Quantitative trait locus mapping reveals complex genetic architecture of quantitative virulence in the wheat pathogen Zymoseptoria tritici

We conducted a comprehensive analysis of virulence in the fungal wheat pathogen Zymoseptoria tritici using quantitative trait locus (QTL) mapping. High‐throughput phenotyping based on automated image analysis allowed the measurement of pathogen virulence on a scale and with a precision that was not previously possible. Across two mapping populations encompassing more than 520 progeny, 540 710 pycnidia were counted and their sizes and grey values were measured. A significant correlation was found between pycnidia size and both spore size and number. Precise measurements of percentage leaf area covered by lesions provided a quantitative measure of host damage. Combining these large and accurate phenotypic datasets with a dense panel of restriction site‐associated DNA sequencing (RADseq) genetic markers enabled us to genetically dissect pathogen virulence into components related to host damage and those related to pathogen reproduction. We showed that different components of virulence can be under separate genetic control. Large‐ and small‐effect QTLs were identified for all traits, with some QTLs specific to mapping populations, cultivars and traits and other QTLs shared among traits within the same mapping population. We associated the presence of four accessory chromosomes with small, but significant, increases in several virulence traits, providing the first evidence for a meaningful function associated with accessory chromosomes in this organism. A large‐effect QTL involved in host specialization was identified on chromosome 7, leading to the identification of candidate genes having a large effect on virulence.     

Natural variation in the genetic architecture of a host-parasite interaction in the bumblebee Bombus terrestris

The genetic architecture of fitness-relevant traits in natural populations is a topic that has remained almost untouched by quantitative genetics. Given the importance of parasitism for the host's fitness, we used QTL mapping to study the genetic architecture of traits relevant for host-parasite interactions in the trypanosome parasite, Crithidia bombi and its host, Bombus terrestris. The three traits analysed were the parasite's infection intensity, the strength of the general immune response (measured as the encapsulation of a novel antigen) and body size. The genetic architecture of these traits was examined in three natural, unmanipulated mapping populations of B. terrestris. Our results indicate that the intracolonial phenotypic variation of all three traits is based on a network of QTLs and epistatic interactions. While these networks are similar between mapping populations in complexity and number of QTLs, as well as in their epistatic interactions, the variability in the position of QTL and the interacting loci was high. Only one QTL for body size was plausibly found in at least two populations. QTLs for encapsulation and Crithidia infection intensity were located on the same linkage groups.     

Identification and fine mapping of quantitative trait loci for the number of vascular bundle in maize stem

Studies that investigated the genetic basis of source and sink related traits have been widely conducted. However, the vascular system that links source and sink received much less attention. When maize was domesticated from its wild ancestor, teosinte, the external morphology has changed dramatically; however, less is known for the internal anatomy changes. In this study, using a large maize‐teosinte experimental population, we performed a high‐resolution quantitative trait locus (QTL) mapping for the number of vascular bundle in the uppermost internode of maize stem. The results showed that vascular bundle number is dominated by a large number of small‐effect QTLs, in which a total of 16 QTLs that jointly accounts for 52.2% of phenotypic variation were detected, with no single QTL explaining more than 6% of variation. Different from QTLs for typical domestication traits, QTLs for vascular bundle number might not be under directional selection following domestication. Using Near Isogenic Lines (NILs) developed from heterogeneous inbred family (HIF), we further validated the effect of one QTL qVb9‐2 on chromosome 9 and fine mapped the QTL to a 1.8‐Mb physical region. This study provides important insights for the genetic architecture of vascular bundle number in maize stem and sets basis for cloning of qVb9‐2.     

Genotypic variation in Norway spruce correlates to fungal communities in vegetative buds

The taxonomically diverse phyllosphere fungi inhabit leaves of plants. Thus, apart from the fungi's dispersal capacities and environmental factors, the assembly of the phyllosphere community associated with a given host plant depends on factors encoded by the host's genome. The host genetic factors and their influence on the assembly of phyllosphere communities under natural conditions are poorly understood, especially in trees. Recent work indicates that Norway spruce (Picea abies) vegetative buds harbour active fungal communities, but these are hitherto largely uncharacterized. This study combines internal transcribed spacer sequencing of the fungal communities associated with dormant vegetative buds with a genome‐wide association study (GWAS) in 478 unrelated Norway spruce trees. The aim was to detect host loci associated with variation in the fungal communities across the population, and to identify loci correlating with the presence of specific, latent, pathogens. The fungal communities were dominated by known Norway spruce phyllosphere endophytes and pathogens. We identified six quantitative trait loci (QTLs) associated with the relative abundance of the dominating taxa (i.e., top 1% most abundant taxa). Three additional QTLs associated with colonization by the spruce needle cast pathogen Lirula macrospora or the cherry spruce rust (Thekopsora areolata) in asymptomatic tissues were detected. The identification of the nine QTLs shows that the genetic variation in Norway spruce influences the fungal community in dormant buds and that mechanisms underlying the assembly of the communities and the colonization of latent pathogens in trees may be uncovered by combining molecular identification of fungi with GWAS.     

