Adaptation to climate through flowering phenology: a case study in Medicago truncatula

Local climatic conditions likely constitute an important selective pressure on genes underlying important fitness‐related traits such as flowering time, and in many species, flowering phenology and climatic gradients strongly covary. To test whether climate shapes the genetic variation on flowering time genes and to identify candidate flowering genes involved in the adaptation to environmental heterogeneity, we used a large Medicago truncatula core collection to examine the association between nucleotide polymorphisms at 224 candidate genes and both climate variables and flowering phenotypes. Unlike genome‐wide studies, candidate gene approaches are expected to enrich for the number of meaningful trait associations because they specifically target genes that are known to affect the trait of interest. We found that flowering time mediates adaptation to climatic conditions mainly by variation at genes located upstream in the flowering pathways, close to the environmental stimuli. Variables related to the annual precipitation regime reflected selective constraints on flowering time genes better than the other variables tested (temperature, altitude, latitude or longitude). By comparing phenotype and climate associations, we identified 12 flowering genes as the most promising candidates responsible for phenological adaptation to climate. Four of these genes were located in the known flowering time QTL region on chromosome 7. However, climate and flowering associations also highlighted largely distinct gene sets, suggesting different genetic architectures for adaptation to climate and flowering onset.     

Nucleotide diversity of vernalization and flowering‐time‐related genes in a germplasm collection of meadow fescue (Festuca pratensis Huds. syn. Lolium pratense (Huds.) Darbysh.)

In plant species, control of flowering time is an important factor for adaptation to local natural environments. The Vrn1, CO, FT1 and CK2α genes are key components in the flowering‐specific signaling pathway of grass species. Meadow fescue is an agronomically important forage grass species, which is naturally distributed across Europe and Western Asia. In this study, meadow fescue flowering‐time‐related genes were resequenced to assess nucleotide diversity in European and Western Asian subpopulations. Identified sequence polymorphisms were then converted into PCR‐based molecular genetic markers, and a meadow fescue germplasm collection was genotyped to investigate global allelic variation. Lower nucleotide diversities were observed for the Vrn1 and CO orthologs, while relatively higher values were observed for the FT1 and casein kinase II α‐subunit (CK2α) orthologs. The nucleotide diversity for FT1 orthologs in the Western Asian subpopulation was significantly higher than those of the European subpopulation. Similarly, significant differences in nucleotide diversity for the remaining genes were observed between several combinations of subpopulation. The global allele distribution pattern was consistent with observed level of nucleotide diversity. These results suggested that the degree of purifying selection acting on the genes differs according to geographical location. As previously shown for model plant species, functional specificities of flowering‐time‐related genes may also vary according to environmental conditions.     

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.     

Genomic signatures of adaptation to Sahelian and Soudanian climates in sorghum landraces of Senegal

Uncovering the genomic basis of climate adaptation in traditional crop varieties can provide insight into plant evolution and facilitate breeding for climate resilience. In the African cereal sorghum (Sorghum bicolor L. [Moench]), the genomic basis of adaptation to the semiarid Sahelian zone versus the subhumid Soudanian zone is largely unknown. To address this issue, we characterized a large panel of 421 georeferenced sorghum landrace accessions from Senegal and adjacent locations at 213,916 single‐nucleotide polymorphisms (SNPs) using genotyping‐by‐sequencing. Seven subpopulations distributed along the north‐south precipitation gradient were identified. Redundancy analysis found that climate variables explained up to 8% of SNP variation, with climate collinear with space explaining most of this variation (6%). Genome scans of nucleotide diversity suggest positive selection on chromosome 2, 4, 5, 7, and 10 in durra sorghums, with successive adaptation during diffusion along the Sahel. Putative selective sweeps were identified, several of which colocalize with stay‐green drought tolerance (Stg) loci, and a priori candidate genes for photoperiodic flowering and inflorescence morphology. Genome‐wide association studies of photoperiod sensitivity and panicle compactness identified 35 and 13 associations that colocalize with a priori candidate genes, respectively. Climate‐associated SNPs colocalize with Stg3a, Stg1, Stg2, and Ma6 and have allelic distribution consistent with adaptation across Sahelian and Soudanian zones. Taken together, the findings suggest an oligogenic basis of adaptation to Sahelian versus Soudanian climates, underpinned by variation in conserved floral regulatory pathways and other systems that are less understood in cereals.     

