Leaf shape evolution has a similar genetic architecture in three edaphic specialists within the Mimulus guttatus species complex

Background and Aims The genetic basis of leaf shape has long interested botanists because leaf shape varies extensively across the plant kingdom and this variation is probably adaptive. However, knowledge of the genetic architecture of leaf shape variation in natural populations remains limited. This study examined the genetic architecture of leaf shape diversification among three edaphic specialists in the Mimulus guttatus species complex. Lobed and narrow leaves have evolved from the entire, round leaves of M. guttatus in M. laciniatus, M. nudatus and a polymorphic serpentine M. guttatus population (M2L).Methods Bulk segregant analysis and next-generation sequencing were used to map quantitative trait loci (QTLs) that underlie leaf shape in an M. laciniatus × M. guttatus F₂ population. To determine whether the same QTLs contribute to leaf shape variation in M. nudatus and M2L, F₂s from M. guttatus × M. nudatus and lobed M2L × unlobed M. guttatus crosses were genotyped at QTLs from the bulk segregant analysis.Key Results Narrow and lobed leaf shapes in M. laciniatus, M. nudatus and M. guttatus are controlled by overlapping genetic regions. Several promising leaf shape candidate genes were found under each QTL.Conclusions The evolution of divergent leaf shape has taken place multiple times in the M. guttatus species complex and is associated with the occupation of dry, rocky environments. The genetic architecture of elongated and lobed leaves is similar across three species in this group. This may indicate that parallel genetic evolution from standing variation or new mutations is responsible for the putatively adaptive leaf shape variation in Mimulus.     

Comparative linkage maps suggest that fission,not polyploidy,underlies near-doubling of chromosome number within monkeyflowers (Mimulus; Phrymaceae)

Changes in chromosome number and structure are important contributors to adaptation, speciation and macroevolution. In flowering plants, polyploidy and subsequent reductions in chromosome number by fusion are major sources of chromosomal evolution, but chromosome number increase by fission has been relatively unexplored. Here, we use comparative linkage mapping with gene-based markers to reconstruct chromosomal synteny within the model flowering plant genus Mimulus (monkeyflowers). Two sections of the genus with haploid numbers ⩾14 have been inferred to be relatively recent polyploids because they are phylogenetically nested within numerous taxa with low base numbers (n=8–10). We combined multiple data sets to build integrated genetic maps of the M. guttatus species complex (section Simiolus, n=14) and the M. lewisii group (section Erythranthe; n=8), and then aligned the two integrated maps using >100 shared markers. We observed strong segmental synteny between M. lewisii and M. guttatus maps, with essentially 1-to-1 correspondence across each of 16 chromosomal blocks. Assuming that the M. lewisii (and widespread) base number of 8 is ancestral, reconstruction of 14 M. guttatus chromosomes requires at least eight fission events (likely shared by Simiolus and sister section Paradanthus (n=16)), plus two fusion events. This apparent burst of fission in the yellow monkeyflower lineages raises new questions about mechanisms and consequences of chromosomal fission in plants. Our comparative maps also provide insight into the origins of a chromosome exhibiting centromere-associated female meiotic drive and create a framework for transferring M. guttatus genome resources across the entire genus.     

A General Modeling Framework for Genome Ancestral Origins in Multiparental Populations

The next generation of QTL (quantitative trait loci) mapping populations have been designed with multiple founders, where one to a number of generations of intercrossing are introduced prior to the inbreeding phase to increase accumulated recombinations and thus mapping resolution. Examples of such populations are Collaborative Cross (CC) in mice and Multiparent Advanced Generation Inter-Cross (MAGIC) lines in Arabidopsis. The genomes of the produced inbred lines are fine-grained random mosaics of the founder genomes. In this article, we present a novel framework for modeling ancestral origin processes along two homologous autosomal chromosomes from mapping populations, which is a major component in the reconstruction of the ancestral origins of each line for QTL mapping. We construct a general continuous time Markov model for ancestral origin processes, where the rate matrix is deduced from the expected densities of various types of junctions (recombination breakpoints). The model can be applied to monoecious populations with or without self-fertilizations and to dioecious populations with two separate sexes. The analytic expressions for map expansions and expected junction densities are obtained for mapping populations that have stage-wise constant mating schemes, such as CC and MAGIC. Our studies on the breeding design of MAGIC populations show that the intercross mating schemes do not matter much for large population size and that the overall expected junction density, and thus map resolution, are approximately proportional to the inverse of the number of founders.     