Complexities in the genetic dissection of quantitative trait loci

The analysis of complex traits, including those involved in many common diseases, has encountered significant difficulties, and, despite major efforts during the past decade, has had little success. Current advances in genomics, however, promise to change this. Recently, Steinmetz et al. used a new technique to produce the first complete quantitative trait locus (QTL) analysis of a complex trait from phenotype to gene to be published entirely in a single report. This marks a significant advance over previous QTL analyses, which took several years. The work exemplifies some of the complexities of QTL mapping and demonstrates a novel method to resolve the underlying genetic architecture of QTLs in yeast. Here we discuss this work in the general context of genetic dissection of complex traits and QTLs.     

Natural variation for carbohydrate content in Arabidopsis. Interaction with complex traits dissected by quantitative genetics

Besides being a metabolic fuel, carbohydrates play important roles in plant growth and development, in stress responses, and as signal molecules. We exploited natural variation in Arabidopsis (Arabidopsis thaliana) to decipher the genetic architecture determining carbohydrate content. A quantitative trait locus (QTL) approach in the Bay-0 x Shahdara progeny grown in two contrasting nitrogen environments led to the identification of 39 QTLs for starch, glucose, fructose, and sucrose contents representing at least 14 distinct polymorphic loci. A major QTL for fructose content (FR3.4) and a QTL for starch content (ST3.4) were confirmed in heterogeneous inbred families. Several genes associated with carbon (C) metabolism colocalize with the identified QTL. QTLs for senescence-related traits, and for flowering time, water status, and nitrogen-related traits, previously detected with the same genetic material, colocalize with C-related QTLs. These colocalizations reflect the complex interactions of C metabolism with other physiological processes. QTL fine-mapping and cloning could thus lead soon to the identification of genes potentially involved in the control of different connected physiological processes.     

QTL mapping for sexually dimorphic fitness-related traits in wild bighorn sheep

Dissecting the genetic architecture of fitness-related traits in wild populations is key to understanding evolution and the mechanisms maintaining adaptive genetic variation. We took advantage of a recently developed genetic linkage map and phenotypic information from wild pedigreed individuals from Ram Mountain, Alberta, Canada, to study the genetic architecture of ecologically important traits (horn volume, length, base circumference and body mass) in bighorn sheep. In addition to estimating sex-specific and cross-sex quantitative genetic parameters, we tested for the presence of quantitative trait loci (QTLs), colocalization of QTLs between bighorn sheep and domestic sheep, and sex × QTL interactions. All traits showed significant additive genetic variance and genetic correlations tended to be positive. Linkage analysis based on 241 microsatellite loci typed in 310 pedigreed animals resulted in no significant and five suggestive QTLs (four for horn dimension on chromosomes 1, 18 and 23, and one for body mass on chromosome 26) using genome-wide significance thresholds (Logarithm of odds (LOD) >3.31 and >1.88, respectively). We also confirmed the presence of a horn dimension QTL in bighorn sheep at the only position known to contain a similar QTL in domestic sheep (on chromosome 10 near the horns locus; nominal P<0.01) and highlighted a number of regions potentially containing weight-related QTLs in both species. As expected for sexually dimorphic traits involved in male-male combat, loci with sex-specific effects were detected. This study lays the foundation for future work on adaptive genetic variation and the evolutionary dynamics of sexually dimorphic traits in bighorn sheep.     

