All roads lead to weediness: Patterns of genomic divergence reveal extensive recurrent weedy rice origins from South Asian Oryza

Weedy rice (Oryza spp.), a weedy relative of cultivated rice (O. sativa), infests and persists in cultivated rice fields worldwide. Many weedy rice populations have evolved similar adaptive traits, considered part of the ‘agricultural weed syndrome’, making this an ideal model to study the genetic basis of parallel evolution. Understanding parallel evolution hinges on accurate knowledge of the genetic background and origins of existing weedy rice groups. Using population structure analyses of South Asian and US weedy rice, we show that weeds in South Asia have highly heterogeneous genetic backgrounds, with ancestry contributions both from cultivated varieties (aus and indica) and wild rice. Moreover, the two main groups of weedy rice in the USA, which are also related to aus and indica cultivars, constitute a separate origin from that of Asian weeds. Weedy rice populations in South Asia largely converge on presence of red pericarps and awns and on ease of shattering. Genomewide divergence scans between weed groups from the USA and South Asia, and their crop relatives are enriched for loci involved in metabolic processes. Some candidate genes related to iconic weedy traits and competitiveness are highly divergent between some weed‐crop pairs, but are not shared among all weed‐crop comparisons. Our results show that weedy rice is an extreme example of recurrent evolution, and suggest that most populations are evolving their weedy traits through different genetic mechanisms.     

Molecular insights into the evolution of crop plants

The domestication and improvement of crop plants have long fascinated evolutionary biologists, geneticists, and anthropologists. In recent years, the development of increasingly powerful molecular and statistical tools has reinvigorated this now fast-paced field of research. In this paper, we provide an overview of how such tools have been applied to the study of crop evolution. We also highlight lessons that have been learned in light of a few long-standing and interrelated hypotheses concerning the origins of crop plants and the nature of the genetic changes underlying their evolution. We conclude by discussing compelling evolutionary genomic approaches that make possible the efficient and unbiased identification of genes controlling crop-related traits and provide further insight into the actual timing of selection on particular genomic regions.     

Population genetic analysis of safflower (Carthamus tinctorius; Asteraceae) reveals a Near Eastern origin and five centers of diversity

Analyses of genetic variation in crop gene pools are a powerful tool for investigating the origin and early evolution of crop lineages. Such analyses also have the potential to identify unique genetic resources for continued crop improvement. The oilseed crop safflower (Carthamus tinctorius) is believed to have been domesticated in the Fertile Crescent region, but up to 10 geographic centers of similarity throughout the world have been proposed based on morphology. Nuclear microsatellite analysis of accessions from each of the 10 proposed centers of similarity, as well as individuals of the progenitor species, suggested the presence of five genetic clusters (1, Europe; 2, Turkey-Iran-Iraq-Afghanistan; 3, Israel-Jordan-Syria; 4, Egypt-Ethiopia; and 5, the Far East-India-Pakistan). North American accessions, products of a secondary introduction from the native range, suggest that a subset of the native accessions harbor unique genetic diversity that could be useful in future breeding efforts. Overall, a Near Eastern origin of safflower was confirmed based on the genetic similarity between the progenitor and the Near Eastern safflower accessions, as well as previous archaeological finds. Genetic differentiation between geographical clusters of accessions is evident, although not to the degree proposed based on morphology.     

The Puzzle of Italian Rice Origin and Evolution: Determining Genetic Divergence and Affinity of Rice Germplasm from Italy and Asia

The characterization of genetic divergence and relationships of a set of germplasm is essential for its efficient applications in crop breeding and understanding of the origin/evolution of crop varieties from a given geographical region. As the largest rice producing country in Europe, Italy holds rice germplasm with abundant genetic diversity. Although Italian rice varieties and the traditional ones in particular have played important roles in rice production and breeding, knowledge concerning the origin and evolution of Italian traditional varieties is still limited. To solve the puzzle of Italian rice origin, we characterized genetic divergence and relationships of 348 rice varieties from Italy and Asia based on the polymorphisms of microsatellite fingerprints. We also included common wild rice O. rufipogon as a reference in the characterization. Results indicated relatively rich genetic diversity (H _e = 0.63-0.65) in Italian rice varieties. Further analyses revealed a close genetic relationship of the Italian traditional varieties with those from northern China, which provides strong genetic evidence for tracing the possible origin of early established rice varieties in Italy. These findings have significant implications for the rice breeding programs, in which appropriate germplasm can be selected from a given region and utilized for transferring unique genetic traits based on its genetic diversity and evolutionary relationships.     

