Adaptation to cold is one of the greatest challenges to forest trees. This process is highly synchronized with environmental cues relating to photoperiod and temperature. Here, we use a candidate gene-based approach to search for genetic associations between 384 single-nucleotide polymorphism (SNP) markers from 117 candidate genes and 21 cold-hardiness related traits. A general linear model approach, including population structure estimates as covariates, was implemented for each marker–trait pair. We discovered 30 highly significant genetic associations [false discovery rate (FDR) Q < 0.10] across 12 candidate genes and 10 of the 21 traits. We also detected a set of 7 markers that had elevated levels of differentiation between sampling sites situated across the Cascade crest in northeastern Washington. Marker effects were small (r2 < 0.05) and within the range of those published previously for forest trees. The derived SNP allele, as measured by a comparison to a recently diverged sister species, typically affected the phenotype in a way consistent with cold hardiness. The majority of markers were characterized as having largely nonadditive modes of gene action, especially underdominance in the case of cold-tolerance related phenotypes. We place these results in the context of trade-offs between the abilities to grow longer and to avoid fall cold damage, as well as putative epigenetic effects. These associations provide insight into the genetic components of complex traits in coastal Douglas fir, as well as highlight the need for landscape genetic approaches to the detection of adaptive genetic diversity.
SummaryForest trees have gained much attention in recent years as nonclassical model eukaryotes for population, evolutionary and ecological genomic studies. Because of low domestication, large open-pollinated native populations, and high levels of both genetic and phenotypic variation, they are ideal organisms to unveil the molecular basis of population adaptive divergence in nature. Population genomics, in its broadsense definition, is an emerging discipline that combines genome-wide sampling with traditional population genetic approaches to understanding evolution. Here we briefly review traditional methods of studying adaptive genetic variation in forest trees, and describe a new, integrated population genomics approach. First, alleles (haplotypes) at candidate genes for adaptive traits and their effects on phenotypes need to be characterized via sequencing and association mapping. At this stage, functional genomics can assist in understanding gene action and regulation by providing detailed transcriptional profiles. Second, frequencies of alleles in native populations for causative single-nucleotide polymorphisms are estimated to identify patterns of adaptive variation across heterogeneous environments. Population genomics, through deciphering allelic effects on phenotypes and identifying patterns of adaptive variation at the landscape level, will in the future constitute a useful tool, if cost-effective, to design conservation strategies for forest trees.
Nuclear sequence variation and linkage disequilibrium (LD) were studied in 15 cold-hardiness-and 3 wood quality-related candidate genes in Douglas fir [Pseudotsuga menziesii (Mirb.) Franco]. This set of genes was selected on the basis of its function in other plants and collocation with cold-hardiness-related quantitative trait loci (QTL). The single-nucleotide polymorphism (SNP) discovery panel represented 24 different trees from six regions in Washington and Oregon plus parents of a segregating population used in the QTL study. The frequency of SNPs was one SNP per 46 bp across coding and noncoding regions on average. Haplotype and nucleotide diversities were also moderately high with H d ¼ 0.827 6 0.043 and p ¼ 0.00655 6 0.00082 on average, respectively. The nonsynonymous (replacement) nucleotide substitutions were almost five times less frequent than synonymous ones and substitutions in noncoding regions. LD decayed relatively slowly but steadily within genes. Haploblock analysis was used to define haplotype tag SNPs (htSNPs). These data will help to select SNPs for association mapping, which is already in progress.
A comparative genetic map was constructed between two important genera of the family Pinaceae. Ten homologous linkage groups in loblolly pine (Pinus taeda L.) and Douglas fir (Pseudotsuga menziesii [Mirb.] Franco) were identified using orthologous expressed sequence tag polymorphism (ESTP) and restriction fragment length polymorphism (RFLP) markers. The comparative mapping revealed extensive synteny and colinearity between genomes of the Pinaceae, consistent with the hypothesis of conservative chromosomal evolution in this important plant family. This study reports the first comparative map in forest trees at the family taxonomic level and establishes a framework for comparative genomics in Pinaceae.
Background: Previous loblolly pine (Pinus taeda L.) genetic linkage maps have been based on a variety of DNA polymorphisms, such as AFLPs, RAPDs, RFLPs, and ESTPs, but only a few SSRs (simple sequence repeats), also known as simple tandem repeats or microsatellites, have been mapped in P. taeda. The objective of this study was to integrate a large set of SSR markers from a variety of sources and published cDNA markers into a composite P. taeda genetic map constructed from two reference mapping pedigrees. A dense genetic map that incorporates SSR loci will benefit complete pine genome sequencing, pine population genetics studies, and pine breeding programs. Careful marker annotation using a variety of references further enhances the utility of the integrated SSR map.
Forest trees exhibit remarkable adaptations to their environments. The genetic basis for phenotypic adaptation to climatic gradients has been established through a long history of common garden, provenance, and genecological studies. The identities of genes underlying these traits, however, have remained elusive and thus so have the patterns of adaptive molecular diversity in forest tree genomes. Here, we report an analysis of diversity and divergence for a set of 121 cold-hardiness candidate genes in coastal Douglas fir (Pseudotsuga menziesii var. menziesii). Application of several different tests for neutrality, including those that incorporated demographic models, revealed signatures of selection consistent with selective sweeps at three to eight loci, depending upon the severity of a bottleneck event and the method used to detect selection. Given the high levels of recombination, these candidate genes are likely to be closely linked to the target of selection if not the genes themselves. Putative homologs in Arabidopsis act primarily to stabilize the plasma membrane and protect against denaturation of proteins at freezing temperatures. These results indicate that surveys of nucleotide diversity and divergence, when framed within the context of further association mapping experiments, will come full circle with respect to their utility in the dissection of complex phenotypic traits into their genetic components.
Despite significant advances in high-throughput DNA sequencing, many important species remain understudied at the genome level. In this study we addressed a question of what can be predicted about the genome-wide characteristics of less studied species, based on the genomic data from completely sequenced species. Using NCBI databases we performed a comparative genome-wide analysis of such characteristics as alternative splicing, number of genes, gene products and exons in 36 completely sequenced model species. We created statistical regression models to fit these data and applied them to loblolly pine (Pinus taeda L.), an example of an important species whose genome has not been completely sequenced yet. Using these models, the genome-wide characteristics, such as total number of genes and exons, can be roughly predicted based on parameters estimated from available limited genomic data, e.g. exon length and exon/gene ratio.
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