Genetic mapping of two components of reproductive isolation between two sibling species of moths,Ostrinia nubilalis and O. scapulalis

We report the quantitative trait loci (QTL) mapping of reproductive isolation traits between Ostrinia nubilalis (the European corn borer) and its sibling species O. scapulalis (the Adzuki bean borer), focusing on two traits: mating isolation (mi) and pheromone production (Pher). Four genetic maps were generated from two backcross families, with two maps (one chromosomal map and one linkage map) per backcross. We located 165–323 AFLP markers on these four maps, resulting in the identification of 27–31 linkage groups, depending on the map considered. No-choice mating experiments with the offspring of each backcross led to the detection of at least two QTLs for mi in different linkage groups. QTLs underlying Pher were located in a third linkage group. The Z heterochromosome was identified by a specific marker (Tpi) and did not carry any of these QTLs. Finally, we considered the global divergence between the two sibling species, distortions of segregation throughout the genome, and the location and effect of mi and Pher QTLs in light of the known candidate genes for reproductive isolation within the genus Ostrinia and, more broadly, in phytophagous insects.     

Evidence of Natural Selection Acting on a Polymorphic Hybrid Incompatibility Locus in Mimulus

As a common cause of reproductive isolation in diverse taxa, hybrid incompatibilities are fundamentally important to speciation. A key question is which evolutionary forces drive the initial substitutions within species that lead to hybrid dysfunction. Previously, we discovered a simple genetic incompatibility that causes nearly complete male sterility and partial female sterility in hybrids between the two closely related yellow monkeyflower species Mimulus guttatus and M. nasutus. In this report, we fine map the two major incompatibility loci—hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2)—to small nuclear genomic regions (each <70 kb) that include strong candidate genes. With this improved genetic resolution, we also investigate the evolutionary dynamics of hms1 in a natural population of M. guttatus known to be polymorphic at this locus. Using classical genetic crosses and population genomics, we show that a 320-kb region containing the hms1 incompatibility allele has risen to intermediate frequency in this population by strong natural selection. This finding provides direct evidence that natural selection within plant species can lead to hybrid dysfunction between species.     

Construction of a high-density genetic map based on large-scale markers developed by specific length amplified fragment sequencing (SLAF-seq) and its application to QTL analysis for isoflavone content in Glycine max

Background

Quantitative trait locus (QTL) mapping is an efficient approach to discover the genetic architecture underlying complex quantitative traits. However, the low density of molecular markers in genetic maps has limited the efficiency and accuracy of QTL mapping. In this study, specific length amplified fragment sequencing (SLAF-seq), a new high-throughput strategy for large-scale SNP discovery and genotyping based on next generation sequencing (NGS), was employed to construct a high-density soybean genetic map using recombinant inbred lines (RILs, Luheidou2 × Nanhuizao, F_5:8). With this map, the consistent QTLs for isoflavone content across various environments were identified.

Results

In total, 23 Gb of data containing 87,604,858 pair-end reads were obtained. The average coverage for each SLAF marker was 11.20-fold for the female parent, 12.51-fold for the male parent, and an average of 3.98-fold for individual RILs. Among the 116,216 high-quality SLAFs obtained, 9,948 were polymorphic. The final map consisted of 5,785 SLAFs on 20 linkage groups (LGs) and spanned 2,255.18 cM in genome size with an average distance of 0.43 cM between adjacent markers. Comparative genomic analysis revealed a relatively high collinearity of 20 LGs with the soybean reference genome. Based on this map, 41 QTLs were identified that contributed to the isoflavone content. The high efficiency and accuracy of this map were evidenced by the discovery of genes encoding isoflavone biosynthetic enzymes within these loci. Moreover, 11 of these 41 QTLs (including six novel loci) were associated with isoflavone content across multiple environments. One of them, qIF20-2, contributed to a majority of isoflavone components across various environments and explained a high amount of phenotypic variance (8.7% - 35.3%). This represents a novel major QTL underlying isoflavone content across various environments in soybean.

