Source: PENNSYLVANIA STATE UNIVERSITY submitted to
BIOLOGICAL IMPROVEMENT OF CHESTNUT THROUGH TECHNOLOGIES THAT ADDRESS MANAGEMENT OF THE SPECIES, ITS PATHOGENS AND PESTS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
1000326
Grant No.
(N/A)
Project No.
PEN04532
Proposal No.
(N/A)
Multistate No.
NE-1333
Program Code
(N/A)
Project Start Date
Oct 1, 2013
Project End Date
Sep 30, 2018
Grant Year
(N/A)
Project Director
Carlson, JO, E..
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Ecosystem Science & Management
Non Technical Summary
This research addresses the issue of restoration of American chestnut through transfer of blight-resistance genes from Chinese chestnut into American chestnut by back-cross breeding. Our roles and approaches in this project are 1) to discover the genes for blight-resistance in Chinese chestnut through genome sequencing, 2) to develop DNA markers in the blight-resistance genes to accelerate the back-cross breeding efforts; 3) to establish additional seed orchards for adaptation of blight-resistant American chestnut to local environments; and 4) to disseminate knowledge of the American chestnut restoration efforts through scientific reports and extension products.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
20106991080100%
Goals / Objectives
Develop and evaluate blight resistant chestnuts for food and fiber through traditional and molecular approaches that incorporate knowledge of the chestnut genome, Investigate chestnut reestablishment in orchard and forest settings with special consideration of the current and historical knowledge of the species and its interaction with other pests and pathogens.
Project Methods
The Carlson lab is developing a reference sequence for the Chinese chestnut (Castanea mollissima) genome using a whole genome sequencing approach based on next generation sequencing technologies. The genome will be assembled and genes identified using bioinformatics software programs. The genes for blight resistance will be identified by a detailed examination of genes in the genome sequenced for the three loci know to impart blight resistance in Chinese chestnut. The results of genes for blight resistance gene identification will be evaluated through transfer or potential disease resistance genes to collaborators who will test the genes in transgenic plants. DNA markers will be evaluated in chestnut breeding programs. Micsky and co-workers will establish new chestnut orchards and evaluate chestnut seedlings from the orchards for vigor and survival in Site Assessment Plots. In addition, Micsky's extension education program will include outreach to new audiences through training workshops, field experiences, extension newsletters, grower/site evaluations, and pest surveys.

