, advances in sequencing technologies have improved the state of genomic resources for both wheat and barley. The availability of reference genomes for wheat and some of its progenitors,as well as for barley, sets the stage for answering unresolved questions in domestication genomics of wheat and barley.     

Gene editing of the wheat homologs of TONNEAU1‐recruiting motif encoding gene affects grain shape and weight in wheat

Grain size and weight are important components of a suite of yield‐related traits in crops. Here, we showed that the CRISPR‐Cas9 gene editing of TaGW7, a homolog of rice OsGW7 encoding a TONNEAU1‐recruiting motif (TRM) protein, affects grain shape and weight in allohexaploid wheat. By editing the TaGW7 homoeologs in the B and D genomes, we showed that mutations in either of the two or both genomes increased the grain width and weight but reduced the grain length. The effect sizes of mutations in the TaGW7 gene homoeologs coincided with the relative levels of their expression in the B and D genomes. The effects of gene editing on grain morphology and weight traits were dosage dependent with the double‐copy mutant showing larger effect than the respective single copy mutants. The TaGW7‐centered gene co‐expression network indicated that this gene is involved in the pathways regulating cell division and organ growth, also confirmed by the cellular co‐localization of TaGW7 with α‐ and β‐tubulin proteins, the building blocks of microtubule arrays. The analyses of exome capture data in tetraploid domesticated and wild emmer, and hexaploid wheat revealed the loss of diversity around TaGW7‐associated with domestication selection, suggesting that TaGW7 is likely to play an important role in the evolution of yield component traits in wheat. Our study showed how integrating CRISPR‐Cas9 system with cross‐species comparison can help to uncover the function of a gene fixed in wheat for allelic variants targeted by domestication selection and select targets for engineering new gene variants for crop improvement.     

A Genetic Framework for Grain Size and Shape Variation in Wheat

Grain morphology in wheat (Triticum aestivum) has been selected and manipulated even in very early agrarian societies and remains a major breeding target. We undertook a large-scale quantitative analysis to determine the genetic basis of the phenotypic diversity in wheat grain morphology. A high-throughput method was used to capture grain size and shape variation in multiple mapping populations, elite varieties, and a broad collection of ancestral wheat species. This analysis reveals that grain size and shape are largely independent traits in both primitive wheat and in modern varieties. This phenotypic structure was retained across the mapping populations studied, suggesting that these traits are under the control of a limited number of discrete genetic components. We identified the underlying genes as quantitative trait loci that are distinct for grain size and shape and are largely shared between the different mapping populations. Moreover, our results show a significant reduction of phenotypic variation in grain shape in the modern germplasm pool compared with the ancestral wheat species, probably as a result of a relatively recent bottleneck. Therefore, this study provides the genetic underpinnings of an emerging phenotypic model where wheat domestication has transformed a long thin primitive grain to a wider and shorter modern grain.     

Intra‐specific variance in sperm morphometry: a comparison between wild and domesticated Zebra Finches Taeniopygia guttata

The Zebra Finch Taeniopygia guttata is a model bird species for the experimental study of behavioural and evolutionary concepts in captivity and especially sexual selection. The validity of sexual selection studies of domesticated birds is of long‐standing concern as little is known about the influence of domestication on sexually selected traits. Most domesticated Zebra Finch populations are maintained under a strict breeding regime to avoid potential inbreeding. However, these breeding regimes may interfere with the processes of sexual selection and influence the evolution of sexually selected traits because they may limit or prohibit active mate choice. Here, we investigated the potential impact of a monogamous breeding scheme in a domesticated population in which active mate choice is largely inhibited, on the evolution of sperm morphometry as a sexually selected trait. We compared sperm morphometric traits (total sperm length and length of sperm head, midpiece and flagellum), and the variance thereof, between a domesticated and two wild Zebra Finch populations. Although we found significant differences between the three populations for certain sperm traits (head length, midpiece length), which may be of importance in postcopulatory sexual selection, overall, variance in sperm morphometry did not differ between the domesticated and the wild Zebra Finch populations. Our results validate the use of domesticated Zebra Finches for further studies of postcopulatory sexual selection and sperm competition.     