Conclusions

Herein, we reported a high-density genetic map for soybean. This map exhibited high resolution and accuracy. It will facilitate the identification of genes and QTLs underlying essential agronomic traits in soybean. The novel major QTL for isoflavone content is useful not only for further study on the genetic basis of isoflavone accumulation, but also for marker-assisted selection (MAS) in soybean breeding in the future.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-1086) contains supplementary material, which is available to authorized users.     

Identification of Novel QTLs for Isolate-Specific Partial Resistance to Plasmodiophora brassicae in Brassica rapa

Plasmodiophora brassicae, the causal agent of clubroot disease of the Brassica crops, is widespread in the world. Quantitative trait loci (QTLs) for partial resistance to 4 different isolates of P. brassicae (Pb2, Pb4, Pb7, and Pb10) were investigated using a BC₁F₁ population from a cross between two subspecies of Brassica rapa, i.e. Chinese cabbage inbred line C59-1 as a susceptible recurrent parent and turnip inbred line ECD04 as a resistant donor parent. The BC₁F₂ families were assessed for resistance under controlled conditions. A linkage map constructed with simple sequence repeats (SSR), unigene-derived microsatellite (UGMS) markers, and specific markers linked to published clubroot resistance (CR) genes of B. rapa was used to perform QTL mapping. A total of 6 QTLs residing in 5 CR QTL regions of the B. rapa chromosomes A01, A03, and A08 were identified to account for 12.2 to 35.2% of the phenotypic variance. Two QTL regions were found to be novel except for 3 QTLs in the respective regions of previously identified Crr1, Crr2, and Crr3. QTL mapping results indicated that 1 QTL region was common for partial resistance to the 2 isolates of Pb2 and Pb7, whereas the others were specific for each isolate. Additionally, synteny analysis between B. rapa and Arabidopsis thaliana revealed that all CR QTL regions were aligned to a single conserved crucifer blocks (U, F, and R) on 3 Arabidopsis chromosomes where 2 CR QTLs were detected in A. thaliana. These results suggest that some common ancestral genomic regions were involved in the evolution of CR genes in B. rapa.     

Genetic mapping of biomass yield in three interconnected Miscanthus populations

Improving biomass yield is a major goal of Miscanthus breeding. We conducted a study on one interspecific Miscanthus sinensis × Miscanthus sacchariflorus F₁ population and two intraspecific M. sinensis F₁ populations, each of which shared a common parent. A field trial was established at Urbana, IL during spring 2011, and phenotypic data were collected in 2012 and 2013 for fourteen yield traits. Six high‐density parental genetic maps, as well as a consensus genetic map integrating M. sinensis and M. sacchariflorus, were developed via the pseudotestcross strategy for noninbred parents with ≥1214 single‐nucleotide polymorphism markers generated from restriction site‐associated DNA sequencing. We confirmed for the first time a whole‐genome duplication in M. sacchariflorus relative to Sorghum bicolor, similar to that observed previously for M. sinensis. Four quantitative trait locus (QTL) analysis methods for detecting marker‐trait associations were compared: (1) individual parental map composite interval mapping analysis, (2) individual parental map stepwise analysis, (3) consensus map single‐population stepwise analysis and (4) consensus map joint‐population stepwise analysis. These four methods detected 288, 264, 133 and 109 total QTLs, which resolved into 157, 136, 106 and 86 meta‐QTLs based on QTL congruency, respectively, including a set of 59 meta‐QTLs common to all four analysis methods. Composite interval mapping and stepwise analysis co‐identified 118 meta‐QTLs across six parental maps, suggesting high reliability of stepwise regression in QTL detection. Joint‐population stepwise analysis yielded the highest resolution of QTLs compared to the other three methods across all meta‐QTLs. Strong, frequently advantageous transgressive segregation in the three populations indicated a promising future for breeding new higher‐yielding cultivars of Miscanthus.     

Epistasis Is a Major Determinant of the Additive Genetic Variance in Mimulus guttatus

The influence of genetic interactions (epistasis) on the genetic variance of quantitative traits is a major unresolved problem relevant to medical, agricultural, and evolutionary genetics. The additive genetic component is typically a high proportion of the total genetic variance in quantitative traits, despite that underlying genes must interact to determine phenotype. This study estimates direct and interaction effects for 11 pairs of Quantitative Trait Loci (QTLs) affecting floral traits within a single population of Mimulus guttatus. With estimates of all 9 genotypes for each QTL pair, we are able to map from QTL effects to variance components as a function of population allele frequencies, and thus predict changes in variance components as allele frequencies change. This mapping requires an analytical framework that properly accounts for bias introduced by estimation errors. We find that even with abundant interactions between QTLs, most of the genetic variance is likely to be additive. However, the strong dependency of allelic average effects on genetic background implies that epistasis is a major determinant of the additive genetic variance, and thus, the population’s ability to respond to selection.     