Genomic architecture of habitat‐related divergence and signature of directional selection in the body shapes of Gnathopogon fishes

Evolution of ecomorphologically relevant traits such as body shapes is important to colonize and persist in a novel environment. Habitat‐related adaptive divergence of these traits is therefore common among animals. We studied the genomic architecture of habitat‐related divergence in the body shape of Gnathopogon fishes, a novel example of lake–stream ecomorphological divergence, and tested for the action of directional selection on body shape differentiation. Compared to stream‐dwelling Gnathopogon elongatus, the sister species Gnathopogon caerulescens, exclusively inhabiting a large ancient lake, had an elongated body, increased proportion of the caudal region and small head, which would be advantageous in the limnetic environment. Using an F₂ interspecific cross between the two Gnathopogon species (195 individuals), quantitative trait locus (QTL) analysis with geometric morphometric quantification of body shape and restriction‐site associated DNA sequencing‐derived markers (1622 loci) identified 26 significant QTLs associated with the interspecific differences of body shape‐related traits. These QTLs had small to moderate effects, supporting polygenic inheritance of the body shape‐related traits. Each QTL was mostly located on different genomic regions, while colocalized QTLs were detected for some ecomorphologically relevant traits that are proxy of body and caudal peduncle depths, suggesting different degree of modularity among traits. The directions of the body shape QTLs were mostly consistent with the interspecific difference, and QTL sign test suggested a genetic signature of directional selection in the body shape divergence. Thus, we successfully elucidated the genomic architecture underlying the adaptive changes of the quantitative and complex morphological trait in a novel system.     

Two reproductive traits show contrasting genetic architectures in Plantago lanceolata

In many species, temperature‐sensitive phenotypic plasticity (i.e., an individual's phenotypic response to temperature) displays a positive correlation with latitude, a pattern presumed to reflect local adaptation. This geographical pattern raises two general questions: (a) Do a few large‐effect genes contribute to latitudinal variation in a trait? (b) Is the thermal plasticity of different traits regulated pleiotropically? To address the questions, we crossed individuals of Plantago lanceolata derived from northern and southern European populations. Individuals naturally exhibited high and low thermal plasticity in floral reflectance and flowering time. We grew parents and offspring in controlled cool‐ and warm‐temperature environments, mimicking what plants would encounter in nature. We obtained genetic markers via genotype‐by‐sequencing, produced the first recombination map for this ecologically important nonmodel species, and performed quantitative trait locus (QTL) mapping of thermal plasticity and single‐environment values for both traits. We identified a large‐effect QTL that largely explained the reflectance plasticity differences between northern and southern populations. We identified multiple smaller‐effect QTLs affecting aspects of flowering time, one of which affected flowering time plasticity. The results indicate that the genetic architecture of thermal plasticity in flowering is more complex than for reflectance. One flowering time QTL showed strong cytonuclear interactions under cool temperatures. Reflectance and flowering plasticity QTLs did not colocalize, suggesting little pleiotropic genetic control and freedom for independent trait evolution. Such genetic information about the architecture of plasticity is environmentally important because it informs us about the potential for plasticity to offset negative effects of climate change.     

Quantitative trait loci affecting amylose,amylopectin and starch content in maize recombinant inbred lines

The loci explaining the variability of quantitative traits related to starch content and composition (amylose, amylopectin and water soluble fraction) were searched for in maize kernels. Multifactorial genetic methods were used to detect and locate QTLs (quantitative trait loci) on a genetic map consisting mainly of RFLP markers for genes with known function. The genetic material was recombinant inbred lines originating from parents differing in starch structure (dent vs. flint). Kernels were harvested from field grown plants for two successive years and under two pollination systems. Main effect and epistasis QTLs were detected using two methods, composite interval mapping (MQTL) and ANOVA. Despite large year-to-year differences, physiologically meaningful co-locations were observed between trait QTLs. Moreover, the number of expressed sequences on our map allowed the search for co-locations between QTLs and genes involved in carbohydrate metabolism. The main co-location was between an amylose QTL and Shrunken 2 (SH2) locus, on chromosome 3 (SH2 encoding for the large subunit of ADPglucose pyrophosphorylase). The importance of this locus as a candidate gene for a starch QTL is in agreement with previous studies based either on QTL co-locations or on revertant analysis. Other co-locations were observed between amylose and amylopectin QTLs and the two loci of IVR1 invertase genes on chromosomes 2 and 10. Further comparison with previously detected QTLs for carbohydrate metabolism in maize leaves showed consistent co-location in map regions devoid of candidate genes, such as near chromosome 1S telomere. The possible contribution of regulatory genes in this region is discussed.     

