Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome

Genetic architecture of flowering time in maize was addressed by synthesizing a total of 313 quantitative trait loci (QTL) available for this trait. These were analyzed first with an overview statistic that highlighted regions of key importance and then with a meta-analysis method that yielded a synthetic genetic model with 62 consensus QTL. Six of these displayed a major effect. Meta-analysis led in this case to a twofold increase in the precision in QTL position estimation, when compared to the most precise initial QTL position within the corresponding region. The 62 consensus QTL were compared first to the positions of the few flowering-time candidate genes that have been mapped in maize. We then projected rice candidate genes onto the maize genome using a synteny conservation approach based on comparative mapping between the maize genetic map and japonica rice physical map. This yielded 19 associations between maize QTL and genes involved in flowering time in rice and in Arabidopsis. Results suggest that the combination of meta-analysis within a species of interest and synteny-based projections from a related model plant can be an efficient strategy for identifying new candidate genes for trait variation.     

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.     

Supermodels: sorghum and maize provide mutual insight into the genetics of flowering time

Nested association mapping (NAM) offers power to dissect complex, quantitative traits. This study made use of a recently developed sorghum backcross (BC)-NAM population to dissect the genetic architecture of flowering time in sorghum; to compare the QTL identified with other genomic regions identified in previous sorghum and maize flowering time studies and to highlight the implications of our findings for plant breeding. A subset of the sorghum BC-NAM population consisting of over 1,300 individuals from 24 families was evaluated for flowering time across multiple environments. Two QTL analysis methodologies were used to identify 40 QTLs with predominately small, additive effects on flowering time; 24 of these co-located with previously identified QTL for flowering time in sorghum and 16 were novel in sorghum. Significant synteny was also detected with the QTL for flowering time detected in a comparable NAM resource recently developed for maize (Zea mays) by Buckler et al. (Science 325:714–718, 2009). The use of the sorghum BC-NAM population allowed us to catalogue allelic variants at a maximal number of QTL and understand their contribution to the flowering time phenotype and distribution across diverse germplasm. The successful demonstration of the power of the sorghum BC-NAM population is exemplified not only by correspondence of QTL previously identified in sorghum, but also by correspondence of QTL in different taxa, specifically maize in this case. The unification across taxa of the candidate genes influencing complex traits, such as flowering time can further facilitate the detailed dissection of the genetic control and causal genes.     

Detection of QTLs for flowering date in three mapping populations of the model legume species Medicago truncatula

Adaptation to the environment and reproduction are dependent on the date of flowering in the season. The objectives of this paper were to evaluate the effect of photoperiod on flowering date of the model species for legume crops, Medicago truncatula and to describe genetic architecture of this trait in multiple mapping populations. The effect of photoperiod (12 and 18 h) was analysed on eight lines. Quantitative variation in three recombinant inbred lines (RILs) populations involving four parental lines was evaluated, and QTL detection was carried out. Flowering occurred earlier in long than in short photoperiods. Modelling the rate of progression to flowering with temperature and photoperiod gave high R(2), with line-specific parameters that indicated differential responses of the lines to both photoperiod and temperature. QTL detection showed a QTL on chromosome 7 that was common to all populations and seasons. Taking advantage of the multiple mapping populations, it was condensed into a single QTL with a support interval of only 0.9 cM. In a bioanalysis, six candidate genes were identified in this interval. This design also indicated other genomic regions that were involved in flowering date variation more specifically in one population or one season. The analysis on three different mapping populations detected more QTLs than on a single population, revealed more alleles and gave a more precise position of the QTLs that were common to several populations and/or seasons. Identification of candidate genes was a result of integration of QTL analysis and genomics in M. truncatula.     

Transmission of important chromosomal regions under selection revealed in rice pedigree breeding programs

Genetic analysis across a whole plant genome based on pedigree information offers considerable potential for enhancing genetic gain from plant breeding programs through quantitative trait loci (QTL) mapping and marker-assisted selection. Here, we report its application for graphically genotyping varieties used in Chinese japonica rice (Oryza sativa L.) pedigree breeding programs. We identified 34 important chromosomal regions from the founder parent that are under selection in the breeding programs, and by comparing donor genomic regions that are under selection with QTL locations of agronomic traits, we found that QTL clustered in important genomic regions, in accordance with association analyses of natural populations and other previous studies. The convergence of genomic regions under selection with QTL locations suggests that donor genomic regions harboring key genes/QTL for important agronomic traits have been selected by plant breeders since the 1950s from the founder rice plants. The results provide better understanding of the effects of selection in breeding programs on the traits of rice cultivars. They also provide potentially valuable information for enhancing rice breeding programs through screening candidate parents for targeted molecular markers, improving crop yield potential and identifying suitable genetic material for use in future breeding programs.     