QTL analysis of heterostyly in Primula sieboldii and its application for morph identification in wild populations

Background and Aims

Primula sieboldii is a perennial clonal herb that is distributed around the Sea of Japan and is endangered in Japan. Its breeding system is characterized by heteromorphic self-incompatibility, and the morph ratio within a population is very important for reproductive success. The aims of this study were to construct a linkage map, map the S locus as a qualitative trait and quantitative trait loci (QTLs) for floral morphological traits related to heterostyly, and predict the morph type in wild populations by using molecular markers for devising a conservation strategy.

Methods

A linkage map was constructed with 126 markers. The QTLs for four floral traits and the S locus were mapped. Using the genotypes of loci that were located near both the S locus and the QTLs with large effects, morphs of 59 wild genets were predicted.

Key Results

The linkage map consisted of 14 linkage groups (LGs). The S locus was mapped to LG 7. Major QTLs for stigma and anther heights were detected in the same region as the S locus. These QTLs exhibited high logarithm of the odds scores and explained a high percentage of the phenotypic variance (>85 %). By analysing these two traits within each morph, additional QTLs for each trait were detected. Using the four loci linked to the S locus, the morphs of 43 genets in three wild populations could be predicted.

Conclusions

This is the first report of a linkage map and QTL analysis for floral morphology related to heterostyly in P. sieboldii. Floral morphologies related to heterostyly are controlled by the S locus in LG 7 and by several QTLs in other LGs. Additionally, this study showed that molecular markers are effective tools for investigating morph ratios in a population containing the non-flowering individuals or during the non-flowering seasons.     

QTL analysis of root traits as related to phosphorus efficiency in soybean

Background and Aims

Low phosphorus (P) availability is a major constraint to soybean growth and production, especially in tropical and subtropical areas. Root traits have been shown to play critical roles in P efficiency in crops. Identification of the quantitative trait loci (QTLs) conferring superior root systems could significantly enhance genetic improvement in soybean P efficiency.

Methods

A population of 106 F₉ recombinant inbred lines (RILs) derived from a cross between BD2 and BX10, which contrast in both P efficiency and root architecture, was used for mapping and QTL analysis. Twelve traits were examined in acid soils. A linkage map was constructed using 296 simple sequence repeat (SSR) markers with the Kosambi function, and the QTLs associated with these traits were detected by composite interval mapping and multiple-QTL mapping.

Key Results

The first soybean genetic map based on field data from parental genotypes contrasting both in P efficiency and root architecture was constructed. Thirty-one putative QTLs were detected on five linkage groups, with corresponding contribution ratios of 9·1–31·1 %. Thirteen putative QTLs were found for root traits, five for P content, five for biomass and five for yield traits. Three clusters of QTLs associated with the traits for root and P efficiency at low P were located on the B1 linkage group close to SSR markers Satt519 and Satt519-Sat_128, and on the D2 group close to Satt458; and one cluster was on the B1 linkage group close to Satt519 at high P.

Conclusions

Most root traits in soybean were conditioned by more than two minor QTLs. The region closer to Satt519 on the B1 linkage group might have great potential for future genetic improvement for soybean P efficiency through root selection.     

Genetics of Cryptic Speciation within an Arctic Mustard,Draba nivalis

Crossing experiments indicate that hybrid sterility barriers frequently have developed within diploid, circumpolar plant species of the genus Draba. To gain insight into the rapid evolution of postzygotic reproductive isolation in this system, we augmented the linkage map of one of these species, D. nivalis, and searched for quantitative trait loci (QTLs) associated with reproductive isolation. The map adds 63 new dominant markers to a previously published dataset of 31 co-dominant microsatellites. These markers include 52 amplified fragment length polymorphisms (AFLPs) and 11 sequence-specific amplified polymorphisms (SSAPs) based on retrotransposon sequence. 22 markers displaying transmission ratio distortion were further included in the map. We resolved eight linkage groups with a total map length of 894 cM. Significant genotype-trait associations, or quantitative trait loci (QTL), were detected for reproductive phenotypes including pollen fertility (4 QTLs), seed set (3 QTLs), flowering time (3 QTLs) and number of flowers (4 QTLs). Observed patterns of inheritance were consistent with the influence of both nuclear-nuclear interactions and chromosomal changes on these traits. All seed set QTLs and one pollen fertility QTL displayed underdominant effects suggestive of the involvement of chromosomal rearrangements in hybrid sterility. Interestingly, D. nivalis is predominantly self-fertilizing, which may facilitate the establishment of underdominant loci and contribute to reproductive isolation.     