QTL analysis of intraspecific differences between two Silene vulgaris ecotypes

BACKGROUND AND AIMS: Serpentine soils provide a highly selective substrate for plant colonization and growth and represent an ideal system for studying the evolution of plant-ecotypes. In the present study the aim was to identify the genetic architecture of morphological traits distinguishing serpentine and non-serpentine ecotypes of Silene vulgaris. METHODS: Using an F(2) mapping population derived from an intraspecific cross between a serpentine and a non-serpentine ecotype of S. vulgaris, the genetic architecture of 12 morphological traits was explored using a quantitative trait locus (QTL) analysis. KEY RESULTS: The QTL analysis identified a total of 49 QTLs, of which 24 were classified as major QTLs. The mean number of QTLs per trait category was found to correspond well with numbers reported in the literature for similar crosses. Clustering of QTLs for different traits was found on several linkage groups. CONCLUSIONS: Morphological traits that differentiate the two ecotypes are strongly correlated, presumably as a consequence of the joint effects of extensive linkage of QTLs for different traits and directional selection. The signature of consistent directional selection was found for leaf and shoot trait divergence. Intraspecific ecotype differences in S. vulgaris were found to be distributed across the entire genome. The study shows that QTL analyses on non-model organisms can provide novel insights into the genetic basis of plant diversification.     

A unified DNA sequence and non‐DNA sequence mapping model of complex traits

Increasing evidence shows that quantitative inheritance is based on both DNA sequence and non‐DNA sequence variants. However, how to simultaneously detect these variants from a mapping study has been unexplored, hampering our effort to illustrate the detailed genetic architecture of complex traits. We address this issue by developing a unified model of quantitative trait locus (QTL) mapping based on an open‐pollinated design composed of randomly sampling maternal plants from a natural population and their half‐sib seeds. This design forms a two‐level hierarchical platform for a joint linkage‐linkage disequilibrium analysis of population structure. The EM algorithm was implemented to estimate and test DNA sequence‐based effects and non‐DNA sequence‐based effects of QTLs. We applied this model to analyze genetic mapping data from the OP design of a gymnosperm coniferous species, Torreya grandis, identifying 25 significant DNA sequence and non‐DNA sequence QTLs for seedling height and diameter growth in different years. Results from computer simulation show that the unified model has good statistical properties and is powerful for QTL detection. Our model enables the tests of how a complex trait is affected differently by DNA‐based effects and non‐DNA sequence‐based transgenerational effects, thus allowing a more comprehensive picture of genetic architecture to be charted and quantified.     

Quantitative trait loci for morphometric traits in multiple families of common carp(Cyprinus carpio)

Quantitative trait locus(QTL) mapping is frequently used to understand the genetic architecture of quantitative traits.Herein,we performed a genome scanfor QTL affecting the morphometric characters in eight full-sib families containing 522 individuals using different statistical methods(Sib-pair and half-sib model).A total of 194 QTLs were detected in 25 different regions on 10 linkage groups(LGs).Among them,37 QTLs on five LGs(eight,13,24,40 and 45) were significant(5%genome-wide level),while the remaining 40(1%chromosome-wide level) and 117(5%chromosome-wide level) indicated suggestive effect on those traits.Heritabilities for most morphometric traits were moderate to high,ranging from 0.21 to 0.66,with generally strong phenotypic and genetic correlations between the traits.A large number of QTLs for morphometric traits were co-located,consistent with their high correlations,and may reflect pleiotropic effect on the same genes.Biological pathways were mapped for possible candidate genes on QTL regions.One significantly enriched pathway was identified onLG45,which had a P-value of 0.04 and corresponded to the "regulation of actin cytoskeleton pathway".The results are expected to be useful in marker-assisted selection(MAS) and provide valuable information for the study of gene pathway for morphometric and growth traits of the common carp.     

亚麻主要农艺与品质相关性状的QTL定位

为了全面了解亚麻产量和品质相关性状的遗传基础,为亚麻基因克隆和分子标记辅助育种提供理论依据,在已构建SNP连锁遗传图谱的基础上,以LH-89为父本,R43为母本构建F2:3家系QTL定位群体,用R/QTL软件采用复合区间作图法对13个农艺和品质性状进行QTL定位。结果表明:(1)该研究共检测出35个QTL位点,与粗脂肪及其组成成分相关的QTL有20个,与农艺性状相关的QTL有15个;其中:亚油酸和粗脂肪各5个,亚麻酸、千粒重各4个,棕榈酸、株高、工艺长度各3个,硬脂酸、分枝数各2个,单株果数、果粒数、单株粒重、油酸各1个。(2)共有18个QTL的表型贡献率超10%(主效基因),其中农艺性状定位8个主效基因,品质性状定位10个主效基因。     

The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.     