Plant genome archaeology: evidence for conserved ancestral chromosome segments in dicotyledonous plant species

We have developed genetic maps, based on expressed sequence tags (ESTs) that are homologous to Arabidopsis genes, in four dicotyledonous crop plant species from different families. A comparison of these maps with the physical map of Arabidopsis reveals common genome segments that appear to have been conserved throughout the evolution of the dicots. In the four crop species analysed these segments comprise between 16 and 33% of the Arabidopsis genome. Our findings extend the synteny patterns previously observed only within plant families, and indicate that structural and functional information from the model species will be, at least in part, applicable in crop plants with large genomes.     

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

Convergent phenotypic evolution provides some of the strongest evidence for adaptation. However, the extent to which recurrent phenotypic adaptation has arisen via parallelism at the molecular level remains unresolved, as does the evolutionary origin of alleles underlying such adaptation. Here, we investigate genetic mechanisms of convergent highland adaptation in maize landrace populations and evaluate the genetic sources of recurrently selected alleles. Population branch excess statistics reveal substantial evidence of parallel adaptation at the level of individual single-nucleotide polymorphism (SNPs), genes, and pathways in four independent highland maize populations. The majority of convergently selected SNPs originated via migration from a single population, most likely in the Mesoamerican highlands, while standing variation introduced by ancient gene flow was also a contributor. Polygenic adaptation analyses of quantitative traits reveal that alleles affecting flowering time are significantly associated with elevation, indicating the flowering time pathway was targeted by highland adaptation. In addition, repeatedly selected genes were significantly enriched in the flowering time pathway, indicating their significance in adapting to highland conditions. Overall, our study system represents a promising model to study convergent evolution in plants with potential applications to crop adaptation across environmental gradients.     

Arabidopsis paves the way: genomic and network analyses in crops

Arabidopsis genomic and network analyses have facilitated crop research towards the understanding of many biological processes of fundamental importance for agriculture. Genes that were identified through genomic analyses in Arabidopsis have been used to manipulate crop traits such as pathogen resistance, yield, water-use efficiency, and drought tolerance, with the effects being tested in field conditions. The integration of diverse Arabidopsis genome-wide datasets in probabilistic functional networks has been demonstrated as a feasible strategy to associate novel genes with traits of interest, and novel genomic methods continue to be developed. The combination of genome-wide location studies, using ChIP-Seq, with gene expression profiling data is affording a genome-wide view of regulatory networks previously delineated through genetic and molecular analyses, leading to the identification of novel components and of new connections within these networks.     

Strigolactones and shoot branching: a new trick for a young dog

Strigolactones secreted by plant roots are exploited by parasitic plants as germination triggers, making their synthesis and signaling important targets for crop protection. Meanwhile, genetic analyses have identified several genes required for the synthesis and signaling of an unknown shoot branching inhibitor. Two recent papers unite these two fields, showing that strigolactones control shoot branching.     

The Application of Reverse Genetics to Polyploid Plant Species

Polyploidy events (polyploidization) followed by progressive loss of redundant genome components are a major feature of plant evolution, with new evidence suggesting that all flowering plants possess ancestral genome duplications. Furthermore, many of our most important crop plants have undergone additional, relatively recent, genome duplication events. Recent advances in DNA sequencing have made vast amounts of new genomic data available for many plants, including a range of important crop species with highly duplicated genomes. Along with assisting traditional forward genetics approaches to study gene function, this wealth of new sequence data facilitates extensive reverse genetics-based functional analyses. However, plants featuring high levels of genome duplication as a result of recent polyploidization pose additional challenges for reverse genetic analysis. Here we review reverse genetic analysis in such polyploid plants and highlight key challenges.     

Evolutionary dynamics of genes controlling floral development

Advances in the understanding of floral developmental genetics in model species such as Arabidopsis continue to provide an important foundation for comparative studies in other flowering plants. In particular, floral organ identity genes are the focus of many projects that are addressing both ancient and recent evolutionary questions. Expanded analyses of the evolution of these gene lineages have highlighted the dynamic nature of the gene birth-and-death process, and may have significant implications for the evolution of genetic pathways. Crucial functional studies of floral organ identity genes in diverse taxa are allowing the first real insight into the conservation of gene function, while findings on the genetic control of organ elaboration offer to open up new avenues for investigation. Taken together, these trends show that the field of floral developmental evolution continues to make significant progress towards elucidating the processes that have shaped the evolution of flower development and morphology.     