Detection of QTL for flowering time in multiple families of elite maize

Flowering time is a fundamental quantitative trait in maize that has played a key role in the postdomestication process and the adaptation to a wide range of climatic conditions. Flowering time has been intensively studied and recent QTL mapping results based on diverse founders suggest that the genetic architecture underlying this trait is mainly based on numerous small-effect QTL. Here, we used a population of 684 progenies from five connected families to investigate the genetic architecture of flowering time in elite maize. We used a joint analysis and identified nine main effect QTL explaining approximately 50?% of the genotypic variation of the trait. The QTL effects were small compared with the observed phenotypic variation and showed strong differences between families. We detected no epistasis with the genetic background but four digenic epistatic interactions in a full 2-dimensional genome scan. Our results suggest that flowering time in elite maize is mainly controlled by main effect QTL with rather small effects but that epistasis may also contribute to the genetic architecture of the trait.     

Identification of genetic variants associated with maize flowering time using an extremely large multi‐genetic background population

Flowering time is one of the major adaptive traits in domestication of maize and an important selection criterion in breeding. To detect more maize flowering time variants we evaluated flowering time traits using an extremely large multi‐ genetic background population that contained more than 8000 lines under multiple Sino‐United States environments. The population included two nested association mapping (NAM) panels and a natural association panel. Nearly 1 million single‐nucleotide polymorphisms (SNPs) were used in the analyses. Through the parallel linkage analysis of the two NAM panels, both common and unique flowering time regions were detected. Genome wide, a total of 90 flowering time regions were identified. One‐third of these regions were connected to traits associated with the environmental sensitivity of maize flowering time. The genome‐wide association study of the three panels identified nearly 1000 flowering time‐associated SNPs, mainly distributed around 220 candidate genes (within a distance of 1 Mb). Interestingly, two types of regions were significantly enriched for these associated SNPs – one was the candidate gene regions and the other was the approximately 5 kb regions away from the candidate genes. Moreover, the associated SNPs exhibited high accuracy for predicting flowering time.     

Quantitative trait locus analysis and construction of consensus genetic map for drought tolerance traits based on three recombinant inbred line populations in cultivated groundnut (Arachis hypogaea L.)

Groundnut (Arachis hypogaea L.) is an important food and cash crop grown mainly in semi-arid tropics (SAT) regions of the world where drought is the major constraint on productivity. With the aim of understanding the genetic basis and identification of quantitative trait loci (QTL) for drought tolerance, two new recombinant inbred line (RIL) mapping populations, namely ICGS 76?×?CSMG 84-1 (RIL-2) and ICGS 44?×?ICGS 76 (RIL-3), were used. After screening of 3,215 simple sequence repeat (SSR) markers on the parental genotypes of these populations, two new genetic maps were developed with 119 (RIL-2) and 82 (RIL-3) SSR loci. Together with these maps and the reference map with 191 SSR loci based on TAG 24?×?ICGV 86031 (RIL-1), a consensus map was constructed with 293 SSR loci distributed over 20 linkage groups, spanning 2,840.8?cM. As all these three populations segregate for drought-tolerance-related traits, a comprehensive QTL analysis identified 153 main effect QTL (M-QTL) and 25 epistatic QTL (E-QTL) for drought-tolerance-related traits. Localization of these QTL on the consensus map provided 16 genomic regions that contained 125 QTL. A few key genomic regions were selected on the basis of the QTL identified in each region, and their expected role in drought adaptation is also discussed. Given that no major QTL for drought adaptation were identified, novel breeding approaches such as marker-assisted recurrent selection (MARS) and genomic selection (GS) approaches are likely to be the preferred approaches for introgression of a larger number of QTL in order to breed drought-tolerant groundnut genotypes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s11032-011-9660-0) contains supplementary material, which is available to authorized users.     