The genetic architecture of freezing tolerance varies across the range of Arabidopsis thaliana

The capacity to tolerate freezing temperatures limits the geographical distribution of many plants, including several species of agricultural importance. However, the genes involved in freezing tolerance remain largely unknown. Here, we describe the variation in constitutive freezing tolerance that occurs among worldwide accessions of Arabidopsis thaliana. We found that although plants from high latitudes tend to be more freezing tolerant than plants from low latitudes, the environmental factors that shape cold adaptation differ across the species range. Consistent with this, we found that the genetic architecture of freezing tolerance also differs across its range. Conventional genome‐wide association studies helped identify a priori and other promising candidate genes. However, simultaneously modelling climate variables and freezing tolerance together pinpointed other excellent a priori candidate genes. This suggests that if the selective factor underlying phenotypic variation is known, multi‐trait mixed models may aid in identifying the genes that underlie adaptation.     

Identification of loci controlling adaptation in Chinese soya bean landraces via a combination of conventional and bioclimatic GWAS

Landraces often contain genetic diversity that has been lost in modern cultivars, including alleles that confer enhanced local adaptation. To comprehensively identify loci associated with adaptive traits in soya bean landraces, for example flowering time, a population of 1938 diverse landraces and 97 accessions of the wild progenitor of cultivated soya bean, Glycine soja was genotyped using tGBS^®. Based on 99 085 high‐quality SNPs, landraces were classified into three sub‐populations which exhibit geographical genetic differentiation. Clustering was inferred from STRUCTURE, principal component analyses and neighbour‐joining tree analyses. Using phenotypic data collected at two locations separated by 10 degrees of latitude, 17 trait‐associated SNPs (TASs) for flowering time were identified, including a stable locus Chr12:5914898 and previously undetected candidate QTL/genes for flowering time in the vicinity of the previously cloned flowering genes, E1 and E2. Using passport data associated with the collection sites of the landraces, 27 SNPs associated with adaptation to three bioclimatic variables (temperature, daylength, and precipitation) were identified. A series of candidate flowering genes were detected within linkage disequilibrium (LD) blocks surrounding 12 bioclimatic TASs. Nine of these TASs exhibit significant differences in flowering time between alleles within one or more of the three individual sub‐populations. Signals of selection during domestication and/or subsequent landrace diversification and adaptation were detected at 38 of the 44 flowering and bioclimatic TASs. Hence, this study lays the groundwork to begin breeding for novel environments predicted to arise following global climate change.     

Lineage‐specific adaptation to climate involves flowering time in North American Arabidopsis lyrata

Adaptation to local climatic conditions is commonly found within species, but whether it involves the same intraspecific genomic variants is unknown. We studied this question in North American Arabidopsis lyrata, whose current distribution is shaped by post‐glacial range expansion from two refugia, resulting in two distinct genetic clusters covering comparable climatic gradients. Using pooled whole‐genome sequence data of 41 outcrossing populations, we identified loci associated with three niche‐determining climatic variables in the two clusters and compared these outliers. Little evidence was found for parallelism in climate adaptation for single nucleotide polymorphisms (SNPs) and for genes with an accumulation of outlier SNPs. Significantly increased selection coefficients supported them as candidates of climate adaptation. However, the fraction of gene ontology (GO) terms shared between clusters was higher compared to outlier SNPs and outlier genes, suggesting that selection acts on similar pathways but not necessarily the same genes. Enriched GO terms involved responses to abiotic and biotic stress, circadian rhythm and development, with flower development and reproduction being among the most frequently detected. In line with GO enrichment, regulators of flowering time were detected as outlier genes. Our results suggest that while adaptation to environmental gradients on the genomic level are lineage‐specific in A. lyrata, similar biological processes seem to be involved. Differential loss of standing genetic variation, probably driven by genetic drift, can in part account for the lack of parallel evolution on the genomic level.     

