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Article ; Online: GWAS on the Attack by Aspen Borer Saperda calcarata on Black Cottonwood Trees Reveals a Response Mechanism Involving Secondary Metabolism and Independence of Tree Architecture

Sepúlveda, Sebastián L. / Neale, David B. / Holliday, Jason A. / Famula, Randi / Fiehn, Oliver / Stanton, Brian J. / Guerra, Fernando P.

Forests. 2023 May 30, v. 14, no. 6

2023

Abstract: Black cottonwood (Populus trichocarpa) is a species of economic interest and an outstanding study model. The aspen borer (Saperda calcarata) causes irreversible damage to poplars and other riparian species in North America. The insect can produce ... ...

Abstract	Black cottonwood (Populus trichocarpa) is a species of economic interest and an outstanding study model. The aspen borer (Saperda calcarata) causes irreversible damage to poplars and other riparian species in North America. The insect can produce multiple effects ranging from the presence of some galleries in the stem to tree death. Despite the ecological and commercial importance of this tree–insect interaction, the genetic mechanisms underlying the response of P. trichocarpa to S. calcarata are scarcely understood. In this study, a common garden trial of P. trichocarpa provenances, established in Davis, California, was assessed at the second year of growth, regarding the infestation of S. calcarata from a natural outbreak. A genome-wide association study (GWAS) was conducted using 629k of exonic SNPs to assess the relationship between genomic variation and insect attack. Tree architecture, in terms of stem number per plant, and the wood metabolome were also included. Insect attack was independent of the number of stems per tree. The performed GWAS identified three significantly associated SNP markers (q-value < 0.2) belonging to the same number of gene models, encoding proteins involved in signal transduction mechanisms and secondary metabolite production, including that of R-mandelonitrile lyase, Chromodomain-helicase-DNA-binding family protein, and Leucine-rich repeat protein. These results are aligned with the current knowledge of defensive pathways in plants and trees, helping to expand the understanding of the defensive response mechanisms of black cottonwood against wood borer insects.
Keywords	Populus trichocarpa ; Saperda calcarata ; genes ; genetic variation ; genome-wide association study ; insects ; metabolism ; metabolome ; models ; plant architecture ; secondary metabolites ; signal transduction ; tree mortality ; trees ; wood ; California
Language	English
Dates of publication	2023-0530
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article ; Online
ZDB-ID	2527081-3
ISSN	1999-4907
ISSN	1999-4907
DOI	10.3390/f14061129
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Phenotypic and Genomic Local Adaptation across Latitude and Altitude in Populus trichocarpa.

Zhang, Man / Suren, Haktan / Holliday, Jason A

Genome biology and evolution

2019 Volume 11, Issue 8, Page(s) 2256–2272

Abstract: Local adaptation to climate allows plants to cope with temporally and spatially heterogeneous environments, and parallel phenotypic clines provide a natural experiment to uncover the genomic architecture of adaptation. Though extensive effort has been ... ...

Abstract	Local adaptation to climate allows plants to cope with temporally and spatially heterogeneous environments, and parallel phenotypic clines provide a natural experiment to uncover the genomic architecture of adaptation. Though extensive effort has been made to investigate the genomic basis of local adaptation to climate across the latitudinal range of tree species, less is known for altitudinal clines. We used exome capture to genotype 451 Populus trichocarpa genotypes across altitudinal and latitudinal gradients spanning the natural species range, and phenotyped these trees for a variety of adaptive traits in two common gardens. We observed clinal variation in phenotypic traits across the two transects, which indicates climate-driven selection, and coupled gene-based genotype-phenotype and genotype-environment association scans to identify imprints of climatic adaptation on the genome. Although many of the phenotype- and climate-associated genes were unique to one transect, we found evidence of parallelism between latitude and altitude, as well as significant convergence when we compared our outlier genes with those putatively involved in climatic adaptation in two gymnosperm species. These results suggest that not only genomic constraint during adaptation to similar environmental gradients in poplar but also different environmental contexts, spatial scale, and perhaps redundant function among potentially adaptive genes and polymorphisms lead to divergent adaptive architectures.
MeSH term(s)	Adaptation, Physiological ; Altitude ; Exome ; Gene Expression Regulation, Plant ; Genetics, Population ; Genome, Plant ; Genomics ; Phenotype ; Phylogeography ; Plant Proteins/genetics ; Polymorphism, Single Nucleotide ; Populus/genetics ; Transcriptome
Chemical Substances	Plant Proteins
Language	English
Publishing date	2019-07-12
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1759-6653
ISSN (online)	1759-6653
DOI	10.1093/gbe/evz151
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Forest genomics: Advancing climate adaptation, forest health, productivity, and conservation.