Hybridisation‐based target enrichment of phenology genes to dissect the genetic basis of yield and adaptation in barley

Barley (Hordeum vulgare L.) is a major cereal grain widely used for livestock feed, brewing malts and human food. Grain yield is the most important breeding target for genetic improvement and largely depends on optimal timing of flowering. Little is known about the allelic diversity of genes that underlie flowering time in domesticated barley, the genetic changes that have occurred during breeding, and their impact on yield and adaptation. Here, we report a comprehensive genomic assessment of a worldwide collection of 895 barley accessions based on the targeted resequencing of phenology genes. A versatile target‐capture method was used to detect genome‐wide polymorphisms in a panel of 174 flowering time‐related genes, chosen based on prior knowledge from barley, rice and Arabidopsis thaliana. Association studies identified novel polymorphisms that accounted for observed phenotypic variation in phenology and grain yield, and explained improvements in adaptation as a result of historical breeding of Australian barley cultivars. We found that 50% of genetic variants associated with grain yield, and 67% of the plant height variation was also associated with phenology. The precise identification of favourable alleles provides a genomic basis to improve barley yield traits and to enhance adaptation for specific production areas.     

Genetic architecture of quantitative trait loci associated with morphological and agronomic trait differences in a wild by cultivated barley cross.

Hordeum vulgare subsp. spontaneum is the progenitor of cultivated barley (Hordeum vulgare L.). Domestication combined with plant breeding has led to the morphological and agronomic characteristics of modern barley cultivars. The objective of this study was to map the genetic factors that morphologically and agronomically differentiate wild barley from modern barley cultivars. To address this objective, we identified quantitative trait loci (QTLs) associated with plant height, flag leaf width, spike length, spike width, glume length in relation to seed length, awn length, fragility of ear rachis, endosperm width and groove depth, heading date, flag leaf length, number of tillers per plant, and kernel color in a Harrington/OUH602 advanced backcross (BC2F8) population. This population was genotyped with 113 simple sequence repeat markers. Thirty QTLs were identified, of which 16 were newly identified in this study. One to 4 QTLs were identified for each of the traits except glume length, for which no QTL was detected. The portion of phenotypic variation accounted for by individual QTLs ranged from about 9% to 54%. For traits with more than one QTL, the phenotypic variation explained ranged from 25% to 71%. Taken together, our results reveal the genetic architecture of morphological and agronomic traits that differentiate wild from cultivated barley.     

Gel observation chamber for rapid screening of root traits in cereal seedlings

A simple gel chamber is described for measurement of seedling root traits. Seedlings are located between two closely spaced flat layers of transparent gel, on plastic plates (at least one of which is transparent). Root system traits can be non-destructively recorded in two-dimensions using a flatbed scanner. Easily measured rooting traits include root length, elongation rate, longest root, deepest root, seminal root number, and angular spread of roots. Examples of wild, landrace, and cultivated barleys were grown in the gel chambers, between gel layers or in loosely packed soil. Root growth on the gel plates was similar to that in loose soil, with the cultivated barley having the most seminal axes (about 7), and widest angular spread of roots (about 120 °), and wild barley the fewest seminal axes (about 3), and narrowest angular spread of roots (about 40 °). Landrace barley lines tested were intermediate between wild barley and modern cultivars. Separate experiments were performed to study the effect of grain mass and grain size on these rooting traits. These experiments included parents of genetic mapping populations. Seminal root number was most strongly dependent on grain mass in the modern cultivar Chime. Grain size significantly influenced root number in the modern cultivar Derkado, the breeding line B83-12/21/5, and a selection from a landrace Tadmor, suggesting that grain size should be controlled in any screening exercise.     

Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity

The control of flowering is central to reproductive success in plants, and has a major impact on grain yield in crop species. The global importance of temperate cereal crops such as wheat and barley has meant emphasis has long been placed on understanding the genetics of flowering in order to enhance yield. Leads gained from the dissection of the molecular genetics of model species have combined with comparative genetic approaches, recently resulting in the isolation of the first flowering time genes in wheat and barley. This paper reviews the genetics and genes involved in cereal flowering pathways and the current understanding of how two of the principal genes, Vrn and Ppd, have been involved in domestication and adaptation to local environments, and the implications for future breeding programmes are discussed.     

Integrating cereal genomics to support innovation in the Triticeae

The genomic resources of small grain cereals that include some of the most important crop species such as wheat, barley, and rye are attaining a level of completion that now is contributing to new structural and functional studies as well as refining molecular marker development and mapping strategies for increasing the efficiency of breeding processes. The integration of new efforts to obtain reference sequences in bread wheat and barley, in particular, is accelerating the acquisition and interpretation of genome-level analyses in both of these major crops.     

Wheat domestication: lessons for the future

Wheat was one of the first crops to be domesticated more than 10,000 years ago in the Middle East. Molecular genetics and archaeological data have allowed the reconstruction of plausible domestication scenarios leading to modern cultivars. For diploid einkorn and tetraploid durum wheat, a single domestication event has likely occurred in the Karacadag Mountains, Turkey. Following a cross between tetraploid durum and diploid T.?tauschii, the resultant hexaploid bread wheat was domesticated and disseminated around the Caucasian region. These polyploidisation events facilitated wheat domestication and created genetic bottlenecks, which excluded potentially adaptive alleles. With the urgent need to accelerate genetic progress to confront the challenges of climate change and sustainable agriculture, wild ancestors and old landraces represent a reservoir of underexploited genetic diversity that may be utilized through modern breeding methods. Understanding domestication processes may thus help identifying new strategies.     

Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World

BACKGROUND: Archaeobotany, the study of plant remains from sites of ancient human activity, provides data for studying the initial evolution of domesticated plants. An important background to this is defining the domestication syndrome, those traits by which domesticated plants differ from wild relatives. These traits include features that have been selected under the conditions of cultivation. From archaeological remains the easiest traits to study are seed size and in cereal crops the loss of natural seed dispersal. SCOPE: The rate at which these features evolved and the ordering in which they evolved can now be documented for a few crops of Asia and Africa. This paper explores this in einkorn wheat (Triticum monococcum) and barley (Hordeum vulgare) from the Near East, rice (Oryza sativa) from China, mung (Vigna radiata) and urd (Vigna mungo) beans from India, and pearl millet (Pennisetum glaucum) from west Africa. Brief reference is made to similar data on lentils (Lens culinaris), peas (Pisum sativum), soybean (Glycine max) and adzuki bean (Vigna angularis). Available quantitative data from archaeological finds are compiled to explore changes with domestication. The disjunction in cereals between seed size increase and dispersal is explored, and rates at which these features evolved are estimated from archaeobotanical data. Contrasts between crops, especially between cereals and pulses, are examined. CONCLUSIONS: These data suggest that in domesticated grasses, changes in grain size and shape evolved prior to non-shattering ears or panicles. Initial grain size increases may have evolved during the first centuries of cultivation, within perhaps 500-1000 years. Non-shattering infructescences were much slower, becoming fixed about 1000-2000 years later. This suggests a need to reconsider the role of sickle harvesting in domestication. Pulses, by contrast, do not show evidence for seed size increase in relation to the earliest cultivation, and seed size increase may be delayed by 2000-4000 years. This implies that conditions that were sufficient to select for larger seed size in Poaceae were not sufficient in Fabaceae. It is proposed that animal-drawn ploughs (or ards) provided the selection pressure for larger seeds in legumes. This implies different thresholds of selective pressure, for example in relation to differing seed ontogenetics and underlying genetic architecture in these families. Pearl millet (Pennisetum glaucum) may show some similarities to the pulses in terms of a lag-time before truly larger-grained forms evolved.     