基于双碱基编辑系统的植物基因靶向随机突变技术

遗传性变异是表型多样性的基础,靶向饱和突变作物基因可以促进产生具有优异农艺性状的突变体。相较于传统诱变育种和异源物种中的定向进化方法,基于双碱基编辑系统的植物基因靶向随机突变技术可对植物内源基因产生高效突变,从而实现原位定向进化,加快植物育种及功能基因研究进程。该文介绍了使用饱和靶向内源基因突变编辑器(STEME)对植...     

Diversifying mechanisms in the on‐farm evolution of crop mixtures

While modern agriculture relies on genetic homogeneity, diversifying practices associated with seed exchange and seed recycling may allow crops to adapt to their environment. This socio‐genetic model is an original experimental evolution design referred to as on‐farm dynamic management of crop diversity. Investigating such model can help in understanding how evolutionary mechanisms shape crop diversity submitted to diverse agro‐environments. We studied a French farmer‐led initiative where a mixture of four wheat landraces called ‘Mélange de Touselles’ (MDT) was created and circulated within a farmers' network. The 15 sampled MDT subpopulations were simultaneously submitted to diverse environments (e.g. altitude, rainfall) and diverse farmers' practices (e.g. field size, sowing and harvesting date). Twenty‐one space‐time samples of 80 individuals each were genotyped using 17 microsatellite markers and characterized for their heading date in a ‘common‐garden’ experiment. Gene polymorphism was studied using four markers located in earliness genes. An original network‐based approach was developed to depict the particular and complex genetic structure of the landraces composing the mixture. Rapid differentiation among populations within the mixture was detected, larger at the phenotypic and gene levels than at the neutral genetic level, indicating potential divergent selection. We identified two interacting selection processes: variation in the mixture component frequencies, and evolution of within‐variety diversity, that shaped the standing variability available within the mixture. These results confirmed that diversifying practices and environments maintain genetic diversity and allow for crop evolution in the context of global change. Including concrete measurements of farmers' practices is critical to disentangle crop evolution processes.     

Beyond Arabidopsis. Translational biology meets evolutionary developmental biology

Developmental processes shape plant morphologies, which constitute important adaptive traits selected for during evolution. Identifying the genes that act in developmental pathways and determining how they are modified during evolution is the focus of the field of evolutionary developmental biology, or evo-devo. Knowledge of genetic pathways in the plant model Arabidopsis serves as the starting point for investigating how the toolkit of developmental pathways has been used and reused to form different plant body plans. One productive approach is to identify genes in other species that are orthologous to genes known to control developmental pathways in Arabidopsis and then determine what changes have occurred in the protein coding sequence or in the gene's expression to produce an altered morphology. A second approach relies on natural variation among wild populations or crop plants. Natural variation can be exploited to identify quantitative trait loci that underlie important developmental traits and, thus, define those genes that are responsible for adaptive changes. The possibility of applying comparative genomics approaches to Arabidopsis and related species promises profound new insights into the interplay of evolution and development.     

Frequent recent origination of brain genes shaped the evolution of foraging behavior in Drosophila

The evolution of the brain and behavior are coupled puzzles. The genetic bases for brain evolution are widely debated, yet whether newly evolved genes impact the evolution of the brain and behavior is vaguely understood. Here, we show that during recent evolution in Drosophila, new genes have frequently acquired neuronal expression, particularly in the mushroom bodies. Evolutionary signatures combined with expression profiling showed that natural selection influenced the evolution of young genes expressed in the brain, notably in mushroom bodies. Case analyses showed that two young retrogenes are expressed in the olfactory circuit and facilitate foraging behavior. Comparative behavioral analysis revealed divergence in foraging behavior between species. Our data suggest that during adaptive evolution, new genes gain expression in specific brain structures and evolve new functions in neural circuits, which might contribute to the phenotypic evolution of animal behavior.     

Evidence of selection on fatty acid biosynthetic genes during the evolution of cultivated sunflower

The identification of genes underlying the phenotypic transitions that took place during crop evolution, as well as the genomic extent of resultant selective sweeps, is of great interest to both evolutionary biologists and applied plant scientists. In this study, we report the results of a molecular evolutionary analysis of 11 genes that underlie fatty acid biosynthesis and metabolism in wild and cultivated sunflower (Helianthus annuus). Seven of these 11 genes showed evidence of selection at the nucleotide level, with 1 (FAD7) having experienced selection prior to domestication, 2 (FAD2-3 and FAD3) having experienced selection during domestication, and 4 (FAB1, FAD2-1, FAD6, and FATB) having experienced selection during the subsequent period of improvement. Sequencing of a subset of these genes from an extended panel of sunflower cultivars revealed little additional variation, and an analysis of the genomic region surrounding one of these genes (FAD2-1) revealed the occurrence of an extensive selective sweep affecting a region spanning at least ca. 100 kb. Given that previous population genetic analyses have revealed a relatively rapid decay of linkage disequilibrium in sunflower, this finding indicates the occurrence of strong selection and a rapid sweep.     