Isabel, Nathalie / Holliday, Jason A / Aitken, Sally N

Evolutionary applications

2019 Volume 13, Issue 1, Page(s) 3–10

Abstract: Forest ecosystems provide important ecological services and resources, from habitat for biodiversity to the production of environmentally friendly products, and play a key role in the global carbon cycle. Humanity is counting on forests to sequester and ... ...

Abstract	Forest ecosystems provide important ecological services and resources, from habitat for biodiversity to the production of environmentally friendly products, and play a key role in the global carbon cycle. Humanity is counting on forests to sequester and store a substantial portion of the anthropogenic carbon dioxide produced globally. However, the unprecedented rate of climate change, deforestation, and accidental importation of invasive insects and diseases are threatening the health and productivity of forests, and their capacity to provide these services. Knowledge of genetic diversity, local adaptation, and genetic control of key traits is required to predict the adaptive capacity of tree populations, inform forest management and conservation decisions, and improve breeding for productive trees that will withstand the challenges of the 21st century. Genomic approaches have well accelerated the generation of knowledge of the genetic and evolutionary underpinnings of nonmodel tree species, and advanced their applications to address these challenges. This special issue of Evolutionary Applications features 14 papers that demonstrate the value of a wide range of genomic approaches that can be used to better understand the biology of forest trees, including species that are widespread and managed for timber production, and others that are threatened or endangered, or serve important ecological roles. We highlight some of the major advances, ranging from understanding the evolution of genomes since the period when gymnosperms separated from angiosperms 300 million years ago to using genomic selection to accelerate breeding for tree health and productivity. We also discuss some of the challenges and future directions for applying genomic tools to address long-standing questions about forest trees.
Language	English
Publishing date	2019-12-23
Publishing country	England
Document type	Journal Article
ZDB-ID	2405496-3
ISSN	1752-4563 ; 1752-4571
ISSN (online)	1752-4563
ISSN	1752-4571
DOI	10.1111/eva.12902
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Article: A plan to diversify a transgenic blight‐tolerant American chestnut population using citizen science

Westbrook, Jared W. / Holliday, Jason A. / Newhouse, Andrew E. / Powell, William A.

Plants, people, planet. 2020 Jan., v. 2, no. 1

2020

Abstract: Over four billion American chestnut trees have been killed as a result of an introduced pathogen, the chestnut blight fungus. Recently, transgenic blight‐tolerant American chestnut trees have been produced by inserting a gene from wheat into the American ...