籼型黑米粒形性状的遗传效应及其与矿质元素含量的遗传相关性

采用禾谷类作物种子数量性状的遗传模型,分析了灿型黑米稻品种双列杂交F1和F2种子的粒重,粒长,粒宽和粒长／粒宽等粒形性状的遗传效应及其与米粒中矿质元素Fe,Zn,Mn和P含量的遗传相关性,结果表明：4种粒形性状同时受制于种子直接遗传效应,母体效应和细胞质作用影响,其中种子直接遗传效应比母体效应和细胞质效应的作用更大,且种子直接遗传效应以加性效应占主导,粒重,粒宽和粒长／粒宽的种子直接遗传率较高,杂种早代单粒选择效果较好,粒长的种子直接遗传率和母体遗传率均属中等,较高世代的杂种进行单株选择和单粒选择均有一定效果,4种粒形性状与其米粒中矿质元素Fe,Zn,Mn和P含量表现较强的种子直接加性相关,直接显性相关,细胞质相关,母体加性相关和母体显性相关,在特种稻育种实践中,可以通过粒形性的间接选择,达到改良其矿质元素含量等营养品质性状的目标。     

An APETALA1 ortholog affects plant architecture and seed yield component in oilseed rape (Brassica napus L.)

Exploring the natural occurring genetic variation of the wild barley genepool has become a major target of barley crop breeding programmes aiming to increase crop productivity and sustainability in global climate change scenarios. However this diversity remains unexploited and effective approaches are required to investigate the benefits that unadapted genomes could bring to crop improved resilience. In the present study, a set of Recombinant Chromosome Substitution Lines (RCSLs) derived from an elite barley cultivar ‘Harrington’ as the recurrent parent, and a wild barley accession from the Fertile Crescent ‘Caesarea 26–24’, as the donor parent (Matus et al. Genome 46:1010–23, 2003) have been utilised in field and controlled conditions to examine the contribution of wild barley genome as a source of novel allelic variation for the cultivated barley genepool. Twenty-eight RCSLs which were selected to represent the entire genome of the wild barley accession, were genotyped using the 9 K iSelect SNP markers (Comadran et al. Nat Genet 44:1388–92, 2012) and phenotyped for a range of morphological, developmental and agronomic traits in 2 years using a rain-out shelter with four replicates and three water treatments. Data were analysed for marker traits associations using a mixed model approach. We identified lines that differ significantly from the elite parent for both qualitative and quantitative traits across growing seasons and water regimes. The detailed genotypic characterisation of the lines for over 1800 polymorphic SNP markers and the design of a mixed model analysis identified chromosomal regions associated with yield related traits where the wild barley allele had a positive response increasing grain weight and size. In addition, variation for qualitative characters, such as the presence of cuticle waxes on the developing spikes, was associated with the wild barley introgressions. Despite the coarse location of the QTLs, interesting candidate genes for the major marker-trait associations were identified using the recently released barley genome assembly. This study has highlighted the role of exotic germplasm to contribute novel allelic variation by using an optimised experimental approach focused on an exotic genetic library. The results obtained constitute a step forward to the development of more tolerant and resilient varieties.     

Transcript-specific, single-nucleotide polymorphism discovery and linkage analysis in hexaploid bread wheat (Triticum aestivum L.)

