Genomic prediction for fusiform rust disease incidence in a large cloned population of Pinus taeda.

In this study, 723 Pinus taeda L. (loblolly pine) clonal varieties genotyped with 16920 SNP markers were used to evaluate genomic selection for fusiform rust disease caused by the fungus Cronartium quercuum f. sp. fusiforme. The 723 clonal varieties were from five full-sib families. They were a subset of a larger population (1831 clonal varieties), field-tested across 26 locations in the southeast US. Ridge regression, Bayes B, and Bayes Cπ models were implemented to study marker-trait associations and estimate predictive ability for selection. A cross-validation scenario based on a random sampling of 80% of the clonal varieties for the model building had higher (0.71-0.76) prediction accuracies of genomic estimated breeding values compared with family and within-family cross-validation scenarios. Random sampling within families for model training to predict genomic estimated breeding values of the remaining progenies within each family produced accuracies between 0.38 and 0.66. Using four families out of five for model training was not successful. The results showed the importance of genetic relatedness between the training and validation sets. Bayesian whole-genome regression models detected three QTL with large effects on the disease outcome, explaining 54% of the genetic variation in the trait. The significance of QTL was validated with GWAS while accounting for the population structure and polygenic effect. The odds of disease incidence for heterozygous AB genotypes were 10.7 and 12.1 times greater than the homozygous AA genotypes for SNP11965 and SNP6347 loci, respectively. Genomic selection for fusiform rust disease incidence could be effective in P. taeda breeding. Markers with large effects could be fit as fixed covariates to increase the prediction accuracies, provided that their effects are validated further.

The evolutionary genetics of the genes underlying phenotypic associations for loblolly pine (Pinus taeda, Pinaceae).

A primary goal of evolutionary genetics is to discover and explain the genetic basis of fitness-related traits and how this genetic basis evolves within natural populations. Unprecedented technological advances have fueled the discovery of genetic variants associated with ecologically relevant phenotypes in many different life forms, as well as the ability to scan genomes for deviations from selectively neutral models of evolution. Theoretically, the degree of overlap between lists of genomic regions identified using each approach is related to the genetic architecture of fitness-related traits and the strength and type of natural selection molding variation at these traits within natural populations. Here we address for the first time in a plant the degree of overlap between these lists, using patterns of nucleotide diversity and divergence for >7000 unique amplicons described from the extensive expressed sequence tag libraries generated for loblolly pine (Pinus taeda L.) in combination with the >1000 published genetic associations. We show that loci associated with phenotypic traits are distinct with regard to neutral expectations. Phenotypes measured at the whole plant level (e.g., disease resistance) exhibit an approximately twofold increase in the proportion of adaptive nonsynonymous substitutions over the genome-wide average. As expected for polygenic traits, these signals were apparent only when loci were considered at the level of functional sets. The ramifications of this result are discussed in light of the continued efforts to dissect the genetic basis of quantitative traits.

Association genetics of the loblolly pine (Pinus taeda, Pinaceae) metabolome.

The metabolome of a plant comprises all small molecule metabolites, which are produced during cellular processes. The genetic basis for metabolites in nonmodel plants is unknown, despite frequently observed correlations between metabolite concentrations and stress responses. A quantitative genetic analysis of metabolites in a nonmodel plant species is thus warranted. Here, we use standard association genetic methods to correlate 3563 single nucleotide polymorphisms (SNPs) to concentrations of 292 metabolites measured in a single loblolly pine (Pinus taeda) association population. A total of 28 single locus associations were detected, representing 24 and 20 unique SNPs and metabolites, respectively. Multilocus Bayesian mixed linear models identified 2998 additional associations for a total of 1617 unique SNPs associated to 255 metabolites. These SNPs explained sizeable fractions of metabolite heritabilities when considered jointly (56.6% on average) and had lower minor allele frequencies and magnitudes of population structure as compared with random SNPs. Modest sets of SNPs (n = 1-23) explained sizeable portions of genetic effects for many metabolites, thus highlighting the importance of multi-SNP models to association mapping, and exhibited patterns of polymorphism consistent with being linked to targets of natural selection. The implications for association mapping in forest trees are discussed.

Association mapping of quantitative disease resistance in a natural population of loblolly pine (Pinus taeda L.).

Genetic resistance to disease incited by necrotrophic pathogens is not well understood in plants. Whereas resistance is often quantitative, there is limited information on the genes that underpin quantitative variation in disease resistance. We used a population genomic approach to identify genes in loblolly pine (Pinus taeda) that are associated with resistance to pitch canker, a disease incited by the necrotrophic pathogen Fusarium circinatum. A set of 498 largely unrelated, clonally propagated genotypes were inoculated with F. circinatum microconidia and lesion length, a measure of disease resistance, data were collected 4, 8, and 12 weeks after inoculation. Best linear unbiased prediction was used to adjust for imbalance in number of observations and to identify highly susceptible and highly resistant genotypes ("tails"). The tails were reinoculated to validate the results of the full population screen. Significant associations were detected in 10 single nucleotide polymorphisms (SNPs) (out of 3938 tested). As hypothesized for genes involved in quantitative resistance, the 10 SNPs had small effects and proposed roles in basal resistance, direct defense, and signal transduction. We also discovered associated genes with unknown function, which would have remained undetected in a candidate gene approach constrained by annotation for disease resistance or stress response.