Dissection of the genetic architecture of three seed‐quality traits and consequences for breeding in Brassica napus

Genome‐wide association studies (GWASs) combining high‐throughput genome resequencing and phenotyping can accelerate the dissection of genetic architecture and identification of genes for plant complex traits. In this study, we developed a rapeseed genomic variation map consisting of 4 542 011 SNPs and 628 666 INDELs. GWAS was performed for three seed‐quality traits, including erucic acid content (EAC), glucosinolate content (GSC) and seed oil content (SOC) using 3.82 million polymorphisms in an association panel. Six, 49 and 17 loci were detected to be associated with EAC, GSC and SOC in multiple environments, respectively. The mean total contribution of these loci in each environment was 94.1% for EAC and 87.9% for GSC, notably higher than that for SOC (40.1%). A high correlation was observed between phenotypic variance and number of favourable alleles for associated loci, which will contribute to breeding improvement by pyramiding these loci. Furthermore, candidate genes were detected underlying associated loci, based on functional polymorphisms in gene regions where sequence variation was found to correlate with phenotypic variation. Our approach was validated by detection of well‐characterized FAE1 genes at each of two major loci for EAC on chromosomes A8 and C3, along with MYB28 genes at each of three major loci for GSC on chromosomes A9, C2 and C9. Four novel candidate genes were detected by correlation between GSC and SOC and observed sequence variation, respectively. This study provides insights into the genetic architecture of three seed‐quality traits, which would be useful for genetic improvement of B. napus.     

Coherent synthesis of genomic associations with phenotypes and home environments

Local adaptation is often studied via (i) multiple common garden experiments comparing performance of genotypes in different environments and (ii) sequencing genotypes from multiple locations and characterizing geographic patterns in allele frequency. Both approaches aim to characterize the same pattern (local adaptation), yet the complementary information from each has not yet been coherently integrated. Here, we develop a genome‐wide association model of genotype interactions with continuous environmental gradients (G × E), that is reaction norms. We present an approach to impute relative fitness, allowing us to coherently synthesize evidence from common garden and genome–environment associations. Our approach identifies loci exhibiting environmental clines where alleles are associated with higher fitness in home environments. Simulations show our approach can increase power to detect loci causing local adaptation. In a case study on Arabidopsis thaliana, most identified SNPs exhibited home allele advantage and fitness trade‐offs along climate gradients, suggesting selective gradients can maintain allelic clines. SNPs exhibiting G × E associations with fitness were enriched in genic regions, putative partial selective sweeps and associations with an adaptive phenotype (flowering time plasticity). We discuss extensions for situations where only adaptive phenotypes other than fitness are available. Many types of data may point towards the loci underlying G × E and local adaptation; coherent models of diverse data provide a principled basis for synthesis.     

Limber pine (Pinus flexilis James) genetic map constructed by exome‐seq provides insight into the evolution of disease resistance and a genomic resource for genomics‐based breeding

Limber pine ( Pinus flexilis ) is a keystone species of high‐elevation forest ecosystems of western North America, but some parts of the geographic range have high infection and mortality from the non‐native white pine blister rust caused by Cronartium ribicola . Genetic maps can provide essential knowledge for understanding genetic disease resistance as well as local adaptation to changing climates. Exome‐seq was performed to construct high‐density genetic maps in two seed families. Composite maps positioned 9612 unigenes across 12 linkage groups ( LG s). Syntenic analysis of genome structure revealed that the majority of orthologs were positional orthologous genes ( POG s) with localization on homologous LG s among conifer species. Gene ontology ( GO) enrichment analysis showed relatively fewer constraints for POG s with putative roles in adaptation to environments and relatively more conservation for POG s with roles in basic cell function and maintenance. The mapped genes included 639 nucleotide‐binding site leucine‐rich repeat genes ( NBS ‐ LRR s) , 290 receptor‐like protein kinase genes ( RLK s), and 1014 genes with potential roles in the defense response and induced systemic resistance to attack by pathogens. Orthologous loci for resistance to rust pathogens were identified and were co‐positioned with multiple members of the R gene family, revealing the evolutionary pressure acting upon them. This high‐density genetic map provides a genomic resource and practical tool for breeding and genetic conservation programs, with applications in genome‐wide association studies ( GWASs ), the characterization of functional genes underlying complex traits, and the sequencing and assembly of the full‐length genomes of limber pine and related Pinus species.     

