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Conifer Evolution, from Demography and Local Adaptation to Evolutionary Rates: Examples from the Picea genus
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Evolutionary process can be inferred at three different levels: the species level, the population level and the molecular level. In this thesis, I applied approaches at these three levels and aimed to get a comprehensive picture of conifer evolution, from speciation and demography to geographic variation and local adaptation, and then to the molecular evolution of proteins and small regulatory RNAs.

Spruce species have been observed to possess a large number of trans-species shared polymorphisms. Using an “Isolation with migration” model, we found that the large effective population size of spruce retained these shared polymorphisms, inheriting them from the common ancestor. Post-divergence gene flow only existed between Picea abies and P. glauca, and between P. wilsonii and P. schrenkiana. The combination of Tajima’s D and Fay & Wu’s H at most of loci suggested an ancient and severe bottleneck for most species except P. breweriana.

Furthermore, I investigated the effect of local selection in two parallel clines, which is one of the major forces that can cause divergence or even speciation. The timing of bud set and growth cessation was found correlated with latitude in populations of P. abies and P. obovata. Using allele frequency spectrum analyses we identified three genes under local selection in both species including two circadian-clock genes GI and PRR7, and one photoperiodic gene FTL2. This indicated that parallel evolution could occur through groups of genes within related pathways. Clinal variation at expression level provided stronger evidence of selection in FTL2, which has previously been associated with bud set in P. abies.

Finally we focused on the molecular evolution of mRNA and small regulatory RNAs in P. abies. With the help of Next-Generation sequencing, we have achieved in spruce the first de novel assembly of the needle transcriptome and a preliminary characterization of sRNA populations. Along with features common in plants, spruce also exhibited novelties in many aspects including lower substitution rate and protein evolutionary rate, dominance of 21-nt sRNA, and a large proportion of TIR-NBS-LRR genes as sRNA sources and targets.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2012. , 52 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 947
Keyword [en]
Speciation, Demographics, clinal variation, convergent evolution, transcriptome, small regulatory RNA
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Functional Genomics; Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-177482ISBN: 978-91-554-8411-8 (print)OAI: oai:DiVA.org:uu-177482DiVA: diva2:541925
Public defence
2012-09-14, Lindahlsalen, EBC, Norbyvägen 18A, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2012-08-24 Created: 2012-07-13 Last updated: 2013-01-22Bibliographically approved
List of papers
1. New insights on the speciation history and nucleotide diversity of three boreal spruce species and a Tertiary relict
Open this publication in new window or tab >>New insights on the speciation history and nucleotide diversity of three boreal spruce species and a Tertiary relict
2010 (English)In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 104, no 1, 3-14 p.Article in journal (Refereed) Published
Abstract [en]

In all, 10 nuclear loci were re-sequenced in four spruce species. Three of the species are boreal species with very large natural ranges: Picea mariana and P. glauca are North American, and P. abies, is Eurasian. The fourth species, P. breweriana, is a Tertiary relict from Northern California, with a very small natural range. Although the boreal species population sizes have fluctuated through the Ice Ages, P. breweriana is believed to have had a rather stable population size through the Quaternary. Indeed, the average Tajima’s D was close to zero in this species and negative in the three boreal ones. Reflecting differences in current population sizes, nucleotide diversity was an order of magnitude lower in P. breweriana than in the boreal species. This is in contrast to the similar and high levels of heterozygosity observed in previous studies at allozyme loci across species. As the species have very different histories and effective population sizes, selection at allozyme loci rather than demography appears to be a better explanation for this discrepancy. Parameters of Isolation-with-Migration (IM) models were also estimated for pairs of species. Shared polymorphisms were extensive and fixed polymorphisms few. Divergence times were much shorter than those previously reported. There was also evidence of historical gene flow between P. abies and P. glauca. The latter was more closely related to P. abies than to its sympatric relative P. mariana. This last result suggests that North American and Eurasian species might have been geographically much closer in the recent past than they are today.