Progress 10/01/13 to 09/30/18

Outputs
Target Audience:Our target audiences are the general scientific community, public research institutes, foundations, tree growers, forest landowners, and the general public interested in tree improvement, especially The American Chestnut Foundation and the USDA Forest Service, the PA Bureau of Forestry, and other collaborators. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has contributed to the training in the Carlson lab of 8 undergraduate students (Maureen Mailander in Arboriculture, Krystle Swartz in Animal Science, Lianna Johnson in Ecosystem Resource Management, Alex Stanish in Horticulture, Byron Bredael in Horticulture, Ethan Mansfield in Forest Biology, Jeffrey Osborne in Forest Biology, and Chelsea Kylerin Forest Biology). This project also contributed to the dissertation theses of 6 graduate students in the Carlson lab (Wanyan Wang, Plant Biology; Di Wu, Forestry; Erin Scully, Genetics; Josh Herr, Plant Biology; T. Casey Weathers, Wildlife and Fisheries Science; and Nathaniel Cannon, Bioinformatics and Genomics) four of whom have earned their degrees to date. This project also contributed to the training in the Carlson lab of 3 post-doctoral fellows (Dongwhan Shim, Charles Addo-Quaye, and Teodora Best). Two research technicians also received training and employment during his project (Tyler Wagner and Nicole Zembower). How have the results been disseminated to communities of interest?The results of the project were disseminated through publications in well-respected peer-reviewed science journals, extension education materials, through invited lectures, in presentations at annual meetings of the NE-1333 USDA multi-state research project, at The American Chestnut Foundation Annual Meeting, and the international Plant and Animal Genome Conference. The results from genomics studies have also been reported to the research community through deposit of data at the NCBI GenBank database and at our own https://hardwoodgenomics.org/ public database. A noteworthy example of our efforts to disseminate results was through hosting The American Chestnut Foundation's 2015 annual meeting (by The Schatz Center for Tree Molecular Genetics) at the Penn State's conference center on October 23 and 24, 2015. The focus of the meeting was to update the TACF membership on the status of and discoveries from chestnut genomics, and plans for integrating the genome resources into TACF advanced breeding efforts. Excellent keynote talks were presented by Antoine Kremer and Ronald Sederoff on the history of forest tree genomics and biotechnology. Talks on the state of genomics with chestnut and other Fagaceae species were presented by Albert Abbott, Catherine Bodénès, Nathaniel Cannon. John Carlson, Rita Costa, Angus Dawe, Jason Holliday, Nurul Islam-Faridi, Scott Merkle, C. Dana Nelson, William Powell, Jeanne Romero-Severson, Margaret Staton, Jared Westbrook, and Isacco Beritognolo for Fiorella Villani. Over 200 people attended, and the TACF membership uniformly expressed their sincere appreciation to all of the speakers. The meeting also included hands-on workshops on chestnut DNA extraction and use of the chestnut genome browsers, along with a tour of Sara Fitzsimmons' and Kim Steiner's BC3 trial in the Arboretum at Penn State. Finally, a discussion forum was held that brought together chestnut genomics researchers and TACF members to discuss next steps in use of genomics tools in the breeding and reforestation efforts. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? I. Chestnut Genome Sequencing Project Activities(John Carlson,Penn State University) During the five-year project, the first version of the Chinese chestnut genome was sequenced and assembled and released to the public in January 2014 at the website https://hardwoodgenomics.org/chinese-chestnut-genome, developed and curated by Margaret Staton at the University of Tennessee - Knoxville. The version 1.1 genome assembly was produced for the TACF cultivar Vanuxem. It comprised 724.4 Mb in 41,270 scaffolds, averaging app. 40,000 bp in length. This represents at least 91% of the Chinese chestnut genome, based on estimates from pre-sequencing era studies. A total of 36,146 likely genes were identified. In addition, DNA clones physically spanning the 3 blight resistance QTL were separately sequenced and assembled into a total of 395 scaffolds covering 13.8 Mb. Over 1,900 genes were found in the QTLs, including 194 known stress-response genes, from which 15 candidate genes for blight resistance were selected for further study. The genome browser and the QTL browser website has had thousands of visits from across the globe, for gene searches and scaffold, gene, transcripts and predicted protein data downloads. The version 1.1 Chinese chestnut genome was used in various studies which demonstrated the power provided by a genome reference, including genotyping and assessing genetic variation among accessions, species, and breeding material in the CAES and TACF orchards. For example, in one study, relatively shallow (10X) depth of DNA sequence data was produced for one C. alnifolia genotype, one C. crenata genotype, five C. dentata genotypes, one C. henryii genotype (Chinese chinkapin), four C. mollissima genotypes, one C. ozarkensis genotype, one C. sativa genotype, one C. seguinii genotype, three third backcross hybrids from the TACF breeding program, and the BC3 C. dentata x C. mollissima parental genotypes - B3119 and B3176. Alignment of the parental and BC3 genotype genome sequences to the Vanuxem reference genome clearly revealed a separation of Chinese, American and the intermediate F1 hybrid genomes, as well as the transitional nature of BC3 genomes. In another important study recently published by LaBonte, et al. (2018), our version 1.1 genome was used as the reference to detect signatures of selection in the Chinese Chestnut genome which predicted genes potentially related to flower phenology and development, fruit maturation, and secondary metabolism, and included some genes homologous to domestication genes in other woody plants. These candidate genes may prove useful in chestnut improvement. For application of the chestnut reference genome in Genome-Wide-Selection to advance back-cross breeding and disease resistance introgression programs, chromosome-scale sequences assemblies of scaffolds are required. We thus worked for the past four years on producing an improved 'version 2' of the Chinese chestnut genome with proper gene order and approximates length at the chromosome-scale. The available approach to accomplish this involved bridging and merging scaffolds using longer genome sequences followed by anchoring large scaffolds to positions on genetic linkage maps using DNA marker sequences. Taking this approach, we first reduced the number of scaffolds to 14,358, covering 784Mb of genome sequence (app. 98% of the estimated genome size) based on BAC-end sequences distributed across the physical length of the genome (Kubisiak et al, 2013b). The 5,745 largest scaffolds were anchored to the integrated genetic-physical map for Chinese chestnut (Kubisiak et al, 2013a), producing a set of 12 "pseudo-chromosome" sequences. However, the Vanuxem pseudo-chromosome sequence assemblies were not highly consistent with the order of loci on several, high-density genetic linkage maps produced by Tatyana Zhebentyayeva for BC3F2 families. In the past year, funding from a USDA NIFA grant with TACF allowed us to generate very long genome sequences by the PACBio technology for bridging scaffolds and closing gaps, reducing the number of genome scaffolds to 12,684, covering 784 Mb (~98% of genome). New pseudo-chromosome sequences were assembled by anchoring 4,314 of the scaffolds to DNA markers in the reference genetic map for Vanuxem. We also produced 8 Gbases of new RNA sequence data from tissues of the Vanuxem reference genotype to aid Margaret Staton's group in finding and annotating genes in the new pseudo-chromosomes. This new assembly, referred to as Version 3.0, will be released to the public as a new genome browser at the Hardwood Genomics website and a peer-reviewed publication, which will include gene positions, where RNAs have been mapped, and organization relative to other chestnut maps and tree genomes. II. Breeding and field trials (Kim Steiner, Penn State University): Dr. Steiner has a long-time partnership with The American Chestnut Foundation on breeding for blight-resistance in American chestnut and on research towards restoring the species to Appalachian forests. TACF's Northcentral Regional Breeding Coordinator is based in the Steiner lab, and the Pennsylvania TACF Chapter's statewide and regional breeding programs have been coordinated by Steiner's PhD student S.F. Fitzsimmons. Dr. Steiner and Sara Fitzsimmons have established a large field trial, on the Penn State campus, of many families of TACF 3rd back-cross generation progeny continue to being evaluated for blight resistance and form. Dr. Steiner has also provided oversight to TACF breeding, restoration, and research efforts as Chair of the Science Cabinet from 2007 to 2012, and currently as Chair of the TACF Board of Directors. III. Wood phenotyping and extension (Charles Ray, Penn State University): A wood sample collection was started in 1909 with H. J. Heltman's collection of specimens from 48 tree species on the Mont Alto campus. In 1956, wood importer Joseph Stearns made a major donation of wood specimens (reportedly between 2,400 and 2,500). To accommodate the larger collection, the then-School of Forest Resources acquired a large cabinet with hundreds of drawers to hold the specimens. Wood technology professor Newell Norton documented part of the 32 different donated collections within the Penn State collection. Dr. Ray and his staff are taking high-resolution, magnified photos of the app. 18,000 specimens in the current "Xylarium" (wood collection), with the intent to make the photos available online, and to make the collection easily accessible to researchers studying the genetics and molecular properties of wood. This collection includes chestnut wood samples from various sources, which is already serving as a reference for researchers and TACF members. We hope that the chestnut wood collection will be supplemented with additional material from NE colleagues and other chestnut enthusiasts.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Scully E., Geib SM, Mason CJ, Carlson JE, Tien M, Chen H-Y, Harding S, Tsai C-J, Hoover K. 2018. Host-plant induced changes in microbial community structure and midgut gene expression in an invasive polyphage (Anoplophora glabripennis) Scientific Reports, 8(1), p.9620, 16 pages.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Steiner, K.C., Westbrook, J.W., Hebard, F.V., Georgi, L.L., Powell, W.A. and Fitzsimmons, S.F., 2017. Rescue of American chestnut with extraspecific genes following its destruction by a naturalized pathogen. New Forests, 48(2), pp.317-336.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Steiner, K., 2017. Genetic differences in resistance of Scotch pine to eastern pineshoot borer. The Great Lakes Entomologist, 7(4), p.2.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Steiner, K.C., Stein, B.S. and Finley, J.C., 2018. A test of the delayed oak dominance hypothesis at mid-rotation in developing upland stands. Forest Ecology and Management, 408, pp.1-8.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: John Carlson, Update on the Chinese Chestnut Genome Project. USDA Multi-state Project NE-1333 Annual Meeting, Pennsylvania State University, University Park, PA, September 7, 2018.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Wanyan Wang, John E. Carlson, Eric S. Fabio, Lawrence B. Smart, 2018, Plant-Microbe Communication in the Shrub Willow Rhizosphere: Microbiome Structure, Function and Crop Yield, Plant and Animal Genome XXVI Conference, San Diego, CA, Phytobiome workshop, Jan. 17, 2018.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2018 Citation: Di Wu, Jennifer Koch, Mark V. Coggeshall, Nicole Zembower, John E. Carlson, 2018, A genetic linkage map for Fraxinus pennsylvanica and synteny analysis with Asterid and Rosid species, Plant and Animal Genome XXVI Conference, San Diego, CA, Jan. 13-17, 2018, poster.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Carlson, JE, Staton, ME; Addo-Quaye, C; Cannon, N; Tomsho, LP; Ficklin, S, Saski, C, Zhebentyayeva, T, Burhans, R, Drautz, D, Islam-Faridi, N, Wagner, TK, Zembower, N, Schuster, SC, Abbott, AG, Westbrook, J, Georgi, L, Holliday, J, Dana, NC, Hebard, FV, 2017, The Chinese Chestnut Genome Project, IUFRO Genomics and Genetics of Fagaceae Conference, Shanghai Botanic Gardens, Shanghai, China, Nov. 1  3, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Wanyan Wang, Craig Carlson, Eric S. Fabio, Larry Smart, and John Carlson, 2017, Genotype-by-Environment Interactions: Insect Herbivore  Shrub Willow Genotype Interactomes, and Soil Microbe Community  Shrub Willow Genotype Interactomes, Mid-Atlantic Bioenergy Expo, Sept. 14, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: John Carlson, 2017, Update on the Chinese Chestnut Genome Project. USDA Multi-state Project NE-1333 Annual Meeting, Maggie Valley, NC, September 8, 2017.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Wanyan Wang, John E. Carlson, Lawrence B. Smart, and Craig H. Carlson, 2017, Transcriptome Analysis of Resistance of Shrub Willow to Empoasca fabae, Plant and Animal Genome XXV Conference, San Diego, CA, Jan. 14-18, 2017, poster abstract P0250.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Di Wu, Thomas Lane, Teodora Orendovici-Best, Nicole Zembower, Margaret Staton, Jennifer Koch, John McGraw, Stephan C. Schuster, Kim C. Steiner and John E. Carlson, 2017, Genome Mapping, Tagging & Characterization: Forest Trees Intra - Species Variation in Green Ash Response to an Invasive Insect, Plant and Animal Genome XXV Conference, San Diego, CA, Jan. 14-18, 2017, poster abstract P0593.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Nathaniel Cannon, Margaret E. Staton, Charles Addo-Quaye, Nurul Islam-Faridi, Lynn P. Tomsho, Stephen Ficklin, Chris Saski, Richard Burhans, Daniela Drautz, Nicole Zembower, Stephan C. Schuster, Albert G. Abbott, C. Dana Nelson, Frederick V. Hebard, John E. Carlson, 2017, The Physical and Genetic Structure of The Chinese Chestnut (Castanea Mollissima) Genome, Plant and Animal Genome XXV Conference, San Diego, CA, Jan. 14-18, 2017, poster abstract.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2017 Citation: Irina Calic, Jennifer Koch, David Carey, Charles Addo-Quaye, John E. Carlson, and David B. Neale, 2017, Genome Mapping, Tagging & Characterization: Forest Trees Genome -Wide Association Study Identifies a Major Gene for Beech Bark Disease Resistance in American Beech Tree (Fagus grandifoliaEhrh.), Plant and Animal Genome XXV Conference, San Diego, CA, Jan. 14-18, 2017, poster abstract P0592.
  • Type: Theses/Dissertations Status: Accepted Year Published: 2018 Citation: Di Wu, Intraspecific Variation In Green Ash Response To An Invasive Insect, A Dissertation in Bioinformatics and Genomics, The Graduate School, Intercollege Program in Integrative Biosciences, The Pennsylvania State University, August 2018.
  • Type: Theses/Dissertations Status: Accepted Year Published: 2018 Citation: Wanyan Wang, Genomics Of Genotype-By-Environment Interactions In Shrub Willow (Salix Spp.): Insect Herbivory And Soil Microbiomes, The Graduate School, The Pennsylvania State University, Intercollege Program in Plant Biology, May 2018.
  • Type: Books Status: Submitted Year Published: 2018 Citation: Merkle SA, Vieitez FJ, Corredoira E, Carlson JE, In press, Castanea spp. Chestnut. In R. Litz, F. Alfaro, & J. Hormaza (Eds.), Biotechnology of Fruit and Nut Crops (2nd ed.). CAB International, submitted September 12, 2017.
  • Type: Journal Articles Status: Submitted Year Published: 2018 Citation: Di Wu, Jennifer Koch, Mark Coggeshall, and John Carlson, The first genetic linkage map for Fraxinus pennsylvanica and syntenic relationships with four related species submitted August 13, 2018, to Plant Molecular Biology, Manu # PLAN-S-18-00440.
  • Type: Journal Articles Status: Submitted Year Published: 2018 Citation: Tuskan, GA, A Groover, J Schmutz, SP DiFazio, A Myburg, D Grattapaglia, LB Smart, TM Yin, J-M Aury, A Kremer, T Leroy, G Le Provost, C Plomion, J Carlson, J Randall, J Westbrook, J Grimwood, W Muchero, D Jacobson, J Mitchener, Hardwood tree genomics: Unlocking woody plant biology, Submitted May 11, 2018, to Frontiers in Plant Science, section Plant Biotechnology. Manuscript # 396811.