Genome‐wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola

Optimum flowering time is the key to maximize canola production in order to meet global demand of vegetable oil, biodiesel and canola‐meal. We reveal extensive variation in flowering time across diverse genotypes of canola under field, glasshouse and controlled environmental conditions. We conduct a genome‐wide association study and identify 69 single nucleotide polymorphism (SNP) markers associated with flowering time, which are repeatedly detected across experiments. Several associated SNPs occur in clusters across the canola genome; seven of them were detected within 20 Kb regions of a priori candidate genes; FLOWERING LOCUS T, FRUITFUL, FLOWERING LOCUS C, CONSTANS, FRIGIDA, PHYTOCHROME B and an additional five SNPs were localized within 14 Kb of a previously identified quantitative trait loci for flowering time. Expression analyses showed that among FLC paralogs, BnFLC.A2 accounts for ~23% of natural variation in diverse accessions. Genome‐wide association analysis for FLC expression levels mapped not only BnFLC.C2 but also other loci that contribute to variation in FLC expression. In addition to revealing the complex genetic architecture of flowering time variation, we demonstrate that the identified SNPs can be modelled to predict flowering time in diverse canola germplasm accurately and hence are suitable for genomic selection of adaptative traits in canola improvement programmes.     

Landscape genomics and a common garden trial reveal adaptive differentiation to temperature across Europe in the tree species Alnus glutinosa

The adaptive potential of tree species to cope with climate change has important ecological and economic implications. Many temperate tree species experience a wide range of environmental conditions, suggesting high adaptability to new environmental conditions. We investigated adaptation to regional climate in the drought‐sensitive tree species Alnus glutinosa (Black alder), using a complementary approach that integrates genomic, phenotypic and landscape data. A total of 24 European populations were studied in a common garden and through landscape genomic approaches. Genotyping‐by‐sequencing was used to identify SNPs across the genome, resulting in 1990 SNPs. Although a relatively low percentage of putative adaptive SNPs was detected (2.86% outlier SNPs), we observed clear associations among outlier allele frequencies, temperature and plant traits. In line with the typical drought avoiding nature of A. glutinosa, leaf size varied according to a temperature gradient and significant associations with multiple outlier loci were observed, corroborating the ecological relevance of the observed outlier SNPs. Moreover, the lack of isolation by distance, the very low genetic differentiation among populations and the high intrapopulation genetic variation all support the notion that high gene exchange combined with strong environmental selection promotes adaptation to environmental cues.     

Flowering time QTL in natural populations of Arabidopsis thaliana and implications for their adaptive value

The genetic basis of phenotypic traits is of great interest to evolutionary biologists, but their contribution to adaptation in nature is often unknown. To determine the genetic architecture of flowering time in ecologically relevant conditions, we used a recombinant inbred line population created from two locally adapted populations of Arabidopsis thaliana from Sweden and Italy. Using these RILs, we identified flowering time QTL in growth chambers that mimicked the natural temperature and photoperiod variation across the growing season in each native environment. We also compared the genomic locations of flowering time QTL to those of fitness (total fruit number) QTL from a previous three‐year field study. Ten total flowering time QTL were found, and in all cases, the Italy genotype caused early flowering regardless of the conditions. Two QTL were consistent across chamber environments, and these had the largest effects on flowering time. Five of the fitness QTL colocalized with flowering time QTL found in the Italy conditions, and in each case, the local genotype was favoured. In contrast, just two flowering time QTL found in the Sweden conditions colocalized with fitness QTL and in only one case was the local genotype favoured. This implies that flowering time may be more important for adaptation in Italy than Sweden. Two candidate genes (FLC and VIN3) underlying the major flowering time QTL found in the current study are implicated in local adaptation.     