Abstract	Over four billion American chestnut trees have been killed as a result of an introduced pathogen, the chestnut blight fungus. Recently, transgenic blight‐tolerant American chestnut trees have been produced by inserting a gene from wheat into the American chestnut genome. Pending federal approval to use these transgenic trees for large‐scale forest restoration, this would be the first instance where a transgenic approach has been used to restore a tree species that has been rendered functionally extinct by an introduced pathogen. With the help of citizen scientists, we estimate that large‐scale forest restoration using blight‐tolerant American chestnut trees is possible within the next few decades. Summary Breeding transgenic blight‐tolerant American chestnuts with susceptible wild‐type (WT) trees is potentially an efficient method to rescue the genetic diversity and adaptive capacity of the American chestnut population for large‐scale restoration. To develop a breeding plan to diversify a transgenic blight‐tolerant population, we simulated pedigrees to estimate inbreeding coefficients and effective population size in scenarios involving outcrossing 1–4 transgenic founders to a maximum of 1,500 WT trees over 1–5 generations. We also simulated marker‐assisted introgression scenarios to minimize the extent of the transgenic founder genome, especially on the transgene carrier chromosome. Simulations suggest that the effective population size may be increased to >500, and the average inbreeding coefficient reduced to <0.01, by outcrossing a single transgenic founder over five generations to 2, 25, 50, 150, and 450 (677 total) WT parents. Three generations of marker‐assisted introgression is predicted to decrease the length of the founder genome to between 7% and 13% of the transgene carrier chromosome length as compared to 42% with event selection (ES) only. Transgenic outcross selections may be intercrossed to select progeny homozygous for the transgene for planting in seed orchards. A diversified population of transgenic blight‐tolerant American chestnut is estimated to be available for use in large‐scale forest restoration 20–35 years after federal approval to distribute the trees. In contrast, trees from earlier generations would be available almost immediately after federal approval for personal or horticultural plantings. Methods to accelerate pollen production and outcrossing are discussed.
Keywords	Castanea dentata ; chestnut blight ; chromosomes ; citizen science ; effective population size ; forest restoration ; fungi ; genetic variation ; genetically modified organisms ; homozygosity ; horticulture ; introgression ; outcrossing ; pathogens ; pollen productivity ; progeny ; transgenes ; trees ; wheat
Language	English
Dates of publication	2020-01
Size	p. 84-95.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ISSN	2572-2611
DOI	10.1002/ppp3.10061
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Targeted enrichment of the black cottonwood ( Populus trichocarpa ) gene space using sequence capture

Zhou Lecong / Holliday Jason A

BMC Genomics, Vol 13, Iss 1, p

2012 Volume 703

Abstract: Abstract Background High-throughput re-sequencing is rapidly becoming the method of choice for studies of neutral and adaptive processes in natural populations across taxa. As re-sequencing the genome of large numbers of samples is still cost-prohibitive ...

Abstract	Abstract Background High-throughput re-sequencing is rapidly becoming the method of choice for studies of neutral and adaptive processes in natural populations across taxa. As re-sequencing the genome of large numbers of samples is still cost-prohibitive in many cases, methods for genome complexity reduction have been developed in attempts to capture most ecologically-relevant genetic variation. One of these approaches is sequence capture, in which oligonucleotide baits specific to genomic regions of interest are synthesized and used to retrieve and sequence those regions. Results We used sequence capture to re-sequence most predicted exons, their upstream regulatory regions, as well as numerous random genomic intervals in a panel of 48 genotypes of the angiosperm tree Populus trichocarpa (black cottonwood, or ‘poplar’). A total of 20.76Mb (5%) of the poplar genome was targeted, corresponding to 173,040 baits. With 12 indexed samples run in each of four lanes on an Illumina HiSeq instrument (2x100 paired-end), 86.8% of the bait regions were on average sequenced at a depth ≥10X. Few off-target regions (>250bp away from any bait) were present in the data, but on average ~80bp on either side of the baits were captured and sequenced to an acceptable depth (≥10X) to call heterozygous SNPs. Nucleotide diversity estimates within and adjacent to protein-coding genes were similar to those previously reported in Populus spp., while intergenic regions had higher values consistent with a relaxation of selection. Conclusions Our results illustrate the efficiency and utility of sequence capture for re-sequencing highly heterozygous tree genomes, and suggest design considerations to optimize the use of baits in future studies.
Keywords	Poplar ; Sureselect ; Exome ; Population genomics ; Genetics ; QH426-470 ; Biology (General) ; QH301-705.5 ; Science ; Q ; DOAJ:Genetics ; DOAJ:Biology ; DOAJ:Biology and Life Sciences ; Biotechnology ; TP248.13-248.65
Language	English
Publishing date	2012-12-01T00:00:00Z
Publisher	BioMed Central
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Targeted enrichment of the black cottonwood (Populus trichocarpa) gene space using sequence capture.

