Genomes of 13 domesticated and wild rice relatives highlight genetic conservation, turnover and innovation across the genus Oryza
Joshua C. SteinYeisoo YuDario CopettiDerrick J. ZwicklLi ZhangChengjun ZhangKapeel ChouguleDongying GaoAiko Iwata‐OtsuboJosé Luis GoicoecheaSharon WeiJun WangYi LiaoMuhua WangJulie JacqueminClaude BeckerDave KudrnaJianwei ZhangCarlos E. M. LondonoXiang SongSeunghee LeePaul L. SanchezAndrea ZuccoloJetty S. S. AmmirajuJayson TalagAnn DanowitzLuis F. RiveraAndrea R. GschwendChristos NoutsosCheng‐Chieh WuShu-Min KaoJhih-wun ZengFu‐Jin WeiQiang ZhaoQi FengMoaïne El BaidouriMarie‐Christine CarpentierÉric LasserreRichard CookeDaniel da Rosa FariasLuciano Carlos da MaiaRailson Schreinert dos SantosKevin G. NybergMillicent D. Alexandrov SanciangcoRamil MauleonNickolai AlexandrovJeremy SchmutzDave FlowersChuanzhu FanDetlef WeigelKshirod K. JenaThomas WickerMingsheng ChenBin HanRobert J HenryYue-Ie HsingNori KurataAntônio Costa de OliveiraOlivier PanaudScott A. JacksonCarlos A. MachadoMichael J. SandersonManyuan LongDoreen WareRod A. Wing
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Abstract:
The genus Oryza is a model system for the study of molecular evolution over time scales ranging from a few thousand to 15 million years. Using 13 reference genomes spanning the Oryza species tree, we show that despite few large-scale chromosomal rearrangements rapid species diversification is mirrored by lineage-specific emergence and turnover of many novel elements, including transposons, and potential new coding and noncoding genes. Our study resolves controversial areas of the Oryza phylogeny, showing a complex history of introgression among different chromosomes in the young 'AA' subclade containing the two domesticated species. This study highlights the prevalence of functionally coupled disease resistance genes and identifies many new haplotypes of potential use for future crop protection. Finally, this study marks a milestone in modern rice research with the release of a complete long-read assembly of IR 8 'Miracle Rice', which relieved famine and drove the Green Revolution in Asia 50 years ago. Genome assemblies of 13 domesticated and wild rice relatives reveal salient features of genome evolution across the genus Oryza, especially rapid species diversification and turnover of transposons. This study also releases a complete long-read assembly of IR 8 'Miracle Rice'.Keywords:
Introgression
Oryza
Oryza rufipogon
The study of crop evolution has focused primarily on the process of initial domestication. Post-domestication adaptation during the expansion of crops from their centers of origin has received considerably less attention. Recent research has revealed that, in at least some instances, crops have received introgression from their wild relatives that has facilitated adaptation to novel conditions encountered during expansion. Such adaptive introgression could bear importantly on the basic study of domestication, affecting estimates of several evolutionary processes of interest ( e.g. , the strength of the domestication bottleneck, the timing of domestication, the targets of selection during domestication). Identification of haplotypes introgressed from the wild may also aid the identification of alleles that are beneficial under particular environmental conditions. Here we review mounting evidence for substantial adaptive wild introgression in several crops and consider the implications of such gene flow to our understanding of crop histories.
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Many excellent genes in wild rice have been lost during the domestication of wild rice to cultivated rice. In this study, introgression lines (ILs) were produced with a wild rice (Oryza rufipogon) accession, BJ194, as a donor parent and an indica restorer line, Zhonghui 8015 (ZH8015), as a recipient parent to map QTLs for plant height. We identified four QTLs (qPH3.1, qPH3.2, qPH2, and qPH8) related to plant height distributed on chromosomes 2, 3 and 8. Furthermore, we sequenced and analyzed qPH3.2 located in the interval of RM15753–RM3525, and found this QTL may be a new locus regulating rice plant height.