Food security is a global concern and substantial yield increases in cereal crops are required to feed the growing world population. Wheat is one of the three most important crops for human and livestock feed. However, the complexity of the genome coupled with a decline in genetic diversity within modern elite cultivars has hindered the application of marker‐assisted selection (MAS) in breeding programmes. A crucial step in the successful application of MAS in breeding programmes is the development of cheap and easy to use molecular markers, such as single‐nucleotide polymorphisms. To mine selected elite wheat germplasm for intervarietal single‐nucleotide polymorphisms, we have used expressed sequence tags derived from public sequencing programmes and next‐generation sequencing of normalized wheat complementary DNA libraries, in combination with a novel sequence alignment and assembly approach. Here, we describe the development and validation of a panel of 1114 single‐nucleotide polymorphisms in hexaploid bread wheat using competitive allele‐specific polymerase chain reaction genotyping technology. We report the genotyping results of these markers on 23 wheat varieties, selected to represent a broad cross‐section of wheat germplasm including a number of elite UK varieties. Finally, we show that, using relatively simple technology, it is possible to rapidly generate a linkage map containing several hundred single‐nucleotide polymorphism markers in the doubled haploid mapping population of Avalon × Cadenza.     

Haplotype structure at seven barley genes: relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication

Archaeological remains indicate that the origin of western agriculture occurred in a brief period about 10,500 years ago in a region of the Middle East known as the Fertile Crescent, where the wild progenitors of several key agricultural cereal species are endemic. Domestication entailed the appearance of agronomic traits such as seed size and threshability. For a representative sample of 20 domesticated barley (Hordeum vulgare) lines, including 13 two-rowed and 7 six-rowed varieties, we determined the haplotypes at seven loci-Adh2, Adh3, Amy1, Dhn9, GAPDH, PEPC and WAXY encompassing 5,616 bases per line-and compared them to the haplotypes at the same loci for 25 wild forms (Hordeum spontaneum) collected within and outside the Fertile Crescent. In comparisons of wild versus domesticated barley, the number of haplotypes (70 vs. 17), average nucleotide diversity, pi, (0.0077 vs. 0.0028), and Watterson's theta at silent sites (0.0104 vs. 0.0028) was reduced in domesticated lines. Two loci, Amy1 and PEPC, were monomorphic in domesticated lines; Amy1 and GAPDH produced significant values of Tajima's D. At GAPDH, pi was slightly higher in domesticated than wild forms, due to divergent high-frequency haplotypes; for the remaining six loci, 87% of nucleotide diversity has been lost in the domesticated forms. Bottlenecks acting on neutrally evolving loci either during the domestication process, during subsequent breeding, or both, are sufficient to account for reduced diversity and the results of Tajima's test, without the need to evoke selection at these loci. Phylogenetic networks data uncover distinct wild and domesticated barley genotypes and suggest that barley may have been domesticated in the Jordan valley. Because, based on AFLP data, the domesticated Turkish cultivars had a genetic basis as large as that present in large germplasm collections, all comparisons provided in this paper are of general value more than being restricted to the Turkish barley germplasm.     

Trends in Biomass Fractionation in Wheat and Barley from Wild Ancestors to Modern Cultivars

Abstract: We tested the hypothesis that cultivar selection during the process of domestication in cereal plants led to a change in dry mass allocation, e.g., less root mass and more leaf mass or more leaf area per unit leaf mass. We divided 24 varieties of diploid, tetraploid and hexaploid winter wheat and two-rowed winter barley into three categories of domestication levels (wild species, old landraces and modern cultivars) and compared the patterns of dry matter fractionation at the time of anthesis under standardized outdoor growth conditions. In both cereals, total biomass per individual increased significantly with domestication level but, to our surprise, we found no significant change in dry matter investment between domestication levels: neither the dry mass fraction of leaves increased, nor was there a trend of reduced investment in stems and roots, contrary to what we expected. Specific leaf area (SLA) and leaf area ratio (LAR) of modern wheat and barley cultivars were significantly lower compared to wild varieties. Major differences in both cereals were of a purely morphological nature, namely a decrease in the number of stems and ears from wild species to domesticated varieties, along with more synchronous tiller development and therefore similar tiller size. Fertilizer increased total biomass in all domestication levels in both cereals, but influenced the dry matter fractionation only in barley. Tissue nitrogen concentration was unresponsive to both domestication and fertilization. The expected shift in functional traits, conventionally considered to determine plant growth, was not found. Indeed, dry matter fractionation among the major plant biomass components seems to be very conservative.     

