Multilocus Patterns of Nucleotide Diversity and Divergence Reveal Positive Selection at Candidate Genes Related to Cold Hardiness in Coastal Douglas Fir (Pseudotsuga menziesii var. menziesii)

Abstract

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.

The heterogeneous levels of linkage disequilibrium in white spruce genes and comparative analysis with other conifers

“…The average levels of nucleotide diversity found in P. glauca gene sequences were similar to those reported in P. sylvestris (Pyhäjärvi et al, 2007;Wachowiak et al, 2009), P. taeda (González-Martínez et al, 2006a), P. abies (Heuertz et al, 2006) and P. menziesii (Eckert et al, 2009a). They were also similar to those reported for the angiosperm tree species Populus tremula (Ingvarsson, 2008), but were lower than those reported for annual species such as Arabidopsis (Schmid et al, 2005) or maize (Wright and Gaut, 2005; Table 4).…”

“…LD in genes from P. taeda and Douglas fir represented a less drastic drop of LD over distance than for the other three species (Table 2; Figure 2). Eckert et al (2009a) reported a half-decay of LD over 1000 bp in Douglas fir genes, which is substantive and above values for all other conifers investigated so far, at the opposite of the observations for white spruce.…”

“…We calculated or retrieved nucleotide diversity values of genes sequenced in other conifer species including values from 18 genes for Picea abies (Heuertz et al, 2006), 18 genes for P. taeda (González-Martínez et al, 2006b), 14 genes for Pinus sylvestris (Pyhäjärvi et al, 2007) and 121 genes for Pseudotsuga menziesii var. menziesii (Eckert et al, 2009a) (Table 1). We then compared the distributions of p values for all sites, synonymous and non-synonymous sites between species (including white spruce).…”

“…In Douglas fir (Pseudostuga menziesii var. menziesii), the sequences were obtained from 24 unrelated trees collected in 6 regions located across Washington and Oregon, and representing various environments (Eckert et al, 2009a). As for P. sylvestris (Pyhäjärvi et al, 2007), the Douglas fir samples were widely distributed and the two species share much in terms of population genetic trends and features.…”

“…Studies of small gene sets have shown low-to-moderate levels of nucleotide diversity and LD decaying within gene limits in several conifer species (Brown et al, 2004;Neale and Savolainen, 2004;Pot et al, 2005;Heuertz et al, 2006;González-Martínez et al, 2006b;Pyhäjärvi et al, 2007;Wachowiak et al, 2009;Li et al, 2010;Namroud et al, 2010). Higher LD was found in Douglas fir genes with a half-decay of LD over 1 kb, on average (Eckert et al, 2009a).…”