Oryza rufipogon
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Oryza
Rice plant
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Summary The study of crop evolution has focused primarily on the process of initial domestication. Post‐domestication adaptation during the expansion of crops from their centers of origin has received considerably less attention. Recent research has revealed that, in at least some instances, crops have received introgression from their wild relatives that has facilitated adaptation to novel conditions encountered during expansion. Such adaptive introgression could have an important impact on the basic study of domestication, affecting estimates of several evolutionary processes of interest (e.g. the strength of the domestication bottleneck, the timing of domestication, the targets of selection during domestication). Identification of haplotypes introgressed from the wild may also help in the identification of alleles that are beneficial under particular environmental conditions. Here we review mounting evidence for substantial adaptive wild introgression in several crops and consider the implications of such gene flow to our understanding of crop histories.
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Iron (Fe) is an essential micronutrient that is frequently inaccessible to plants. Rice (Oryza sativa L.) plants employ the Combined Strategy for Fe uptake, which is composed by all features of Strategy II, common to all Poaceae species, and some features of Strategy I, common to non-Poaceae species. To understand the evolution of Fe uptake mechanisms, we analyzed the root transcriptomic response to Fe deficiency in O. sativa and its wild progenitor O. rufipogon. We identified 622 and 2,017 differentially expressed genes in O. sativa and O. rufipogon, respectively. Among the genes up-regulated in both species, we found Fe transporters associated with Strategy I, such as IRT1, IRT2 and NRAMP1; and genes associated with Strategy II, such as YSL15 and IRO2. In order to evaluate the conservation of these Strategies among other Poaceae, we identified the orthologs of these genes in nine species from the Oryza genus, maize and sorghum, and evaluated their expression profile in response to low Fe condition. Our results indicate that the Combined Strategy is not specific to O. sativa as previously proposed, but also present in species of the Oryza genus closely related to domesticated rice, and originated around the same time the AA genome lineage within Oryza diversified. Therefore, adaptation to Fe2+ acquisition via IRT1 in flooded soils precedes O. sativa domestication.
Oryza rufipogon
Oryza
Genetic algorithm
Lineage (genetic)
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The study of crop evolution has focused primarily on the process of initial domestication. Post-domestication adaptation during the expansion of crops from their centers of origin has received considerably less attention. Recent research has revealed that, in at least some instances, crops have received introgression from their wild relatives that has facilitated adaptation to novel conditions encountered during expansion. Such adaptive introgression could bear importantly on the basic study of domestication, affecting estimates of several evolutionary processes of interest ( e.g. , the strength of the domestication bottleneck, the timing of domestication, the targets of selection during domestication). Identification of haplotypes introgressed from the wild may also aid the identification of alleles that are beneficial under particular environmental conditions. Here we review mounting evidence for substantial adaptive wild introgression in several crops and consider the implications of such gene flow to our understanding of crop histories.
Introgression
Identification
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Modern cultivated rice (Oryza sativa) typically experiences limited growth benefits from arbuscular mycorrhizal (AM) symbiosis. This could be due to the long-term domestication of rice under favorable phosphorus conditions. However, there is limited understanding of whether and how the rice domestication has modified AM properties. This study compared AM properties between a collection of wild (Oryza rufipogon) and domesticated rice genotypes and investigated the mechanisms underlying their differences by analyzing physiological, genomic, transcriptomic, and metabolomic traits critical for AM symbiosis. The results revealed significantly lower mycorrhizal growth responses and colonization intensity in domesticated rice compared to wild rice, and this change of AM properties may be associated with the domestication modifications of plant phosphorus utilization efficiency at physiological and genomic levels. Domestication also resulted in a decrease in the activity of the mycorrhizal phosphorus acquisition pathway, which may be attributed to reduced mycorrhizal compatibility of rice roots by enhancing defense responses like root lignification and reducing carbon supply to AM fungi. In conclusion, rice domestication may have changed its AM properties by modifying P nutrition-related traits and reducing symbiotic compatibility. This study offers new insights for improving AM properties in future rice breeding programs to enhance sustainable agricultural production.