Admixture mapping of quantitative traits in Populus hybrid zones: power and limitations

Uncovering the genetic architecture of species differences is of central importance for understanding the origin and maintenance of biological diversity. Admixture mapping can be used to identify the number and effect sizes of genes that contribute to the divergence of ecologically important traits, even in taxa that are not amenable to laboratory crosses because of their long generation time or other limitations. Here, we apply admixture mapping to naturally occurring hybrids between two ecologically divergent Populus species. We map quantitative trait loci for eight leaf morphological traits using 77 mapped microsatellite markers from all 19 chromosomes of Populus. We apply multivariate linear regression analysis allowing the modeling of additive and non-additive gene action and identify several candidate genomic regions associated with leaf morphology using an information-theoretic approach. We perform simulation studies to assess the power and limitations of admixture mapping of quantitative traits in natural hybrid populations for a variety of genetic architectures and modes of gene action. Our results indicate that (1) admixture mapping has considerable power to identify the genetic architecture of species differences if sample sizes and marker densities are sufficiently high, (2) modeling of non-additive gene action can help to elucidate the discrepancy between genotype and phenotype sometimes seen in interspecific hybrids, and (3) the genetic architecture of leaf morphological traits in the studied Populus species involves complementary and overdominant gene action, providing the basis for rapid adaptation of these ecologically important forest trees.     

Quantitative trait loci (QTLs) analysis of palm oil fatty acid composition in an interspecific pseudo-backcross from Elaeis oleifera (H.B.K.) Cortés and oil palm (Elaeis guineensis Jacq.)

We chose an Elaeis interspecific pseudo-backcross of first generation (E. oleifera × E. guineensis) × E. guineensis to identify quantitative trait loci (QTLs) for fatty acid composition of palm oil. A dense microsatellite linkage map of 362 loci spanned 1.485 cM, representing the 16 pairs of homologous chromosomes in the Elaeis genus from which we traced segregating alleles from both E. oleifera and E. guineensis grandparents. The relative linear orders of mapped loci suggested the probable absence of chromosome rearrangements between the E. oleifera and E. guineensis genomes. A total of 19 QTL associated to the palm oil fatty acid composition were evidenced. The QTL positions and the species origin as well as the estimated effects of the QTL marker alleles were in coherence with the knowledge of the oil biosynthesis pathway in plants and with the individual phenotypic correlations between the traits. The mapping of chosen Elaeis key genes related to oleic acid C18:1, using intra-gene SNPs, supported several QTLs underlying notably FATA and SAD enzymes. The high number of hyper-variable SSR loci of known relative linear orders and the QTL information make these resources valuable for such mapping study in other Elaeis breeding materials.     

Targeted linkage map densification to improve cell wall related QTL detection and interpretation in maize

Several QTLs for cell wall degradability and lignin content were previously detected in the F288 × F271 maize RIL progeny, including a set of major QTLs located in bin 6.06. Unexpectedly, allelic sequencing of genes located around the bin 6.06 QTL positions revealed a monomorphous region, suggesting that these QTLs were likely “ghost” QTLs. Refining the positions of all QTLs detected in this population was thus considered, based on a linkage map densification in most important QTL regions, and in several large still unmarked regions. Re-analysis of data with an improved genetic map (173 markers instead of 108) showed that ghost QTLs located in bin 6.06 were then fractionated over two QTL positions located upstream and downstream of the monomorphic region. The area located upstream of bin 6.06 position carried the major QTLs, which explained from 37 to 59 % of the phenotypic variation for per se values and extended on only 6 cM, corresponding to a physical distance of 2.2 Mbp. Among the 92 genes present in the corresponding area of the B73 maize reference genome, nine could putatively be considered as involved in the formation of the secondary cell wall [bHLH, FKBP, laccase, fasciclin, zinc finger C2H2-type and C3HC4-type (two genes), NF-YB, and WRKY]. In addition, based on the currently improved genetic map, eight QTLs were detected in bin 4.09, while only one QTL was highlighted in the initial investigation. Moreover, significant epistatic interaction effects were shown for all traits between these QTLs located in bin 4.09 and the major QTLs located in bin 6.05. Three genes related to secondary cell wall assembly (ZmMYB42, COV1-like, PAL-like) underlay QTL support intervals in this newly identified bin 4.09 region. The current investigations, even if they were based only on one RIL progeny, illustrated the interest of a targeted marker mapping on a genetic map to improve QTL position.     