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.     

Adaptation of Maize to Temperate Climates: Mid-Density Genome-Wide Association Genetics and Diversity Patterns Reveal Key Genomic Regions,with a Major Contribution of the Vgt2 (ZCN8) Locus

The migration of maize from tropical to temperate climates was accompanied by a dramatic evolution in flowering time. To gain insight into the genetic architecture of this adaptive trait, we conducted a 50K SNP-based genome-wide association and diversity investigation on a panel of tropical and temperate American and European representatives. Eighteen genomic regions were associated with flowering time. The number of early alleles cumulated along these regions was highly correlated with flowering time. Polymorphism in the vicinity of the ZCN8 gene, which is the closest maize homologue to Arabidopsis major flowering time (FT) gene, had the strongest effect. This polymorphism is in the vicinity of the causal factor of Vgt2 QTL. Diversity was lower, whereas differentiation and LD were higher for associated loci compared to the rest of the genome, which is consistent with selection acting on flowering time during maize migration. Selection tests also revealed supplementary loci that were highly differentiated among groups and not associated with flowering time in our panel, whereas they were in other linkage-based studies. This suggests that allele fixation led to a lack of statistical power when structure and relatedness were taken into account in a linear mixed model. Complementary designs and analysis methods are necessary to unravel the architecture of complex traits. Based on linkage disequilibrium (LD) estimates corrected for population structure, we concluded that the number of SNPs genotyped should be at least doubled to capture all QTLs contributing to the genetic architecture of polygenic traits in this panel. These results show that maize flowering time is controlled by numerous QTLs of small additive effect and that strong polygenic selection occurred under cool climatic conditions. They should contribute to more efficient genomic predictions of flowering time and facilitate the dissemination of diverse maize genetic resources under a wide range of environments.     

Identification of Quantitative Trait Loci Associated with Resistance to Viral Haemorrhagic Septicaemia (VHS) in Turbot (Scophthalmus maximus): A Comparison Between Bacterium,Parasite and Virus Diseases

One of the main objectives of genetic breeding programs in turbot industry is to reduce disease-related mortality. In the present study, a genome scan to detect quantitative trait loci (QTL) affecting resistance and survival to viral haemorrhagic septicaemia (VHS) was carried out. Three full-sib families with approximately 90 individuals each were genotyped and evaluated by linear regression and maximum likelihood approaches. In addition, a comparison between QTL detected for resistance and survival time to other important bacterial and parasite diseases affecting turbot (furunculosis and scuticociliatosis) was also carried out. Finally, the relationship between QTL affecting resistance/survival time to the virus and growth-related QTL was also evaluated. Several genomic regions controlling resistance and survival time to VHS were detected. Also significant associations between the evaluated traits and genotypes at particular markers were identified, explaining up to 14 % of the phenotypic variance. Several genomic regions controlling general and specific resistance to different diseases in turbot were detected. A preliminary gene mining approach identified candidate genes related to general or specific immunity. This information will be valuable to develop marker-assisted selection programs and to discover candidate genes related to disease resistance to improve turbot production.     

玉米叶形相关性状的Meta-QTL及候选基因分析

叶长、叶宽、叶面积及叶夹角不仅影响玉米(Zea mays)光合效率, 也是株型的重要构成因素。通过对620个叶形QTL进行整合, 构建不同遗传背景下的叶形QTL整合图谱, 利用元分析发掘出22个叶长、22个叶宽、12个叶面积以及17个叶夹角mQTL; 进一步运用生物信息学手段, 确定44个与叶片发育密切相关的候选基因。分析发现, 仅有NAL7-like、YABBY6- like和GRF2等13个基因位于mQTL区间内, 而玉米中已克隆的KNOTTED1、AN3/GIF1、rgd1/lbl1、mwp1及SRL2-like、HYL1-like和CYCB2;4-like等水稻(Oryza sativa)和拟南芥(Arabidopsis thaliana)叶形同源基因位于未被整合的QTL内; 对44个候选基因在叶片长、宽、厚发育过程中基部-末端、中央-边缘、远轴-近轴的调控机理进行归纳分析, 发现玉米中仅有少数几个候选基因被报道, 揭示了叶形发育的部分分子机理。因此, 对玉米叶形相关mQTL/QTL及基因进行全面深入的分析, 不仅有助于增加对其遗传结构的了解, 发掘更多候选基因, 阐明叶形发育和形成的分子机制, 还可为耐密理想株型的分子标记辅助选择提供依据。     