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:Target audiences are the general scientific community, public research institutes, foundations, tree growers, forest landowners, and the general public interested in tree improvement, especially The American Chestnut Foundation and the USDA Forest Service, the PA Bureau of Forestry, and other collaborators. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Three PhD students and several undergraduate students have been involved in aspects of this project, inlcuding assembly of the chinese chestmut genome. How have the results been disseminated to communities of interest?The results of the project are disseminated throuh publication in well-respected science journals and at annual meetings of the NE-1333 USDA multi-state prject and The Amercian Chestnut Foundation and the Plant and Animal Genome Conference. What do you plan to do during the next reporting period to accomplish the goals? The Chinese chestnut pseudochromosome sequences will be released to the public for browsing and downloading at the Hardwood Genomics website - https://hardwoodgenomics.org/chinese-chestnut-genome We will submit a refereed journal article on Chinese chestnut reference genome to a high visibility, highly respected research journal (in preparation).

Impacts
What was accomplished under these goals? Version 1.1 of the Chinese chestnut genome is still available to the public at the website https://hardwoodgenomics.org/chinese-chestnut-genome, created and curated by colleague Margaret Staton at the University of Tennessee-Knoxville. The version 1.1 genome assembly (cv. Vanuxem) consists of 724.4 Mb in 41,270 scaffolds, averaging app. 40,000 bp in length. A total of 36,146 gene models and 38,146 peptide sequences were predicted in the genome. BAC contigs spanning the 3 blight resistance QTL (identified in the early F2 QTL mapping population) were also sequenced and assembled into 395 scaffolds. A total of 1,952 genes were predicted within the 3 QTLs, including 194 known stress-response genes, from which 15 candidate genes for blight resistance were selected for further study, based on gene expression data. The anticipated public release of the improved and validated version 2 of the Chinese chestnut genome, is pending journal publication. This assembly consists of 14,358 scaffolds representing 784Mb of genome sequence, almost the estimated genome size. The integrated genetic and physical map was used to distill the 14,358 scaffolds into 12 "pseudo"-chromosome sequences, representing the 12 linkage groups and providing 98% genome coverage. The arrangement of scaffolds in the pseudo-chromosome sequences has been validated by comparison to the order of thousands of DNA markers on new high density genetic linkage maps produced at Clemson, and by comparison to very long PACBio technology genome sequences, with support from a USDA grant awarded to TACF. Jason Holiday's lab at VA Tech University produced RNA sequence data from 9 tissues from grafted clones of the Vanuxem reference genotype, which we have mapped to the new pseudo-chromosomes. All but a few of computer-predicted gene models were validated. The Chinese chestnut genome was used as a reference to genotype, and assess genetic variation, at the DNA level among 18 genotypes. Alignment of parental and BC3 genotype genome sequences to the Vanuxem reference genome revealed varying extents of transition of the BC3 genomes towards the American genome content from backcrossing. A similar, but more extensive study of genome sequence variation within and among chestnut species has been conducted in the lab Keith Woeste in the HTIRC at Purdue University.