Mapping in the era of sequencing: high density genotyping and its application for mapping TYLCV resistance in Solanum pimpinellifolium

Background

A RIL population between Solanum lycopersicum cv. Moneymaker and S. pimpinellifolium G1.1554 was genotyped with a custom made SNP array. Additionally, a subset of the lines was genotyped by sequencing (GBS).

Results

A total of 1974 polymorphic SNPs were selected to develop a linkage map of 715 unique genetic loci. We generated plots for visualizing the recombination patterns of the population relating physical and genetic positions along the genome.This linkage map was used to identify two QTLs for TYLCV resistance which contained favourable alleles derived from S. pimpinellifolium. Further GBS was used to saturate regions of interest, and the mapping resolution of the two QTLs was improved. The analysis showed highest significance on Chromosome 11 close to the region of 51.3 Mb (qTy-p11) and another on Chromosome 3 near 46.5 Mb (qTy-p3). Furthermore, we explored the population using untargeted metabolic profiling, and the most significant differences between susceptible and resistant plants were mainly associated with sucrose and flavonoid glycosides.

Conclusions

The SNP information obtained from an array allowed a first QTL screening of our RIL population. With additional SNP data of a RILs subset, obtained through GBS, we were able to perform an in silico mapping improvement to further confirm regions associated with our trait of interest. With the combination of different ~ omics platforms we provide valuable insight into the genetics of S. pimpinellifolium-derived TYLCV resistance.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-1152) contains supplementary material, which is available to authorized users.     

Genetic analysis of Verticillium wilt resistance in a backcross inbred line population and a meta-analysis of quantitative trait loci for disease resistance in cotton

Background

Verticillium wilt (VW) and Fusarium wilt (FW), caused by the soil-borne fungi Verticillium dahliae and Fusarium oxysporum f. sp. vasinfectum, respectively, are two most destructive diseases in cotton production worldwide. Root-knot nematodes (Meloidogyne incognita, RKN) and reniform nematodes (Rotylenchulus reniformis, RN) cause the highest yield loss in the U.S. Planting disease resistant cultivars is the most cost effective control method. Numerous studies have reported mapping of quantitative trait loci (QTLs) for disease resistance in cotton; however, very few reliable QTLs were identified for use in genomic research and breeding.

Results

This study first performed a 4-year replicated test of a backcross inbred line (BIL) population for VW resistance, and 10 resistance QTLs were mapped based on a 2895 cM linkage map with 392 SSR markers. The 10 VW QTLs were then placed to a consensus linkage map with other 182 VW QTLs, 75 RKN QTLs, 27 FW QTLs, and 7 RN QTLs reported from 32 publications. A meta-analysis of QTLs identified 28 QTL clusters including 13, 8 and 3 QTL hotspots for resistance to VW, RKN and FW, respectively. The number of QTLs and QTL clusters on chromosomes especially in the A-subgenome was significantly correlated with the number of nucleotide-binding site (NBS) genes, and the distribution of QTLs between homeologous A- and D- subgenome chromosomes was also significantly correlated.

Conclusions

Ten VW resistance QTL identified in a 4-year replicated study have added useful information to the understanding of the genetic basis of VW resistance in cotton. Twenty-eight disease resistance QTL clusters and 24 hotspots identified from a total of 306 QTLs and linked SSR markers provide important information for marker-assisted selection and high resolution mapping of resistance QTLs and genes. The non-overlapping of most resistance QTL hotspots for different diseases indicates that their resistances are controlled by different genes.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1682-2) contains supplementary material, which is available to authorized users.