Mapping QTL associated with photoperiod sensitivity and assessing the importance of QTL×environment interaction for flowering time in maize

Background

An understanding of the genetic determinism of photoperiod response of flowering is a prerequisite for the successful exchange of germplasm across different latitudes. In order to contribute to resolve the genetic basis of photoperiod sensitivity in maize, a set of 201 recombinant inbred lines (RIL), derived from a temperate and tropical inbred line cross were evaluated in 5 field trials spread in short- and long-day environments.

Methodology/Principal Findings

Firstly, QTL analyses for flowering time and photoperiod sensitivity in maize were conducted in individual photoperiod environments separately, and then, the total genetic effect was partitioned into additive effect (A) and additive-by-environment interaction effect (AE) by using a mixed-model-based composite interval mapping (MCIM) method.

Conclusions/Significance

Seven putative QTL were found associated with DPS thermal time based on the data estimated in individual environments. Nine putative QTL were found associated with DPS thermal time across environments and six of them showed significant QTL×enviroment (QE) interactions. Three QTL for photoperiod sensitivity were identified on chromosome 4, 9 and 10, which had the similar position to QTL for DPS thermal time in the two long-day environment. The major photoperiod sensitive loci qDPS10 responded to both short and long-day photoperiod environments and had opposite effects in different photoperiod environment. The QTL qDPS3, which had the greatest additive effect exclusively in the short-day environment, were photoperiod independent and should be classified in autonomous promotion pathway.     

Genome-wide association study reveals the genetic architecture of flowering time in rapeseed (Brassica napus L.)

Flowering time adaptation is a major breeding goal in the allopolyploid species Brassica napus. To investigate the genetic architecture of flowering time, a genome-wide association study (GWAS) of flowering time was conducted with a diversity panel comprising 523 B. napus cultivars and inbred lines grown in eight different environments. Genotyping was performed with a Brassica 60K Illumina Infinium SNP array. A total of 41 single-nucleotide polymorphisms (SNPs) distributed on 14 chromosomes were found to be associated with flowering time, and 12 SNPs located in the confidence intervals of quantitative trait loci (QTL) identified in previous researches based on linkage analyses. Twenty-five candidate genes were orthologous to Arabidopsis thaliana flowering genes. To further our understanding of the genetic factors influencing flowering time in different environments, GWAS was performed on two derived traits, environment sensitivity and temperature sensitivity. The most significant SNPs were found near Bn-scaff_16362_1-p380982, just 13 kb away from BnaC09g41990D, which is orthologous to A. thaliana CONSTANS (CO), an important gene in the photoperiod flowering pathway. These results provide new insights into the genetic control of flowering time in B. napus and indicate that GWAS is an effective method by which to reveal natural variations of complex traits in B. napus.     

A gene regulatory network model for floral transition of the shoot apex in maize and its dynamic modeling

The transition from the vegetative to reproductive development is a critical event in the plant life cycle. The accurate prediction of flowering time in elite germplasm is important for decisions in maize breeding programs and best agronomic practices. The understanding of the genetic control of flowering time in maize has significantly advanced in the past decade. Through comparative genomics, mutant analysis, genetic analysis and QTL cloning, and transgenic approaches, more than 30 flowering time candidate genes in maize have been revealed and the relationships among these genes have been partially uncovered. Based on the knowledge of the flowering time candidate genes, a conceptual gene regulatory network model for the genetic control of flowering time in maize is proposed. To demonstrate the potential of the proposed gene regulatory network model, a first attempt was made to develop a dynamic gene network model to predict flowering time of maize genotypes varying for specific genes. The dynamic gene network model is composed of four genes and was built on the basis of gene expression dynamics of the two late flowering id1 and dlf1 mutants, the early flowering landrace Gaspe Flint and the temperate inbred B73. The model was evaluated against the phenotypic data of the id1 dlf1 double mutant and the ZMM4 overexpressed transgenic lines. The model provides a working example that leverages knowledge from model organisms for the utilization of maize genomic information to predict a whole plant trait phenotype, flowering time, of maize genotypes.     

