We report the draft genome of the black cottonwood tree, Populus trichocarpa . Integration of shotgun sequence assembly with genetic mapping enabled chromosome-scale reconstruction of the genome. More than 45,000 putative protein-coding genes were identified. Analysis of the assembled genome revealed a whole-genome duplication event; about 8000 pairs of duplicated genes from that event survived in the Populus genome. A second, older duplication event is indistinguishably coincident with the divergence of the Populus and Arabidopsis lineages. Nucleotide substitution, tandem gene duplication, and gross chromosomal rearrangement appear to proceed substantially more slowly in Populus than in Arabidopsis. Populus has more protein-coding genes than Arabidopsis , ranging on average from 1.4 to 1.6 putative Populus homologs for each Arabidopsis gene. However, the relative frequency of protein domains in the two genomes is similar. Overrepresented exceptions in Populus include genes associated with lignocellulosic wall biosynthesis, meristem development, disease resistance, and metabolite transport.
The renewed interest in the use of hybrid zones for studying speciation calls for the identification and study of hybrid zones across a wide range of organisms, especially in long-lived taxa for which it is often difficult to generate interpopulation variation through controlled crosses. Here, we report on the extent and direction of introgression between two members of the "model tree" genus Populus: Populus alba (white poplar) and Populus tremula (European aspen), across a large zone of sympatry located in the Danube valley. We genotyped 93 hybrid morphotypes and samples from four parental reference populations from within and outside the zone of sympatry for a genome-wide set of 20 nuclear microsatellites and eight plastid DNA restriction site polymorphisms. Our results indicate that introgression occurs preferentially from P. tremula to P. alba via P. tremula pollen. This unidirectional pattern is facilitated by high levels of pollen vs. seed dispersal in P. tremula (pollen/seed flow = 23.9) and by great ecological opportunity in the lowland floodplain forest in proximity to P. alba seed parents, which maintains gene flow in the direction of P. alba despite smaller effective population sizes (N(e)) in this species (P. alba N(e)c. 500-550; P. tremula N(e)c. 550-700). Our results indicate that hybrid zones will be valuable tools for studying the genetic architecture of the barrier to gene flow between these two ecologically divergent Populus species.
Admixture between genetically divergent populations facilitates genomic studies of the mechanisms involved in adaptation, reproductive isolation, and speciation, including mapping of the loci involved in these phenomena. Little is known about how pre-and postzygotic barriers will affect the prospects of ''admixture mapping'' in wild species. We have studied 93 mapped genetic markers (microsatellites, indels, and sequence polymorphisms, $60,000 data points) to address this topic in hybrid zones of Populus alba and P. tremula, two widespread, ecologically important forest trees. Using genotype and linkage information and recently developed analytical tools we show that (1) reproductive isolation between these species is much stronger than previously assumed but this cannot prevent the introgression of neutral or advantageous alleles, (2) unexpected genotypic gaps exist between recombinant hybrids and their parental taxa, (3) these conspicuous genotypic patterns are due to assortative mating and strong postzygotic barriers, rather than recent population history. We discuss possible evolutionary trajectories of hybrid lineages between these species and outline strategies for admixture mapping in hybrid zones between highly divergent populations. Datasets such as this one are still rare in studies of natural hybrid zones but should soon become more common as high throughput genotyping and resequencing become feasible in nonmodel species.
Adaptation to new environments can start from new mutations or from standing variation already present in natural populations. Whether admixture constrains or facilitates adaptation from standing variation is largely unknown, especially in ecological keystone or foundation species. We examined patterns of neutral and adaptive population divergence in Populus tremula L., a widespread forest tree, using mapped molecular genetic markers. We detected the genetic signature of postglacial admixture between a Western and an Eastern lineage of P. tremula in Scandinavia, an area suspected to represent a zone of postglacial contact for many species of animals and plants. Stringent divergence‐based neutrality tests provided clear indications for locally varying selection at the European scale. Six of 12 polymorphisms under selection were located less than 1 kb away from the nearest gene predicted by the Populus trichocarpa genome sequence. Few of these loci exhibited a signature of ‘selective sweeps’ in diversity‐based tests, which is to be expected if adaptation occurs primarily from standing variation. In Scandinavia, admixture explained genomic patterns of ancestry and the nature of clinal variation and strength of selection for bud set, a phenological trait of great adaptive significance in temperate trees, measured in a common garden trial. Our data provide a hitherto missing direct link between past range shifts because of climatic oscillations, and levels of standing variation currently available for selection and adaptation in a terrestrial foundation species.