Mating system and environmental variation drive patterns of adaptation in Boechera spatifolia (Brassicaceae)

Determining the relative contribution of population genetic processes to the distribution of natural variation is a major goal of evolutionary biology. Here, we take advantage of variation in mating system to test the hypothesis that local adaptation is constrained by asexual reproduction. We explored patterns of variation in ecological traits and genome‐wide molecular markers in Boechera spatifolia (Brassicaceae), a species that contains both apomictic (asexual) and sexual individuals. Using a combination of quantitative genetics, neutral genetic (SSR) and genome‐wide single nucleotide polymorphism, we assessed the hypothesis that asexual lineages should have reduced signatures of adaptation relative to sexual conspecifics. All three measures (traits, SSRs, SNPs) demonstrated that apomicts are genetically distinct from sexuals, regardless of population location. Additionally, phylogenetic clustering revealed that the apomictic group shared a single common ancestor. Across the landscape, sexual genome‐wide SNP variation was strongly associated with latitude (r² > 0.9), indicating that sexual populations have differentiated across an environmental gradient. Furthermore, flowering time and growth rate, as assessed in a common garden, strongly covary with the elevation and latitude of the source population. Despite a wide geographic distribution that largely overlaps with sexual populations, there was little evidence for differentiation in molecular markers or quantitative characters among apomictic populations. Combined, these data indicated that, in contrast to asexual populations, sexual populations show evidence of local adaptation.     

Genomic analyses reveal the genetic basis of early maturity and identification of loci and candidate genes in upland cotton (Gossypium hirsutum L.)

Although upland cotton (Gossypium hirsutism L.) originated in the tropics, this early maturity cotton can be planted as far north as 46°N in China due to the accumulation of numerous phenotypic and physiological adaptations during domestication. However, how the genome of early maturity cotton has been altered by strong human selection remains largely unknown. Herein, we report a cotton genome variation map generated by the resequencing of 436 cotton accessions. Whole‐genome scans for sweep regions identified 357 putative selection sweeps covering 4.94% (112 Mb) of the upland cotton genome, including 5184 genes. These genes were functionally related to flowering time control, hormone catabolism, ageing and defence response adaptations to environmental changes. A genome‐wide association study (GWAS) for seven early maturity traits identified 307 significant loci, 22.48% (69) of which overlapped with putative selection sweeps that occurred during the artificial selection of early maturity cotton. Several previously undescribed candidate genes associated with early maturity were identified by GWAS. This study provides insights into the genetic basis of early maturity in upland cotton as well as breeding resources for cotton improvement.     

Will phenotypic plasticity affecting flowering phenology keep pace with climate change?

Rising temperatures have begun to shift flowering time, but it is unclear whether phenotypic plasticity can accommodate projected temperature change for this century. Evaluating clines in phenological traits and the extent and variation in plasticity can provide key information on assessing risk of maladaptation and developing strategies to mitigate climate change. In this study, flower phenology was examined in 52 populations of big sagebrush (Artemisia tridentata) growing in three common gardens. Flowering date (anthesis) varied 91 days from late July to late November among gardens. Mixed‐effects modeling explained 79% of variation in flowering date, of which 46% could be assigned to plasticity and genetic variation in plasticity and 33% to genetics (conditional R² = 0.79, marginal R² = 0.33). Two environmental variables that explained the genetic variation were photoperiod and the onset of spring, the Julian date of accumulating degree‐days >5 °C reaching 100. The genetic variation was mapped for contemporary and future climates (decades 2060 and 2090), showing flower date change varies considerably across the landscape. Plasticity was estimated to accommodate, on average, a ±13‐day change in flowering date. However, the examination of genetic variation in plasticity suggests that the magnitude of plasticity could be affected by variation in the sensitivity to photoperiod and temperature. In a warmer common garden, lower‐latitude populations have greater plasticity (+16 days) compared to higher‐latitude populations (+10 days). Mapped climatypes of flowering date for contemporary and future climates illustrate the wide breadth of plasticity and large geographic overlap. Our research highlights the importance of integrating information on genetic variation, phenotypic plasticity and climatic niche modeling to evaluate plant responses and elucidate vulnerabilities to climate change.     