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Islam-Faridi N, Majid MA, Zhebentyayeva T, Georgi LL, Fan S, Hebard V, Sisco PH, Westbrook J, Carlson JE, Abbott AG, Nelson CD. 2016. FISH Confirmation of a Reciprocal Translocation in Chestnut. In Cytogenetic And Genome Research 2016 Jan 1, Vol. 148, No. 2-3, pp. 144-144, Allschwilerstrasse 10, Ch-4009 Basel, Switzerland: Karger.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Nelson, C., Powell, W., Merkle, S., Carlson, J., Staton, M., Nairn, C., Holliday, J., Westbrook, J., Georgi, L. and Hebard, F., 2016, Shovel-ready trees: Forest Health Initiative a model for rapid development and deployment of disease resistant trees. In Phytopathology (Vol. 106, No. 12, Pp. 170-170). 3340 Pilot Knob Road, St Paul, Mn 55121 USA: American Phytopathological Society.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Harmon M, Lane T, Staton M, Coggeshall MV, Best T, Chen CC, Liang H, Zembower N, Drautz-Moses DI, Hwee YZ, Schuster SC, Schlarbaum SE, Carlson JE, and Gailing O. 2017. Development of novel genic microsatellite markers from transcriptome sequencing in sugar maple (Acer saccharum Marsh.). BMC Research Notes, 10(1), p.369.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: ?ali? I, Koch J, Carey D, Addo-Quaye C, Carlson JE, Neale DB, 2017. Genome-wide association study identifies a major gene for beech bark disease resistance in American beech (Fagus grandifolia Ehrh.). BMC genomics, 18(1), p.547.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Wu, Y., Zhang, R., Staton, M., Schlarbaum, S., Coggeshall, M., Romero-Severson, J., Carlson, J., Liang, H., Xu, Y., Drautz-Moses, D., Schuster, S., Gailing, O. 2017. Development of genic and genomic microsatellites in Gleditsia triacanthos L. (Fabaceae) using Illumina sequencing. Annals of Forest Research 60(2), DOI:10.15287/afr.2017.819
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Konar A, Choudury O, Bullis R, Fiedler L, Kruser J, Stephens M, Gailing O, Schlarbaum S, Coggeshall MV, Staton ME, Carlson JE, Emrich S, Romero-Severson J. 2017. High-quality genetic mapping with ddRADseq in the non-model tree Quercus rubra. BMC Genomics, 18(1):417, 12 pages.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Gailing O, Staton ME, Lane T, Schlarbaum SE, Nipper R, Owusu SA, and Carlson JE. 2017. Construction of a Framework Genetic Linkage Map in Gleditsia triacanthos L. Plant Molecular Biology Reporter, Volume 35(2): 177187.


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:Our target audiences are the general scientific community, public research institutes, foundations, tree growers, forest landowners, state and federal researchers, and the general public interested in tree improvement, especially The American Chestnut Foundation and the USDA Forest Service, the PA Bureau of Forestry, and other collaborators. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?The 2015 annual meeting of The American Chestnut Foundation was hosted by The Schatz Center for Tree Molecular Genetics and held at the Penn State conference center on October 23 and 24, 2015. The focus of the meeting was to update the TACF membership on the status of and discoveries from chestnut genomics, and plans for integrating the genome resources into TACF advanced breeding efforts. Excellent keynote talks were presented by Antoine Kremer and Ronald Sederoff on the history of forest tree genomics and biotechnology. Talks on the state of genomics with chestnut and other Fagaceae species were presented by Albert Abbott, Catherine Bodénès, Nathaniel Cannon. John Carlson, Rita Costa, Angus Dawe, Jason Holliday, Nurul Islam-Faridi, Scott Merkle, C. Dana Nelson, William Powell, Jeanne Romero-Severson, Margaret Staton, Jared Westbrook, and Isacco Beritognolofor Fiorella Villani. Over 200 people attended, and the TACF membership uniformly expressed their sincere appreciation to all of the speakers. The meeting also included hands-on workshops on chestnut DNA extraction and use of the chestnut genome browsers, along with a tour of Sara Fitzsimmons' and Kim Steiner's BC3 trial in the Arboretum at Penn State. Finally, a discussion forum was held that brought together chestnut genomics researchers and TACF members to discuss next steps in use of genomics tools in the breeding and reforestation efforts. What do you plan to do during the next reporting period to accomplish the goals?Work in the coming year will focus on: 1)Validatingand improvingthe Chinese chestnut pseudochromosome sequences using very long genome sequences produced from the PacBio single molecule sequencing technology (USDA AFRI grant). 2)Obtain deep RNA sequence data from several tissues of Chinese chestnut cv. Vanuxem to refine the identification and annotation of genes in the reference genome. 3)Submit refereed journal article on Chinese chestnut reference genome.