Genetic and physical mapping of flowering time loci in canola (Brassica napus L.)

We identified quantitative trait loci (QTL) underlying variation for flowering time in a doubled haploid (DH) population of vernalisation—responsive canola (Brassica napus L.) cultivars Skipton and Ag-Spectrum and aligned them with physical map positions of predicted flowering genes from the Brassica rapa genome. Significant genetic variation in flowering time and response to vernalisation were observed among the DH lines from Skipton/Ag-Spectrum. A molecular linkage map was generated comprising 674 simple sequence repeat, sequence-related amplified polymorphism, sequence characterised amplified region, Diversity Array Technology, and candidate gene based markers loci. QTL analysis indicated that flowering time is a complex trait and is controlled by at least 20 loci, localised on ten different chromosomes. These loci each accounted for between 2.4 and 28.6 % of the total genotypic variation for first flowering and response to vernalisation. However, identification of consistent QTL was found to be dependant upon growing environments. We compared the locations of QTL with the physical positions of predicted flowering time genes located on the sequenced genome of B. rapa. Some QTL associated with flowering time on A02, A03, A07, and C06 may represent homologues of known flowering time genes in Arabidopsis; VERNALISATION INSENSITIVE 3, APETALA1, CAULIFLOWER, FLOWERING LOCUS C, FLOWERING LOCUS T, CURLY LEAF, SHORT VEGETATIVE PHASE, GA3 OXIDASE, and LEAFY. Identification of the chromosomal location and effect of the genes influencing flowering time may hasten the development of canola varieties having an optimal time for flowering in target environments such as for low rainfall areas, via marker-assisted selection.     

Most significant genome regions involved in the control of earliness traits in bread wheat, as revealed by QTL meta-analysis

Earliness is one of the most important adaptation traits in plant breeding. Our purpose was to identify the genome regions of bread wheat involved in the control of earliness and its three components: photoperiod sensitivity (PS), vernalization requirement (VR) and intrinsic earliness (IE). A QTL meta-analysis was carried out to examine the replicability of QTL across 13 independent studies and to propose meta-QTL (MQTL). Initial QTL were projected on a recent consensus map (2004). Quality criteria were proposed to assess the reliability of this projection. These criteria were based on the distances between markers in the QTL regions. Chromosomes of groups 2 and 5 had a greater incidence on earliness control as they carry the known, major genes Ppd and Vrn. Other chromosome regions played an intermediate role in earliness control: 4A [heading date (HD) Meta-QTL], 4B (HD MQTL), 2B (VR MQTL) and 5B (IE MQTL). Markers at this four MQTL should prove helpful in marker-assisted selection, to better control earliness.     

Genetic dissection of tocopherol content and composition in maize grain using quantitative trait loci analysis and the candidate gene approach

Tocopherols are essential micronutrients for humans and animals, with several beneficial effects in plants. Among cereals, only maize grains contain high concentrations of tocopherols. In this investigation we analyzed, during 2004 and 2005, by high-performance liquid chromatography (HPLC), a population of 233 recombinant inbred lines (RIL) which were derived from two diverse parents and had extremely variable tocopherol content and composition. A genetic map was constructed using 208 polymorphic molecular markers including gene-targeted markers based on six candidate genes of the tocopherol biosynthesis pathway (HPPD, VTE1, VTE3, VTE4, P3VTE5, and P4VTE5). Thirty-one quantitative trait loci (QTL) associated with quantitative variation of tocopherol content and composition were identified by composite interval mapping (CIM); these were located on sixteen genomic regions covering all the chromosomes except chromosome 4. Most (65%) QTL were co-located, suggesting that in some cases the same QTL predominantly affected the amounts of more than one tocopherol. Two candidate genes, HPPD and VTE4 showed co-localization with major QTL for tocopherol content and composition whereas only one interval (umc1075–umc1304) on chromosome eight exhibited a QTL for α, δ, γ, and total tocopherols with high LOD and PVE values. The candidate genes associated with tocopherol content and with composition, especially VTE4 and HPPD, could be precisely used for alteration of the tocopherol content and composition of maize grains by development of functional markers. Other identified major QTL especially those on chromosomes 8, 1, and 2 (near candidate gene VTE5) can also be used for improvement of maize grain quality by marker-assisted selection.