More than one way to evolve a weed: parallel evolution of US weedy rice through independent genetic mechanisms

Many different crop species were selected for a common suite of ‘domestication traits’, which facilitates their use for studies of parallel evolution. Within domesticated rice (Oryza sativa), there has also been independent evolution of weedy strains from different cultivated varieties. This makes it possible to examine the genetic basis of parallel weed evolution and the extent to which this process occurs through shared genetic mechanisms. We performed comparative QTL mapping of weediness traits using two recombinant inbred line populations derived from crosses between an indica crop variety and representatives of each of the two independently evolved weed strains found in US rice fields, strawhull (S) and blackhull awned (B). Genotyping‐by‐sequencing provided dense marker coverage for linkage map construction (average marker interval <0.25 cM), with 6016 and 13 730 SNPs mapped in F₅ lines of the S and B populations, respectively. For some weediness traits (awn length, hull pigmentation and pericarp pigmentation), QTL mapping and sequencing of underlying candidate genes confirmed that trait variation was largely attributable to individual loci. However, for more complex quantitative traits (including heading date, panicle length and seed shattering), we found multiple QTL, with little evidence of shared genetic bases between the S and B populations or across previous studies of weedy rice. Candidate gene sequencing revealed causal genetic bases for 8 of 27 total mapped QTL. Together these findings suggest that despite the genetic bottleneck that occurred during rice domestication, there is ample genetic variation in this crop to allow agricultural weed evolution through multiple genetic mechanisms.     

Duplicative transfer of a MADS box gene to a plant Y chromosome

Y chromosomes carry genes with functions in male reproduction and often have few other loci. Their evolution and the causes of genetic degeneration are of great interest. In addition to genetic degeneration, the acquisition of autosomal genes may be important in Y chromosome evolution. We here report that the dioecious plant Silene latifolia harbors a complete MADS box gene, SlAP3Y, duplicated onto the Y chromosome. This gene has no X-linked homologs but only an autosomal paralog, SlAP3A, and sequence divergence suggests that the duplication is a quite old event that occurred soon after the evolution of the sex chromosomes. Evolutionary sequence analyses using homologs of closely related species, including hermaphroditic Silene conica and dioecious Silene dioica and Silene diclinis, suggest that both SlAP3A and SlAP3Y genes encode functional proteins. Indeed, quantitative RT-PCR and in situ hybridization analyses showed that SlAP3A is expressed specifically in developing petals, but SlAP3Y is much more strongly expressed in developing stamens. The S. conica homolog, ScAP3A, is expressed in developing petals, suggesting subfunctionalization with evolution of male-specific functions, possibly due to evolutionary change in regulatory elements. Our results suggest that the acquisition of autosomal genes is an important event in the evolution of plant Y chromosomes.     

New perspectives on the origin and evolution of new world domesticated plants: Introduction

The symposium “New perspectives on the origin and evolution of New World domesticated plants” includes nine papers that all deal with the systematic relationships, center(s) of origin, and genetic diversity of particular New World crops. Recent molecular analyses and fieldwork in remote regions have supplied much new biosystematic evidence bearing on these topics. This new evidence, as well as the further integration of plant breeding, systematic/evolutionary, ethnobotanical, and archaeobotanical research, has done much to clarify New World crop origins and evolution.     

Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers

Pigeonpea is an important legume food crop grown primarily by smallholder farmers in many semi-arid tropical regions of the world. We used the Illumina next-generation sequencing platform to generate 237.2 Gb of sequence, which along with Sanger-based bacterial artificial chromosome end sequences and a genetic map, we assembled into scaffolds representing 72.7% (605.78 Mb) of the 833.07 Mb pigeonpea genome. Genome analysis predicted 48,680 genes for pigeonpea and also showed the potential role that certain gene families, for example, drought tolerance-related genes, have played throughout the domestication of pigeonpea and the evolution of its ancestors. Although we found a few segmental duplication events, we did not observe the recent genome-wide duplication events observed in soybean. This reference genome sequence will facilitate the identification of the genetic basis of agronomically important traits, and accelerate the development of improved pigeonpea varieties that could improve food security in many developing countries.