Zhou, Lecong / Holliday, Jason A

BMC genomics

2012 Volume 13, Page(s) 703

Abstract: Background: High-throughput re-sequencing is rapidly becoming the method of choice for studies of neutral and adaptive processes in natural populations across taxa. As re-sequencing the genome of large numbers of samples is still cost-prohibitive in ... ...

Abstract	Background: High-throughput re-sequencing is rapidly becoming the method of choice for studies of neutral and adaptive processes in natural populations across taxa. As re-sequencing the genome of large numbers of samples is still cost-prohibitive in many cases, methods for genome complexity reduction have been developed in attempts to capture most ecologically-relevant genetic variation. One of these approaches is sequence capture, in which oligonucleotide baits specific to genomic regions of interest are synthesized and used to retrieve and sequence those regions. Results: We used sequence capture to re-sequence most predicted exons, their upstream regulatory regions, as well as numerous random genomic intervals in a panel of 48 genotypes of the angiosperm tree Populus trichocarpa (black cottonwood, or 'poplar'). A total of 20.76Mb (5%) of the poplar genome was targeted, corresponding to 173,040 baits. With 12 indexed samples run in each of four lanes on an Illumina HiSeq instrument (2x100 paired-end), 86.8% of the bait regions were on average sequenced at a depth ≥10X. Few off-target regions (>250bp away from any bait) were present in the data, but on average ~80bp on either side of the baits were captured and sequenced to an acceptable depth (≥10X) to call heterozygous SNPs. Nucleotide diversity estimates within and adjacent to protein-coding genes were similar to those previously reported in Populus spp., while intergenic regions had higher values consistent with a relaxation of selection. Conclusions: Our results illustrate the efficiency and utility of sequence capture for re-sequencing highly heterozygous tree genomes, and suggest design considerations to optimize the use of baits in future studies.
MeSH term(s)	British Columbia ; Genetic Variation ; High-Throughput Nucleotide Sequencing/methods ; Metagenomics/methods ; Northwestern United States ; Oligonucleotides/genetics ; Polymorphism, Single Nucleotide/genetics ; Populus/genetics
Chemical Substances	Oligonucleotides
Language	English
Publishing date	2012-12-14
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1471-2164
ISSN (online)	1471-2164
DOI	10.1186/1471-2164-13-703
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Frozen in time: Rangewide genomic diversity, structure, and demographic history of relict American chestnut populations

Sandercock, Alexander M. / Westbrook, Jared W. / Zhang, Qian / Johnson, Hayley A. / Saielli, Thomas M. / Scrivani, John A. / Fitzsimmons, Sara F. / Collins, Kendra / Perkins, Matthew Taylor / Craddock, James Hill / Schmutz, Jeremy / Grimwood, Jane / Holliday, Jason A.

Molecular ecology. 2022 Sept., v. 31, no. 18

2022

Abstract: American chestnut (Castanea dentata) was once the most economically and ecologically important hardwood species in the eastern United States. In the first half of the 20th century, an exotic fungal pathogen—Cryphonectria parasitica—decimated the species, ...