Impacts
What was accomplished under these goals? Goal (1) Develop and evaluate blight resistant chestnuts for food and fiber through traditional and molecular approaches that incorporate knowledge of the chestnut genome: Version 1 of the Chinese chestnut genome has been available to the public since January 2014 at the website http://www.hardwoodgenomics.org/content/tools, curated by Margaret Staton at the University of Tennessee - Knoxville. The version 1 genome assembly (for TACF cv. Vanuxem) consisted of 724.4 Mb in 41,270 scaffolds, averaging app. 40,000 bp in length. A total of 36,146 gene models and 38,146 peptide sequences were machine-predicted, with gene expression support. In addition, BAC contigs spanning the 3 blight resistance QTL (identified in the early F2 QTL mapping population) were sequenced and assembled into a total of 395 scaffolds. A total of 1,952 genes were predicted and annotated in the QTLs, including 194 known stress-response genes, from which 15 candidate genes for blight resistance were selected for further study. The website has had thousands of visits from across the globe for use of the genome browser and the QTL browser, and for searches and downloads of data from the scaffolds, gene models, predicted transcripts and predicted proteomes databases there. (bigger pieces averaging ~40K bp) We will soon release an improved and validated version 2 of the Chinese chestnut genome, for which the assembly consists of only 14,358 scaffolds representing 784Mb of genome sequence, or app. 98% of the estimated genome size. The 5,745 largest scaffolds were anchored to the integrated genetic-physical map to produce a set of 12 pseudo-chromosome sequences, representing the 12 linkage groups and providing 798 Mbp (98%) of genome coverage. The predicted gene positions have been transferred over to the pseudo-chromosomes, as well as the previously assembled QTL sequences. The arrangement of scaffolds in the pseudo-chromosome sequence assemblies has been validated by comparison to the order of thousands of DNA markers on new high density genetic linkage maps produced by Tatyana Zhebentyayeva at Clemson. We also await the production of very long genome sequences by the PACBio technology for further validation and gap closing. PACBio data generation is supported by a new USDA AFRI program grant that was awarded to TACF during the past reporting period. Vanuxem genomic DNA was prepared several times at PSU, but did not meet Washington State University PACBio service lab standards. Vanuxem leaves were collected from a tarp-shaded branch and sent in June from TACF to Arizona Genomics Institute for DNA extraction by their PACBio sequencing support staff, which proved successful. Presently we are in a queue for PACBio sequencing at Arizona Genomics Institute in February. To test the value of the chestnut reference genome for use in genetic variation studies and in Genome-Wide-Selection in the TACF breeding program, we produced app. 10X depth sequence data in 2015 for the following chestnut genotypes from CAES and TACF orchards: one C. alnifolia genotype, one C. crenata genotype, five C. dentata genotypes (GMBig, Ted Farm A, Alex R, Huan Row1Tree18(MK5), and Ellis 1), one C. henryii genotype (Chinese chinkapin), four C. mollissima genotypes (Mahogany, Nanking, PA Fat Camp, and PA Stone Valley), one C. ozarkensis genotype, one C. sativa genotype, one C. seguinii genotype, three third backcross hybrids from the TACF breeding program (from parents B3119 x B3176), and the BC3 C. dentata x C. mollissima parental genotypes - B3119 and B3176. Alignment of the parental and BC3 genotype sequences to the Vanuxem reference genome provided a very clear display of the varying extents of transition of the genomes towards American genome content as a result if the backcrossing process. These results were presented at the TACF annual meeting in October 2015. Jason Holiday and Jared Westbrook are now developing a Genome-Wide-Selection Model for use in the TACF breeding program, with funding from USDA. The Staton group produced a set of potentially diagnostic 714,039 SNPs supported by sequencing from all three American genotypes for use in developing the GWS model(s).

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Lane T, Best T, Zembower N, Davitt J, Henry N, Xu Y, Koch J, Liang H, McGraw J, Schuster S, Shim D, Coggeshall M, Carlson JE, Staton ME. 2016. The green ash transcriptome and identification of genes responding to abiotic and biotic stresses. BMC Genomics 17:702, 16 pages.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Carroll RA, Jones C, Best T, Shumaker K, Carlson J. 2016. Gene expression in hardwood trees species exposed to ozone. Journal of Undergraduate Research and Scholarly Excellence, Volume VII: 32-35.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Owusu S, Schlarbaum S, Carlson J, Gailing O. 2016. Pollen gene flow and molecular identification of full-sib families in small and isolated population fragments of Gleditsia triacanthos L. Botany, 94: 523532.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Herr JR, Scully ED, Geib SM, Hoover K, Carlson JE, Geiser DM. 2016. Genome sequence of Fusarium isolate MYA-4552 from the midgut of Anoplophora glabripennis, an invasive, wood-boring beetle. Genome Announcements 4(4):e00544-16, 2 pages.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Staton ME, Best TO, Khodwekar SD, Owusu SA, Xu T, Yu Y, Jennings TN, Knaus BJ, Cronn RC, Arumuganathan AK, Coggeshall MV, Gailing O, Liang H, Romero-Severson J, Schlarbaum SE, Carlson JE. 2015. Preliminary genomic characterization of ten hardwood tree species from multiplexed low coverage whole genome sequencing. PLoS ONE 10(12): e0145031, 13 pages.
  • Type: Book Chapters Status: Published Year Published: 2016 Citation: Pereira-Lorenzo, S., Costa, R., Anagnostakis, S., Serdar, U., Yamamoto, T., Saito, T., Ramos-Cabrer, A.M., Ling, Q, Barreneche, T, Robin, C., Botta, R., Contessa, C., Conedera, M., Mart�n, L.M., Mart�n, A., Laranjo, J., Villani, F., Carlson, J.E. 2016. Chapter 15 - Interspecific hybridization of chestnut. In: Polyploidy and Hybridisation for Crop Improvement. Published May 15, 2016 by CRC Press, 440 Pages, ISBN 9781498740661 - CAT# K26702.


Progress 10/01/14 to 09/30/15

Outputs
Target Audience:Our target audiences are the general scientific community, public research institutes, foundations, tree growers, forest landowners, state and federal researchers,and the general public interested in tree improvement, especially The American Chestnut Foundation and the USDA Forest Service, the PA Bureau of Forestry, and other collaborators. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Professional development - Over the past year, this project contributed to the training of four undergraduate students (Alex Stanish, Horticulture; Byron Bredael, Horticulture; Jeffrey Osborne, Forest Biology; Lianna Johnson,Environmental Resource Management), and two graduate students (Di Wu, Forestryand Nathaniel Cannon, Bioinformatics) and post-doctoral fellowTeodora Best. Outreach was conducted by Extension Educator Gary Micsky to develop and utilize a network of trained volunteers who can be informed and mobilized electronically to assist in multiple chestnut restoration activities. Activities included; 14 training workshops and field experience;Extension newsletters, press releases, woodland owner association newsletters;Grower/Site evaluations; andPest Surveys. How have the results been disseminated to communities of interest?The results of our research are prrimaily disseminated through peer-reviewed journal publications, extension education materials, poster and oral presentations at local and international scientific conferences, invited lectures, and websites. What do you plan to do during the next reporting period to accomplish the goals?Plans for the coming year include: 1)Validate and improve the Chinese chestnut pseudochromosome sequences using very long genome sequences produced from the PacBio single molecule sequencing technology (proposal submitted by Hebard et al to the USDA AFRI program). 2)Prepare draft genome assemblies for American chestnut genotype GMBig, Chinese chestnut genotypes Nanking and Mahogany, and backcross parent genotypes Clapper and Graves (proposals submitted by Carlson and Westbrook). 3)Obtain deep RNA sequence data from several tissues of Chinese chestnut cv. Vanuxem to refine the identification and annotation of genes in the reference genome. 4)Submit refereed journal article on Chinese chestnut reference genome (in preparation. 5)Host the 2015 annual meeting of The American Chestnut Foundation on October 23 and 24, 2015, to update the TACF membership on the status of and discoveries from chestnut genomics. The meeting will include a workshop that brings together chestnut genomics researchers and TACF members to begin the process of integrating tools from genomics into the breeding and reforestation efforts. 6)Continue outreach and education/training sessions for community volunteers to engage in chestnut restoration.