Quantifying relationships between rooting traits and water uptake under drought in Mediterranean barley and durum wheat

In Mediterranean regions drought is the major factor limiting spring barley and durum wheat grain yields. This study aimed to compare spring barley and durum wheat root and shoot responses to drought and quantify relationships between root traits and water uptake under terminal drought.One spring barley（Hordeum vulgare L. cv. Rum） and two durum wheat Mediterranean cultivars（Triticum turgidum L. var durum cvs Hourani and Karim） were examined in soil‐column experiments under well watered and drought conditions. Root system architecture traits, water uptake, and plant growth were measured. Barley aerial biomass and grain yields were higher than for durum wheat cultivars in well watered conditions. Drought decreased grain yield more for barley（47%） than durum wheat（30%, Hourani）. Root‐to‐shoot dry matter ratio increased for durum wheat under drought but not for barley, and root weight increased for wheat in response todrought but decreased for barley. The critical root length density（RLD） and root volume density（RVD） for 90% available water capture for wheat were similar to（cv. Hourani） or lower than（cv. Karim） for barley depending on wheat cultivar. For both species, RVD accounted for a slightly higher proportion of phenotypic variation in water uptake under drought than RLD.     

Wild barley: a source of genes for crop improvement in the 21st century?

The development of new barleys tolerant of abiotic and biotic stresses is an essential part of the continued improvement of the crop. The domestication of barley, as in many crops, resulted in a marked truncation of the genetical variation present in wild populations. This process is significant to agronomists and scientists because a lack of allelic variation will prevent the development of adapted cultivars and hinder the investigation of the genetic mechanisms underlying performance. Wild barley would be a useful source of new genetic variation for abiotic stress tolerance if surveys identify appropriate genetic variation and the development of marker-assisted selection allows efficient manipulation in cultivar development. There are many wild barley collections from all areas of its natural distribution, but the largest are derived from the Mediterranean region. The results of a range of assays designed to explore abiotic stress tolerance in barley are reported in this paper. The assays included; sodium chloride uptake in wild barley and a mapping population, effects for delta 13C and plant dry weight in wheat aneuploids, effects of photoperiod and vernalization in wild barley, and measurements of root length in wild barley given drought and nitrogen starvation treatments in hydroponic culture. There are examples of the use of wild barley in breeding programmes, for example, as a source of new disease resistance genes, but the further exploration of the differences between wild barley and cultivars is hampered by the lack of good genetic maps. In parallel to the need for genetic studies there is also a need for the development of good physiological models of crop responses to the environment. Given these tools, wild barley offers the prospect of a 'goldmine' of untapped genetic reserves.     

Experimental and modelling studies of drought‐adaptive root architectural traits in wheat (Triticum aestivum L.)

Abstract

This paper presents an interdisciplinary approach to crop improvement that links physiology with plant breeding and simulation modelling to enhance the selection of high‐yielding, drought‐tolerant varieties. In a series of field experiments in Queensland, Australia, we found that the yield of CIMMYT wheat line SeriM82 ranged from 6% to 28% greater than the current cultivar Hartog. Physiological studies on the adaptive traits revealed that SeriM82 had a narrower root architecture and extracted more soil moisture, particularly deep in the profile. Results of a simulation analysis of these adaptive root traits with the cropping system model APSIM for a range of rain‐fed environments in southern Queensland indicated a mean relative yield benefit of 14.5% in water‐deficit seasons. Furthermore, each additional millimetre of water extracted during grain filling generated an extra 55 kg ha^?1 of grain yield. Further root studies of a large number of wheat genotypes revealed that wheat root architecture is closely linked to the angle of seminal roots at the seedling stage – a trait which is suitable for large‐scale and cost‐effective screening programmes. Overall, our results suggest that an interdisciplinary approach to crop improvement is likely to enhance the rate of yield improvement in rain‐fed crops.