Bayesian robust analysis for genetic architecture of quantitative traits

MOTIVATION: In most quantitative trait locus (QTL) mapping studies, phenotypes are assumed to follow normal distributions. Deviations from this assumption may affect the accuracy of QTL detection and lead to detection of spurious QTLs. To improve the robustness of QTL mapping methods, we replaced the normal distribution for residuals in multiple interacting QTL models with the normal/independent distributions that are a class of symmetric and long-tailed distributions and are able to accommodate residual outliers. Subsequently, we developed a Bayesian robust analysis strategy for dissecting genetic architecture of quantitative traits and for mapping genome-wide interacting QTLs in line crosses. RESULTS: Through computer simulations, we showed that our strategy had a similar power for QTL detection compared with traditional methods assuming normal-distributed traits, but had a substantially increased power for non-normal phenotypes. When this strategy was applied to a group of traits associated with physical/chemical characteristics and quality in rice, more main and epistatic QTLs were detected than traditional Bayesian model analyses under the normal assumption.     

Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris

Serpentine soils provide a difficult substrate for plant colonization and growth and therefore represent an ideal system for studying the genetics of habitat adaptation and the evolution of plant-ecotypes. Using an F2 mapping population derived from an intraspecific cross between a serpentine and a nonserpentine ecotype of Silene vulgaris, the genetic architecture of seven morphological, physiological and life-history traits was explored. A quantitative trait locus (QTL) analysis identified 23 QTLs, 15 of which were classified as major QTLs. The observed genetic architecture suggests that traits potentially involved in habitat adaptation are controlled by few genes of major effect and have evolved under consistent directional selection. Several linkage groups harboured overlapping QTLs for different traits, which can be due to either pleiotropy or linkage. The potential roles of these factors and of the time available for habitat adaptation and ecological speciation on serpentine are discussed.     

A genetic analysis of seed and berry weight in grapevine.

Fruit size and seedlessness are highly relevant traits in many fruit crop species, and both are primary targets of breeding programs for table grapes. In this work we performed a quantitative genetic analysis of size and seedlessness in an F1 segregating population derived from the cross between a classical seeded (Vitis vinifera L. 'Dominga') and a newly bred seedless ('Autumn Seedless') cultivar. Fruit size was scored as berry weight (BW), and for seedlessness we considered both seed fresh weight (SFW) and the number of seeds and seed traces (SN) per berry. Quantitative trait loci (QTL) analysis of BW detected 3 QTLs affecting this trait and accounting for up to 67% of the total phenotypic variance. QTL analysis for seedlessness detected 3 QTLs affecting SN (explaining up to 35% of total variance) and 6 affecting SFW (explaining up to 90% of total variance). Among them, a major effect QTL explained almost half of the phenotypic variation for SFW. Comparative analysis of QTLs for these traits reduced the number of grapevine genomic regions involved, one of them being a major effect QTL for seedlessness. Association analyses showed that microsatellite locus VMC7F2, closely linked to this QTL, is a useful marker for selection of seedlessnes.     

Genetic bases of appearance quality of rice grains in Shanyou 63, an elite rice hybrid

Appearance quality of the rice grain represents a major problem of rice production in many rice-producing areas of the world, especially in hybrid rice production in China. In this study, we conducted a molecular marker-based genetic analysis of the traits that are determinants of the appearance quality of rice grains, including traits specifying grain shape and endosperm opacity. The materials used in the analysis included an F_2:3 population and an F₁₀ recombinant inbred line population from a cross between the parents of Shanyou 63, the most widely grown rice hybrid in China. Molecular marker-based QTL (quantitative trait locus) analyses revealed that grain length and grain width were each controlled by a major QTL accounting for a very large proportion of the genetic variation, plus one or two minor QTLs each explaining a small proportion of the genetic variation. The major QTLs can be detected in both the F_2:3 and recombinant inbred line population using both paddy rice and brown rice, whereas the minor QTLs were detected only occasionally. The QTL located in the interval of RG393-C1087 on chromosome 3 is the major locus for grain length, and the one in the interval RG360-C734a on chromosome 5 plays a major role in determining grain width. Similarly, white belly, which largely determines the opacity of the endosperm, is almost entirely controlled by a major locus on chromosome 5, located in the same genomic region as the major QTL for grain width. The implications of the results with respect to hybrid rice improvement were discussed. Received: 20 February 2000 / Accepted: 21 March 2000