Keyword
picea; nucleotide diversity; divergence time; migration; speciation
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-119939 (URN)10.1038/hdy.2009.88 (DOI)000272794600002 ()
Available from: 2010-03-03 Created: 2010-03-03 Last updated: 2017-12-12Bibliographically approved
2. Demographic histories of four spruce (Picea) species of the Qinghai-Tibetan Plateau and neighboring areas inferred from multiple nuclear loci
Open this publication in new window or tab >>Demographic histories of four spruce (Picea) species of the Qinghai-Tibetan Plateau and neighboring areas inferred from multiple nuclear loci
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2010 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 27, no 5, 1001-1014 p.Article in journal (Refereed) Published
Abstract [en]

Nucleotide variation at 12 to 16 nuclear loci was studied in three spruce species from the Qinghai-Tibetan Plateau (QTP), Picea likiangensis, P. wilsonii and P. purpurea, and one species from the Tian Shan mountain range, P. schrenkiana. Silent nucleotide diversity was limited in P. schrenkiana and high in the three species from the QTP, with values higher than in boreal spruce species, despite their much more restricted distributions compared to that of the boreal species. In contrast to European boreal species that have experienced severe bottlenecks in the past, coalescent-based analysis suggests that DNA polymorphism in the species from the QTP and adjacent areas is compatible with the standard neutral model (P. likiangensis, P. wilsonii, P. schrenkiana) or with population growth (P. purpurea). In order to test if P. purpurea is a diploid hybrid of P. likiangensis and P. wilsonii, we used a combination of approaches, including model based inference of population structure, Isolation-with-Migration models and recent theoretical results on the effect of introgression on the geographic distribution of diversity. In contrast to the three other species, each of which was predominantly assigned to a single cluster in the Structure analysis, P. purpurea individuals were scattered over the three main clusters and not, as we had expected, confined to the P. likiangensis and P. wilsonii clusters. Furthermore the contribution of P. schrenkiana was by far the largest one. In agreement with this, the divergence between P. purpurea and P. schrenkiana was lower than the divergence of either P. likiangensis or P. wilsonii from P. schrenkiana. These results, together with previous ones showing that P. purpurea and P. wilsonii share the same haplotypes at both chloroplast and mitochondrial markers, suggest that P. purpurea has a complex origin, possibly involving additional species.

Keyword
Picea, Qinghai Tibetan Plateau, effective population size, divergence time, introgression, speciation
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-121399 (URN)10.1093/molbev/msp301 (DOI)000276994800004 ()20031927 (PubMedID)
Available from: 2010-03-23 Created: 2010-03-23 Last updated: 2017-12-12Bibliographically approved
3. Disentangling the Roles of History and Local Selection in Shaping Clinal Variation of Allele Frequencies and Gene Expression in Norway Spruce (Picea abies)
Open this publication in new window or tab >>Disentangling the Roles of History and Local Selection in Shaping Clinal Variation of Allele Frequencies and Gene Expression in Norway Spruce (Picea abies)
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2012 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 191, no 3, 865-881 p.Article in journal (Refereed) Published
Abstract [en]

Understanding the genetic basis of local adaptation is challenging due to the subtle balance among conflicting evolutionary forces that are involved in its establishment and maintenance. One system with which to tease apart these difficulties is clines in adaptive characters. Here we analyzed genetic and phenotypic variation in bud set, a highly heritable and adaptive trait, among 18 populations of Norway spruce (Picea abies), arrayed along a latitudinal gradient ranging from 47°N to 68°N. We confirmed that variation in bud set is strongly clinal, using a subset of five populations. Genotypes for 137 single-nucleotide polymorphisms (SNPs) chosen from 18 candidate genes putatively affecting bud set and 308 control SNPs chosen from 264 random genes were analyzed for patterns of genetic structure and correlation to environment. Population genetic structure was low (F(ST) = 0.05), but latitudinal patterns were apparent among Scandinavian populations. Hence, part of the observed clinal variation should be attributable to population demography. Conditional on patterns of genetic structure, there was enrichment of SNPs within candidate genes for correlations with latitude. Twenty-nine SNPs were also outliers with respect to F(ST). The enrichment for clinal variation at SNPs within candidate genes (i.e., SNPs in PaGI, PaPhyP, PaPhyN, PaPRR7, and PaFTL2) indicated that local selection in the 18 populations, and/or selection in the ancestral populations from which they were recently derived, shaped the observed cline. Validation of these genes using expression studies also revealed that PaFTL2 expression is significantly associated with latitude, thereby confirming the central role played by this gene in the control of phenology in plants.