Abstract	American chestnut (Castanea dentata) was once the most economically and ecologically important hardwood species in the eastern United States. In the first half of the 20th century, an exotic fungal pathogen—Cryphonectria parasitica—decimated the species, killing billions of chestnut trees. Two approaches to developing blight‐resistant American chestnut populations show promise, but both will require introduction of adaptive genomic diversity from wild germplasm to produce diverse, locally adapted restoration populations. Here we characterize population structure, demographic history, and genomic diversity in a range‐wide sample of 384 wild American chestnuts to inform conservation and breeding with blight‐resistant varieties. Population structure analyses suggest that the chestnut range can be roughly divided into northeast, central, and southwest populations. Within‐population genomic diversity estimates revealed a clinal pattern with the highest diversity in the southwest, which likely reflects bottleneck events associated with Quaternary glaciation. Finally, we identified genomic regions under positive selection within each population, which suggests that defence against fungal pathogens is a common target of selection across all populations. Taken together, these results show that American chestnut underwent a postglacial expansion from the southern portion of its range leading to three extant genetic populations. These populations will serve as management units for breeding adaptive genetic variation into the blight‐resistant tree populations for targeted reintroduction efforts.
Keywords	Castanea dentata ; fungi ; genetic variation ; genomics ; germplasm ; glaciation ; hardwood ; population structure ; trees
Language	English
Dates of publication	2022-09
Size	p. 4640-4655.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	1126687-9
ISSN	1365-294X ; 0962-1083
ISSN (online)	1365-294X
ISSN	0962-1083
DOI	10.1111/mec.16629
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Frozen in time: Rangewide genomic diversity, structure, and demographic history of relict American chestnut populations.

Sandercock, Alexander M / Westbrook, Jared W / Zhang, Qian / Johnson, Hayley A / Saielli, Thomas M / Scrivani, John A / Fitzsimmons, Sara F / Collins, Kendra / Perkins, Matthew Taylor / Craddock, James Hill / Schmutz, Jeremy / Grimwood, Jane / Holliday, Jason A

Molecular ecology

2022 Volume 31, Issue 18, Page(s) 4640–4655

Abstract: American chestnut (Castanea dentata) was once the most economically and ecologically important hardwood species in the eastern United States. In the first half of the 20th century, an exotic fungal pathogen-Cryphonectria parasitica-decimated the species, ...

Abstract	American chestnut (Castanea dentata) was once the most economically and ecologically important hardwood species in the eastern United States. In the first half of the 20th century, an exotic fungal pathogen-Cryphonectria parasitica-decimated the species, killing billions of chestnut trees. Two approaches to developing blight-resistant American chestnut populations show promise, but both will require introduction of adaptive genomic diversity from wild germplasm to produce diverse, locally adapted restoration populations. Here we characterize population structure, demographic history, and genomic diversity in a range-wide sample of 384 wild American chestnuts to inform conservation and breeding with blight-resistant varieties. Population structure analyses suggest that the chestnut range can be roughly divided into northeast, central, and southwest populations. Within-population genomic diversity estimates revealed a clinal pattern with the highest diversity in the southwest, which likely reflects bottleneck events associated with Quaternary glaciation. Finally, we identified genomic regions under positive selection within each population, which suggests that defence against fungal pathogens is a common target of selection across all populations. Taken together, these results show that American chestnut underwent a postglacial expansion from the southern portion of its range leading to three extant genetic populations. These populations will serve as management units for breeding adaptive genetic variation into the blight-resistant tree populations for targeted reintroduction efforts.
MeSH term(s)	Demography ; Fagaceae/genetics ; Fagaceae/microbiology ; Genomics ; Plant Breeding ; Plant Diseases/genetics ; Plant Diseases/microbiology ; Trees/microbiology
Language	English
Publishing date	2022-08-14
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1126687-9
ISSN	1365-294X ; 0962-1083
ISSN (online)	1365-294X
ISSN	0962-1083
DOI	10.1111/mec.16629
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Exome Resequencing Reveals Evolutionary History, Genomic Diversity, and Targets of Selection in the Conifers Pinus taeda and Pinus elliottii.

Acosta, Juan J / Fahrenkrog, Annette M / Neves, Leandro G / Resende, Márcio F R / Dervinis, Christopher / Davis, John M / Holliday, Jason A / Kirst, Matias

Genome biology and evolution

2019 Volume 11, Issue 2, Page(s) 508–520

Abstract: Loblolly pine (Pinus taeda) and slash pine (Pinus elliottii) are ecologically and economically important pine species that dominate many forest ecosystems in the southern United States, but like all conifers, the study of their genetic diversity and ... ...