Rapid genome‐wide evolution in Brassica rapa populations following drought revealed by sequencing of ancestral and descendant gene pools

There is increasing evidence that evolution can occur rapidly in response to selection. Recent advances in sequencing suggest the possibility of documenting genetic changes as they occur in populations, thus uncovering the genetic basis of evolution, particularly if samples are available from both before and after selection. Here, we had a unique opportunity to directly assess genetic changes in natural populations following an evolutionary response to a fluctuation in climate. We analysed genome‐wide differences between ancestors and descendants of natural populations of Brassica rapa plants from two locations that rapidly evolved changes in multiple phenotypic traits, including flowering time, following a multiyear late‐season drought in California. These ancestor‐descendant comparisons revealed evolutionary shifts in allele frequencies in many genes. Some genes showing evolutionary shifts have functions related to drought stress and flowering time, consistent with an adaptive response to selection. Loci differentiated between ancestors and descendants (F_ST outliers) were generally different from those showing signatures of selection based on site frequency spectrum analysis (Tajima's D), indicating that the loci that evolved in response to the recent drought and those under historical selection were generally distinct. Very few genes showed similar evolutionary responses between two geographically distinct populations, suggesting independent genetic trajectories of evolution yielding parallel phenotypic changes. The results show that selection can result in rapid genome‐wide evolutionary shifts in allele frequencies in natural populations, and highlight the usefulness of combining resurrection experiments in natural populations with genomics for studying the genetic basis of adaptive evolution.     

Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping

To identify the ecological and genetic mechanisms of local adaptation requires estimating selection on traits, identifying their genetic basis, and evaluating whether divergence in adaptive traits is due to conditional neutrality or genetic trade‐offs. To this end, we conducted field experiments for three years using recombinant inbred lines (RILs) derived from two ecotypes of Arabidopsis thaliana (Italy, Sweden), and at each parental site examined selection on flowering time and mapped quantitative trait loci (QTL). There was strong selection for early flowering in Italy, but weak selection in Sweden. Eleven distinct flowering time QTL were detected, and for each the Italian genotype caused earlier flowering. Twenty‐seven candidate genes were identified, two of which (FLC and VIN3) appear under major flowering time QTL in Italy. Seven of eight QTL in Italy with narrow credible intervals colocalized with previously reported fitness QTL, in comparison to three of four in Sweden. The results demonstrate that the magnitude of selection on flowering time differs strikingly between our study populations, that the genetic basis of flowering time variation is multigenic with some QTL of large effect, and suggest that divergence in flowering time between ecotypes is due mainly to conditional neutrality.     

Genomic adaptation of flowering‐time genes during the expansion of rice cultivation area

The diversification of flowering time in response to natural environments is critical for the spread of crops to diverse geographic regions. In contrast with recent advances in understanding the molecular basis of photoperiodic flowering in rice (Oryza sativa), little is known about how flowering‐time diversification is structured within rice subspecies. By analyzing genome sequencing data and a set of 429 chromosome segment substitution lines (CSSLs) originating from 10 diverse rice accessions with wide distributions, we revealed diverse effects of allelic variations for common flowering‐time quantitative trait loci in the recipient's background. Although functional variations associated with a few loci corresponded to standing variations among subspecies, the identified functional nucleotide polymorphisms occurred recently after rice subgroup differentiation, indicating that the functional diversity of flowering‐time gene sequences was not particularly associated with phylogenetic relationship between rice subspecies. Intensive analysis of the Hd1 genomic region identified the signature of an early introgression of the Hd1 with key mutation(s) in aus and temperate japonica accessions. Our data suggested that, after such key introgressions, new mutations were selected and accelerated the flowering‐time diversity within subspecies during the expansion of rice cultivation area. This finding may imply that new genome‐wide changes for flowering‐time adaptation are one of the critical determinants for establishing genomic architecture of local rice subgroups. In‐depth analyses of various rice genomes coupling with the genetically confirmed phenotypic changes in a large set of CSSLs enabled us to demonstrate how rice genome dynamics has coordinated with the adaptation of cultivated rice during the expansion of cultivation area.