Impacts
What was accomplished under these goals? Goal (1) Develop and evaluate blight resistant chestnuts for food and fiber through traditional and molecular approaches that incorporate knowledge of the chestnut genome: The Chinese chestnut genome sequencing project participants include John Carlson (PI), Charles Addo-Quaye, Nathaniel Cannon, Lynn Tomsho, Daniela Drautz, Lindsay Kasson, Tyler Wagner, Nicole Zembower, Abdelali Barakat, Richard Burhans, Webb Miller, and Stephan Schuster at Penn State University, with Steven Ficklin, Chis Saski, and Bert Abbott at Clemson University, Margaret Staton at the University of Tennessee, Dana Nelson of the USDA Forest Service, and Fred Hebard and Laura Georgi of TACF. Over the past year the assembly of the Chinese chestnut cultivar 'Vanuxem' genome was significantly improved. The current status of the genome sequence is a set of 14,358 scaffolds representing 784Mb of genome sequence, or app. 98% of the estimated genome size (improved from 724.4 Mp in 41,270 scaffolds in our last report). The size of the largest individual scaffold is now 3.17Mb, with average scaffold size of app. 55Kb (improved from N50 of 39.6Kb and largest scaffold of 429 Kb in 2014). Another major step forward has been the anchoring of almost 90% of the genome scaffolds to the genetic map, using the chestnut integrated genetic-and-physical map and the BAC-end sequences covering the physical map of cv. Vanuxem. This allowed us to assemble the scaffolds into a set of 12 pseudo-chromosome sequences, covering the majority of positions along the 12 linkage groups. The draft pseudo-chromosomes allow the physical position of all genetically mapped sequences and the genetic map position of sequences on the pseudo-chromosomes to now be estimated. The website for the genome and QTL assemblies was upgraded to JBrowse format. (http://www.hardwoodgenomics.org/content/tools). The scaffolds, gene models, predicted transcripts and predicted proteomes are allavailable to the community to download at the hardwood genomics website. The genome is also now present in the NCBI database. In addition, over the past year an intensive, manual annotation of genes in the QTL assemblies was conducted, which are also represented in the browser. Also 'resequencing' depth (app. 10X) data wasobtainedfor the following set of species and genotypes from CAES and TACF orchards: one C. alnifolia genotype, one C. crenata genotype, five C. dentata genotypes (GMBig, Ted Farm A, Alex R, Huan Row1Tree18(MK5), and Ellis 1), one C. henryii genotype (Chinese chinkapin), four C. mollissima genotypes (Mahogany, Nanking, PA Fat Camp, and PA Stone Valley), one C. ozarkensis genotype, one C. sativa genotype, one C. seguinii genotype, three third backcross hybrids from the TACF breeding program (from parents B3119 x B3176), and the BC3 C. dentata x C. mollissima parental genotypes - B3119 and B3176. We have aligned these sequences to the reference Vanuxem genome to assess within and between species sequence variation in chestnut.

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2015 Citation: Joshua R. Herr Erin D. Scully, Scott M. Geib, Kelli Hoover, David M. Geiser, Ming Tien, John E. Carlson. Genome sequence of a Fusarium species (MYA-4552) isolated from the midgut of Anoplophora glabripennis, an invasive, wood-boring beetle. Submitted to Genome Announcements, Sept 18, 2015. Manuscript # genomeA01303-15.
  • Type: Journal Articles Status: Submitted Year Published: 2015 Citation: Rebecca A. Carroll, Chicko Jones, Teodora Best, Ketia Shumaker and John Carlson. Gene expression in hardwood trees species exposed to ozone, Submitted June 21, 2015, to the Journal of Undergraduate Research and Scholarly Excellence.
  • Type: Journal Articles Status: Submitted Year Published: 2015 Citation: Timothy Odom, KelviNeisha Williams, Teodora Best, Nicole Zembower, Ketia Shumaker, John Carlson, An analysis of gene expression induced by elevated atmospheric ozone in hardwood trees native to Eastern North America, Submitted June 21, 2015, to the Journal of Undergraduate Research and Scholarly Excellence.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2015 Citation: JE Carlson, M Staton, T Orendovici-Best, N Zembower, T Lane, J Davitt, T Zhebentyayeva, D Wu, D Moses, M Coggeshall, O Gailing, H Liang, J Romero-Severson, CA Saski, S Schlarbaum, K Shumaker, S Schuster, N Wheeler. Genomic Resources for North American Hardwoods. Plant and Animal Genome XXIII Conference, San Diego, CA, Jan. 11, 2015, poster #15556.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2015 Citation: E. Sollars, L. J. Kelly, D. Swarbreck, B. Clavijo, J. Zohren, D. Boshier, J. Clark, S. Lee, J. Koch, J. E. Carlson, E. D. Kjaer, L. R. Nielsen, W. Crowther, S. J. Rossiter, A. Joecker, S. Ayling, M. Caccamo, R. J. A. Buggs. Genome sequencing of Fraxinus species to identify loci relevant to ash dieback and emerald ash borer. 16  17 June 2015, Boston, MA, USA.
  • Type: Websites Status: Published Year Published: 2015 Citation: Updated database and web site for the Hardwood Genomics Project - www.hardwoodgenomics.org.
  • Type: Websites Status: Published Year Published: 2015 Citation: Database and portal for the Chinese Chestnut Genome project - http://www.hardwoodgenomics.org/chinese-chestnutgenome.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Pang T, Guo L, Shim D, Cannon N, Tang S, Chen J, Carlson JE, Xia X, Yin W. 2015. Characterization of the transcriptome of the xerophyte Ammopiptanthus mongolicus under drought stress by 454 pyrosequencing. PLoS ONE 10(8): e0136495, 25 pages.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen C-C, Xu Y, Xu T, Staton M, Stott G, Bukles O, Schlarbaum SE, Carlson JE, Liang H. 2015. Diversity level of genomic microsatellites in redbay (Persea borbonia L.) generated by Illumina sequencing. Journal of Plant Science and Molecular Breeding. 4:2, 5 pages.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Khodwekar S, Staton M, Coggeshall MV, Carlson JE, Gailing O. 2015. Nuclear microsatellite markers for population genetic studies in sugar maple (Acer saccharum Marsh.). Ann. For. Res. 58(2): 1-12.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Zhang X, Carlson A, Tian Z, Staton M, Schlarbaum SE, Carlson JE, Liang H. 2015. Genetic characterization of Liriodendron seed orchards with EST-SSR markers. Journal of Plant Science and Molecular Breeding. 4:1, 9 pages.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Chen CC, Bates R, Carlson J. 2015. Effect of environmental and cultural conditions in medium pH and plant growth performance of Douglas-fir (Pseudotsuga menziesii) shoot culture, F1000Research, 3:298, 14 pages.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Diningrat DS, Widiyanto SM, Pancoro1 A, Iriawati, Shim D, Panchangam B, Zembower N, Carlson JE. 2014. Transcriptomes of Teak (Tectona grandis, L.f) in Vegetative to Generative Transition Stage Development. International Journal of Innovation and Applied Studies, 9(3): 1416-1427.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Scully E; Geib SM; Carlson JE; Tien M; Hoover K. 2014. Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics, 15:1096, 21 pages.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: ang H-Y, Rhee J-Y, Carlson JE, Ahn S-J. 2014. The Camelina aquaporin CsPIP2;1 is regulated by phosphorylation at Ser273, but not at Ser277, of the C-terminus and is involved in salt- and drought-stress responses . Journal of Plant Physiology, 171(15): 1401-1412.
  • Type: Journal Articles Status: Accepted Year Published: 2015 Citation: Staton M, Zhebentyayeva T, Olukolu B, Fang GC, Nelson D, Carlson JE, Abbott AG. 2015. Substantial genome synteny preservation among woody angiosperm species: comparative genomics of Chinese chestnut (Castanea mollissima) and plant reference genomes. BMC Genomics. 16:744.