Abstract	Loblolly pine (Pinus taeda) and slash pine (Pinus elliottii) are ecologically and economically important pine species that dominate many forest ecosystems in the southern United States, but like all conifers, the study of their genetic diversity and demographic history has been hampered by their large genome size. A small number of studies mainly based on candidate-gene sequencing have been reported for P. taeda to date, whereas none are available for P. elliottii. Targeted exome resequencing has recently enabled population genomics studies for conifers, approach used here to assess genomic diversity, signatures of selection, population structure, and demographic history of P. elliottii and P. taeda. Extensive similarities were revealed between these species: both species feature rapid linkage disequilibrium decay and high levels of genetic diversity. Moreover, genome-wide positive correlations for measures of genetic diversity between the species were also observed, likely due to shared structural genomic constraints. Also, positive selection appears to be targeting a common set of genes in both pines. Demographic history differs between both species, with only P. taeda being affected by a dramatic bottleneck during the last glacial period. The ability of P. taeda to recover from a dramatic reduction in population size while still retaining high levels of genetic diversity shows promise for other pines facing environmental stressors associated with climate change, indicating that these too may be able to adapt successfully to new future conditions even after a drastic population size contraction.
MeSH term(s)	Biological Evolution ; Computer Simulation ; Genetic Variation ; Linkage Disequilibrium ; Ovule/chemistry ; Pinus taeda/genetics ; Population Dynamics ; Selection, Genetic
Language	English
Publishing date	2019-01-28
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1759-6653
ISSN (online)	1759-6653
DOI	10.1093/gbe/evz016
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Divergent selection and heterogeneous migration rates across the range of Sitka spruce (Picea sitchensis)

Holliday, Jason A / Suren, Haktan / Aitken, Sally N

Proceedings. Biological sciences. 2012 May 7, v. 279, no. 1734

2012

Abstract: Gene flow and effective population size (Ne) should depend on a population's position within its range: those near the edges are expected to have smaller Ne and lower relative emigration rates, whereas those nearer the centre should have larger Ne and ... ...

Abstract	Gene flow and effective population size (Ne) should depend on a population's position within its range: those near the edges are expected to have smaller Ne and lower relative emigration rates, whereas those nearer the centre should have larger Ne and higher relative emigration rates. In species with continuous ranges, this phenomenon may limit the ability of peripheral populations to respond to divergent selection. Here, we employ Sitka spruce as a model to test these predictions. We previously genotyped 339 single nucleotide polymorphisms (SNPs) in 410 individuals from 13 populations, and used these data to identify putative targets of divergent selection, as well as to explore the extent to which central–peripheral structure may impede adaptation. Fourteen SNPs had outlier FST estimates suggestive of divergent selection, of which nine were previously associated with phenotypic variation in adaptive traits (timing of autumn budset and cold hardiness). Using coalescent simulations, we show that populations from near the centre of the range have higher effective populations sizes than those from the edges, and that central populations contribute more migrants to marginal populations than the reverse. Our results suggest that while divergent selection appears to have shaped allele frequencies among populations, asymmetrical movement of alleles from the centre to the edges of the species range may affect the adaptive capacity of peripheral populations. In southern peripheral populations, the movement of cold-adapted alleles from the north represents a significant impediment to adaptation under climate change, while in the north, movement of warm-adapted alleles from the south may enhance adaptation.
Keywords	Picea sitchensis ; alleles ; autumn ; climate change ; cold tolerance ; gene flow ; gene frequency ; phenotypic variation ; population size ; prediction ; single nucleotide polymorphism
Language	English
Dates of publication	2012-0507
Size	p. 1675-1683.
Publishing place	Royal Society
Document type	Article
ZDB-ID	209242-6
ISSN	1471-2954 ; 0080-4649 ; 0962-8452 ; 0950-1193
ISSN (online)	1471-2954
ISSN	0080-4649 ; 0962-8452 ; 0950-1193
Database	NAL-Catalogue (AGRICOLA)

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