Keyword
clinal variation, photoperiodic pathway, Norway spruce, FT genes
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-177467 (URN)10.1534/genetics.112.140749 (DOI)000308999900015 ()22542968 (PubMedID)
Available from: 2012-07-13 Created: 2012-07-13 Last updated: 2017-12-07Bibliographically approved
4. Clinal variation in allele frequency at photoperiodic genes in Siberian spruce: an example of convergent evolution?
Open this publication in new window or tab >>Clinal variation in allele frequency at photoperiodic genes in Siberian spruce: an example of convergent evolution?
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Functional Genomics; Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-177474 (URN)
Available from: 2012-07-13 Created: 2012-07-13 Last updated: 2013-01-22
5. Sequencing of the needle transcriptome from Norway spruce (Picea abies Karst L.) reveals lower substitution rates, but similar selective constraints in gymnosperms compared to angiosperms
Open this publication in new window or tab >>Sequencing of the needle transcriptome from Norway spruce (Picea abies Karst L.) reveals lower substitution rates, but similar selective constraints in gymnosperms compared to angiosperms
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2012 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 13, 589- p.Article in journal (Other academic) Published
Abstract [en]

Background: A detailed knowledge about which genes are expressed in which tissues and at which developmental stage is important for understanding both the function of genes and their evolution. For the vast majority of species, transcriptomes are still largely uncharacterized and even in those where substantial information is available it is often in the form of partially sequenced transcriptomes. With the development of next generation sequencing, a single experiment can now give both a snap-shot of the transcribed part of a species genome and simultaneously estimate levels of gene expression.

Results: mRNA from actively growing needles of Norway spruce (Picea abies) was sequenced using next generation sequencing technology. In total, close to 70 million fragments with a length of 76 bp were sequenced resulting in 5 Gbp of raw data. A de novo assembly of these reads were, together with publicly available expressed sequence tag (EST) data from Norway spruce, used to create a reference transcriptome. Of the 38,419 PUTs (putative unique transcripts) longer than 150 bp in this reference assembly, 59% show similarity to ESTs from other spruce species and of the remaining PUTs, 3,704 show similarity to protein sequences from other plant species, leaving 4,167 PUTs with limited similarity to currently available plant proteins. By predicting coding frames and comparing not only the Norway spruce PUTs, but also PUTs from the close relatives Picea glauca and Picea sitchensis to both Pinus taeda and Taxus mairei, we obtained estimates of synonymous and non-synonymous divergence among conifer species. In addition, we detected close to 15,000 SNPs of high quality and estimated gene expression difference between samples collected during dark and light conditions.

Conclusions: Our study yielded a large number of single nucleotide polymorphisms as well as estimates of gene expression on transcriptome scale. In agreement with a recent study we find that the synonymous substitution rate per year (0.6 × 10-09 and 1.1 × 10-09) is an order of magnitude smaller than values reported for angiosperm herbs, but if one takes generation time in to account, most of this difference disappear. The estimates of the non-synonymous over the synonymous divergence (dN/dS ratio) reported here is in general much lower than 1 and only a few genes showed a ratio larger than 1.

National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-177479 (URN)10.1186/1471-2164-13-589 (DOI)000314646900001 ()
Available from: 2012-07-13 Created: 2012-07-13 Last updated: 2017-12-07Bibliographically approved
6. Major difference in short RNA populations among plants - the results of interaction with pathogen?
Open this publication in new window or tab >>Major difference in short RNA populations among plants - the results of interaction with pathogen?
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Small RNA (sRNA) including miRNA and siRNA are important in the regulation of diverse biological processes. Comparative studies of sRNA from plants have mainly focused on miRNA even though this group in most cases is just a mere fraction of the total sRNA diversity. In the present study we report results from an in-depth analysis of the sRNA population from the conifer Picea abies and compared the results to those of a range of species from the plant kingdom. The vast majority of sRNA in P. abies was 21 nucleotides long siRNA, of which a large fraction originate from degradation of transcribed sequences related to TIR-NBS-LRR (Toll/Interleukin-1-Nucleotide Binding Site-Leucine Rich Repeats) type resistance genes. Over 90% of all genes predicted to contain either a TIR or an NBS domain showed evidence of siRNA degradation. Data further suggests that those phased siRNA are initiated from miRNA guided cleavage, often by an abundant 22 nt miRNA. Comparative analysis over a range of divergent plant species revealed a large variation between species in the abundance of this phenomenon. The process seemed to be virtually absent in several species, including Arabidopsis thaliana, Oryza sativa and non-vascular plants, while particularly high frequencies were observed in Vitis vinifera and Populus thrichocarpa. This divergent pattern between species might reflect a mechanism to limit runaway transcription of these genes in species with rapidly expanding NBS-LRR gene families. Alternatively it might reflect variation in a counter-counter defence mechanism partly affected by differences in life history traits, e.g. perennial versus annual life cycles. A major difference between annuals and perennials, affecting the evolution of resistance, is that perennials will with almost certainty encounter many different pathogens before reproduction, and that the long generation times confers problems in matching the evolutionary rates of the pathogens.

National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Functional Genomics
Identifiers
urn:nbn:se:uu:diva-177475 (URN)
Available from: 2012-07-13 Created: 2012-07-13 Last updated: 2013-06-27

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