The use of admixed human populations to scan the genome for chromosomal segments affecting complex phenotypic traits has proved a powerful analytical tool. However, its potential in other organisms has not yet been evaluated. Here, we use DNA microsatellites to assess the feasibility of this approach in hybrid zones between two members of the 'model tree' genus Populus: Populus alba (white poplar) and Populus tremula (European aspen). We analyzed samples of both species and a Central European hybrid zone (N ¼ 544 chromosomes) for a genome-wide set of 19 polymorphic DNA microsatellites. Our results indicate that allele frequency differentials between the two species are substantial (mean d ¼ 0.61970.067). Background linkage disequilibrium (LD) in samples of the parental gene pools is moderate and should respond to sampling schemes that minimize drift and account for rare alleles. LD in hybrids decays with increasing number of backcross generations as expected from theory and approaches background levels of the parental gene pools in advanced generation backcrosses. Introgression from P. tremula into P. alba varies strongly across marker loci. For several markers, alleles from P. tremula are slightly over-represented relative to neutral expectations, whereas a single locus exhibits evidence of selection against P. tremula genotypes. We interpret our results in terms of the potential for admixture mapping in these two ecologically divergent Populus species, and we validate a modified approach of studying genotypic clines in 'mosaic' hybrid zones. Keywords: hybrid zone; admixture; introgression; linkage disequilibrium; rare alleles; Populus Introduction 'Admixture mapping' as suggested by Chakraborty and Weiss (1988) and Briscoe et al. (1994) utilizes linkage disequilibrium (LD) induced by the mixing of genes from two divergent gene pools. In an outcrossing species and in the absence of confounding population structure, LD will decay with increasing genetic map or chromosomal distance (Lynch and Walsh, 1998), because the chance that stretches of DNA are broken up by recombination becomes greater the further two loci are apart. Admixture will effectively widen the region of a genome that is affected by LD, because recombination will take several/many generations to break up the chromosome blocks derived from each parental population (Briscoe et al., 1994;Chapman and Thompson, 2002). Hence, admixture potentially facilitates molecular marker-based 'genome-scans' to narrow in on genomic regions conferring trait differences between two divergent source gene pools (Chakraborty and Weiss, 1988;Briscoe et al., 1994;McKeigue et al., 2000;Pfaff et al., 2001). This prediction has been verified recently by successful admixture genome-scans for two complex traits in humans -hypertension and susceptibility for multiple sclerosis (Reich et al., 2005;Zhu et al., 2005).The requirements for genome-scans through admixture in humans have been carefully evaluated by geneticists for years (e.g., McKeigue et al., 2000;Pfaff et al., 2001;H...
This paper provides a review of theoretical and practical aspects related to genetic management of forest trees. The implementation of international commitments on forest genetic diversity has been slow and partly neglected. Conservation of forest genetic diversity is still riddled with problems, and complexities of national legal and administrative structures. Europe is an example of a complex region where the distribution ranges of tree species extend across large geographical areas with profound environmental differences, and include many countries. Conservation of forest genetic diversity in Europe has been hampered by lack of common understanding on the management requirements for genetic conservation units of forest trees. The challenge resides in integrating scientific knowledge on conservation genetics into management of tree populations so that recommendations are feasible to implement across different countries. Here, we present pan-European minimum requirements for dynamic conservation units of forest genetic diversity. The units are natural or man-made tree populations which are managed for maintaining evolutionary processes and adaptive potential across generations. Each unit should have a designated status and a management plan, and one or more tree species recognized for as target species for genetic conservation. The minimum sizes of the units are set at 500, 50 or 15 reproducing individuals depending on tree species and conservation objectives. Furthermore, silvicultural interventions should be allowed to enhance genetic processes, as needed, and field inventories carried out to monitor regeneration and the population size. These minimum requirements are now used by 36 countries to improve management of forest genetic diversity.
The maintenance of species barriers in the face of gene flow is often thought to result from strong selection against intermediate genotypes, thereby preserving genetic differentiation. Most speciation genomic studies thus aim to identify exceptionally divergent loci between populations, but divergence will be affected by many processes other than reproductive isolation (RI) and speciation. Through genomic studies of recombinant hybrids sampled in the wild, genetic variation associated with RI can be observed in situ, because selection against incompatible genotypes will leave detectable patterns of variation in the hybrid genomes. To better understand the mechanisms directly involved in RI, we investigated three natural 'replicate' hybrid zones between two divergent Populus species via locus-specific patterns of ancestry across recombinant hybrid genomes. As expected, genomic patterns in hybrids and their parental species were consistent with the presence of underdominant selection at several genomic regions. Surprisingly, many loci displayed greatly increased between-species heterozygosity in recombinant hybrids despite striking genetic differentiation between the parental genomes, the opposite of what would be expected with selection against intermediate genotypes. Only a limited, reproducible set of genotypic combinations was present in hybrid genomes across localities. In the absence of clearly delimited 'hybrid habitats', our results suggest that complex epistatic interactions within genomes play an important role in advanced stages of RI between these ecologically divergent forest trees. This calls for more genomic studies that test for unusual patterns of genomic ancestry in hybridizing species.
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