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Oryza
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ABSTRACT Grapevine ( Vitis vinifera L.) is one of the most significant crops in the world. Today’s richness in grapevine diversity results from a complex domestication history over multiple historical periods. Here, we employed whole genome resequencing to elucidate different aspects of the recent evolutionary history of this crop. Our results support a model in which a central domestication event in grapevine was followed by post-domestication hybridization with local wild genotypes, leading to the presence of an introgression signature in modern wine varieties across Western Europe. The strongest signal was associated with a subset of Iberian grapevine varieties, which show large introgression tracts. We targeted this study group for further analysis, demonstrating how regions under selection in wild populations from the Iberian Peninsula were preferentially passed on to the cultivated varieties by geneflow. Examination of underlying genes suggests that environmental adaptation played a fundamental role in both the evolution of wild genotypes and the outcome of hybridization with cultivated varieties, supporting a case of adaptive introgression in grapevine.
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Abstract The domestication and subsequent development of sheep are crucial events in the history of human civilization and the agricultural revolution. However, the impact of interspecific introgression on the genomic regions under domestication and subsequent selection remains unclear. Here, we analyze the whole genomes of domestic sheep and all their wild relative species. We found introgression from wild sheep such as the snow sheep and its American relatives (bighorn and thinhorn sheep) into urial, Asiatic and European mouflons. We observed independent events of adaptive introgression from wild sheep into the Asiatic and European mouflons, as well as shared introgressed regions from both snow sheep and argali into Asiatic mouflon before or during the domestication process. We revealed European mouflons arose through hybridization events between a now extinct sheep in Europe and feral domesticated sheep around 6,000 – 5,000 years BP. We also unveiled later introgressions from wild sheep to their sympatric domestic sheep after domestication. Several of the introgression events contain loci with candidate domestication genes (e.g., PAPPA2 , NR6A1 , SH3GL3 , RFX3 and CAMK4 ), associated with morphological, immune, reproduction or production traits (wool/meat/milk). We also detected introgression events that introduced genes related to nervous response ( NEURL1 ), neurogenesis ( PRUNE2 ), hearing ability ( USH2A ) and placental viability ( PAG11 and PAG3 ) to domestic sheep and their ancestral wild species from other wild species.
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All red rice found in commercial rice in the United States has traditionally been classified as Oryza sativa ssp. indica. This assumption was tested by analyzing red rice samples collected from across the southern United States rice belt with 18 simple sequence length polymorphism (SSLP) markers distributed across all 12 chromosomes. The results clearly demonstrate that the traditional classification of red rice is inadequate. Some red rice is closely related to O. sativa ssp. indica cultivated rice. However, other red rice is more closely related to O. sativa ssp. japonica. Most importantly, some red rice samples collected from Arkansas, Louisiana, Mississippi, and Texas form a distinct group that includes a number of Oryza nivara and Oryza rufipogon accessions from the National Small Grains Center. In particular, red rice samples from three states were identified that for all 18 markers are identical to the O. rufipogon accession IRGC 105491. These different classes of red rice are intermingled across the southern U.S. rice belt and within individual production fields. Oryza sativa ssp. indica-like red rice and O. rufipogon-like red rice have been found within a single 9-m2 collection site. While the classification of red rice as O. sativa ssp. indica, O. sativa ssp. japonica, or O. rufipogon using DNA markers is generally in agreement with classification based on simple morphological traits, readily observed morphological traits alone are not sufficient to reliably classify red rice. Because red rice is much more diverse than previously assumed, this diversity must be considered when developing red rice management strategies.
Oryza rufipogon
Red rice
Oryza
Weedy rice
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