Progress 10/01/13 to 09/30/14

Outputs
Target Audience: Our target audiences are the general scientific community, public research institutes, foundations, tree growers, forest landowners, and the general public interested in tree improvement, especially The American Chestnut Foundation and the USDA Forest Service, the PA Bureau of Forestry, and other collaborators. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Over the past year, this project has contributed to the training of four undergraduate students (Alex Stanish, Horticulture; Byron Bredael, Horticulture; Jeffrey Osborne, Forest Biology; Chelsea Kyler, Forest Biology), four graduate students (Wanyan Wang, Plant Biology; Di Wu, Forestry; Erin Scully, Genetics; and Nathaniel Cannon, Bioinformatics) and post-octoral fellows Dongwhan Shim and Teodora Best. How have the results been disseminated to communities of interest? The results of our research are prrimaily disseminated through peer-reviewed journal publications, extension education materials, poster and oral presentations at local and international scientific conferences, invited lectures, and websites. What do you plan to do during the next reporting period to accomplish the goals? In the coming year we will focus on establishing a solid platform for genome-wide marker-assisted selection studies in the Amerrican chestnut beeding progam using the Chinese chestnut genome through genotyping-by-sequencing, transcript mapping, and genome-wide association with phenotypes. This research may include improvement to the genome assembly. We will also participate in the evaluation of willow biomass energy test plots for growth, yield, and genotype-by-environment inteactions as part of the USDA NEWBio project.

Impacts
What was accomplished under these goals? Goal (1) Develop and evaluate blight resistant chestnuts for food and fiber through traditional and molecular approaches that incorporate knowledge of the chestnut genome: The Chinese chestnut genome sequencing project was initiated in 2009 to produce a reference genome sequence for Castanea mollissima cv Vanuxem as a platform for the identification of blight resistance genes and to conduct marker-assisted selection at the whole genome level. Participants in the project have included John Carlson (PI), Charles Addo-Quaye, Lynn Tomsho, Daniela Drautz, Lindsay Kasson, Tyler Wagner, Nicole Zembower, Abdelali Barakat, Richard Burhans, Webb Miller, and Stephan Schuster at Penn State University, with Meg Staton, Steven Ficklin, Chis Saski, and Bert Abbott at Clemson University, Dana Nelson of the USDA Forest Service, and Fred Hebard of TACF. A second round of sequencing and assembly produced a new draft genome of 724.4 Mp in 41,270 scaffolds. This represents 90% of the estimated size of the chestnut genome, in which 38,268 genes were identified, supported by gene expression data. We also produced deep sequence of the Chinese chestnut blight resistance QTL, which were assembled into 214 scaffolds (6.8 Mb of DNA sequence) for QTL cbr1 on Linkage Group (LG) B, 128 scaffolds (4.1 Mb) for QTL cbr2 on LG F, anroduce d 53 scaffolds (3.0 Mb) for QTL cbr3 on LG G. In total we identified 1952 genes in the 3 QTL, from which 15 genes were selected as high priority candidate genes for blight resistance based on defense-response gene annotations, including transcription factors, CC-NBS-LRR resistance proteins, RNA-binding protein, 14-3-3-like protein, endopeptidase, protease, disease resistance genes, glycosyltransferase, receptor-like kinase, and a histone-methyltransferase. In the past year, we have concentrated on analyzing the current genome and QTL assemblies for publication and for use in American chestnut breeding. Browsers for the genome and QTL assemblies were released at the hardwood genomics website (http://www.hardwoodgenomics.org/content/tools). The scaffolds, gene models, predicted transcripts and proteomes are fully annotated to model plant genomes, and are available to the public to download. A site for the genome was also recently completed at the NCBI database (http://www.ncbi.nlm.nih.gov/bioproject/?term=castanea%20genome). The current draft of the Chinese chestnut genome was presented to the broader research community through talks and posters at the Plant & Animal Genome Conference XXII, San Diego, CA, on January 12, 2014, and at the PAG-Asia Conference in Singapore, May 19-21, 2014. Manuscripts describing the blight resistance QTL sequences and the Chinese chestnut genome are in preparation for submission in 2014. The genome manuscript will include assignments of scaffolds to linkage groups, gene family orthology groups, repetitive DNA families, statistics on genome sequence divergence among chestnut species, and the results of comparative genomic studies.

Publications

  • Type: Book Chapters Status: Published Year Published: 2014 Citation: Nelson, C.D., W.A. Powell, S.A. Merkle, J.E. Carlson, F.V. Hebard, N. Islam-Faridi, M.E. Staton, L. Georgi. 2014. Biotechnology of Trees: Chestnut. In: Ramawat K, Merillon JM, Ahuja MR (eds), Tree Biotechnology, Chapter 1. CRC Press, Boca Raton, Florida, USA, April 1, 2014, pp. 3-35, ISBN 9781466597143.
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Herr JR and JE Carlson. Traditional Breeding, Genomics-Assisted Breeding, and Biotechnological Modification of Forest Trees and Short Rotation Woody Crops. 2013. In: Jacobson M, Ciolkosz D (eds), Wood-Based Energy in the Northern Forests. New York: Springer, pp 79-99. ISBN: 978-1-4614-9477-5 (Print) 978-1-4614-9478-2.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Nelson, C.D., Powell, W.A., Maynard, C.A., Baier, K.M., Newhouse, A., Merkle, S.A., Nairn, C.J., Kong, L., Carlson, J.E., Addo-Quaye, C., Staton, M.E., Hebard, F.V., Georgi, L.L., Abbott, A.G., Olukolu, B.A. and Zhebentyayeva, T. 2014. The forest health initiative, American chestnut (Castanea dentate) as a model for forest tree restoration: biological research program. Acta Hort. (ISHS) 1019:179-189.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Fang GC, Blackmon BP, Staton ME, Nelson CD, Kubisiak TL, Olukolu BA, Henry D, Zhebentyayeva Y, Saski CA, Cheng CH, Monsanto M, Ficklin S, Atkins M, Georgi LL, Barakat A, Wheeler N, Carlson JE, Sederoff R, Abbott AG. 2013. A physical map of the Chinese chestnut (Castanea mollissima) genome and its integration with the genetic map. Tree Genetics & Genomes, 9(2): 525-537.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Petit RJ, Carlson J, Curtu AL, Loustau ML, Plomion C, Gonz�lez-Rodr�guez A, Sork V, Ducousso A. 2013. Fagaceae trees as models to integrate ecology, evolution and genomics. New Phytologist, 197: 369  371.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Meinhardt LW, Thomazella DPT, Teixeira PJPL, Costa GGL, Carazzolle MF, Schuster SC, Carlson JE, Guiltinan MJ, Mieczkowski P, Farmer A, Ramaraj T, Crozier J, Davis RE, Shao J, Melnick RL, Pereira GAG, Bailey BA. 2014. Genome and secretome analysis of the hemibiotrophic fungal pathogen, Moniliophthora roreri, which causes frosty pod rot disease of cacao: Mechanisms of the biotrophic and necrotrophic phases. BMC Genomics, 15(1): 164, 25 pp.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Sha T, Liang H, Yan D, Zhao Y, Han X, Carlson JE, Xia X, Yin W. 2013. Populus euphratica: the transcriptomic response to drought stress. Plant Molecular Biology 83(6): 539-557.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Owusu SA, Staton M, Jennings TN, Schlarbaum S, Coggeshall MV, Romero-Severson J, Carlson JE, Gailing O. 2013. Development of Genomic Microsatellites in Gleditsia triacanthos (Fabaceae) Using Illumina Sequencing. Applications in Plant Sciences, 1(12): 1300050, doi:10.3732/apps.1300050, 4 pp.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Scully ED, Hoover K, Carlson JE, Tien M, Geib SM. 2013. Midgut transcriptome profiling of Anoplophora glabripennis, a lignocellulose degrading cerambycid beetle. BMC Genomics, 14:850. doi 10.1186/1471-2164-14-850.
  • Type: Journal Articles Status: Submitted Year Published: 2014 Citation: Xinfu Zhang, Alanna Carlson, Zhenkun Tian, Margaret Staton, Scott E. Schlarbaum, John E. Carlson, Haiying Liang, Genetic characterization of Liriodendron seed orchards with EST-SSR markers, Submitted to Euphytica, Oct 21, 2014.
  • Type: Journal Articles Status: Submitted Year Published: 2014 Citation: Erin Scully; Scott M Geib; John E. Carlson; Ming Tien; Kelli Hoover, Metatranscriptome Analysis and Community Profiling of Microbes Associated with a Xylophagous Beetle Midgut: Insights into Nutritional Ecology, submitted to BMC Genomics, July 29, 2014.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2014 Citation: John E. Carlson, Margaret E. Staton, Charles Addo-Quaye, Nathaniel Cannon, Lynn P. Tomsho, Stephen Ficklin, Chris Saski, Richard Burhans, Daniela Drautz, Tyler Kane Wagner, Nicole Zembower, Stephan C. Schuster, Albert G. Abbott, C. Dana Nelson, Frederick V. Hebard, 2014. The Chestnut Genome Project. Plant & Animal Genome Conference XXII, San Diego, CA, January 12, 2014, Abstract W307.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2013 Citation: Genomics Resources for Forest Ecosystem Health, Appalachian Lab, University of Maryland, November 1, 2013.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2014 Citation: John E. Carlson, Margaret E. Staton, Charles Addo-Quaye, Nathaniel Cannon, Lynn P. Tomsho, Stephen Ficklin, Chris Saski, Richard Burhans, Daniela Drautz, Tyler Kane Wagner, Nicole Zembower, Stephan C. Schuster, Albert G. Abbott, C. Dana Nelson, Frederick V. Hebard, 2014. The Chinese Chestnut (Castanea mollissima) Genome. PAG-Asia Conference II, Singapore, May 19-21, 2014.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2014 Citation: Albert G. Abbott, M. Staton, T. Zhebentyayeva, John E. Carlson, Veronique Decroocq, L. Georgi, Nurul Islam-Faridi, F. Hebard, Catherine Bodenes, Christophe Plomion, C. Dana Nelson. 2014. Comparative Genomics of Key Forest and Fruit Tree Species: A Strategic Path to Forest Health Improvement, Plant & Animal Genome Conference XXII, San Diego, CA, January 12, 2014, Abstract W309.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2014 Citation: Nurul Islam-Faridi, M.a. Majid, T. Zhebentyayeva, L. Georgi, M. Staton, F. Hebard, P. Sisco, John E. Carlson, C. Dana Nelson. 2014. Chestnut (Castanea spp.) Cytogenetics for Genomics and Breeding, Plant & Animal Genome Conference XXII, San Diego, CA, January 13, 2014, P481.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2014 Citation: John E. Carlson, M. Staton Clemson, Charles Addo-Quaye, Jeanne Romero-Severson, Scott Schlarbaum, Mark Coggeshall, Haiying Liang, Oliver Gailing, Ketia Shumaker, Teodora Orendovici-Best, Nicole Zembower, Nicholas Wheeler. 2014. Genomic Resources for North American Hardwoods. Plant & Animal Genome Conference XXII, San Diego, CA, January 13, 2014, P1109.
  • Type: Websites Status: Published Year Published: 2014 Citation: Updated database and web site for the Hardwood Genomics Project - www.hardwoodgenomics.org.
  • Type: Websites Status: Published Year Published: 2014 Citation: Database and portal for the Chinese Chestnut Genome project - http://www.hardwoodgenomics.org/chinese-chestnut-genome.