Four chromosome scale genomes and a pan-genome annotation to accelerate pecan tree breeding

Lovell, John T.; Bentley, Nolan B.; Bhattarai, Gaurab; Jenkins, Jerry W.; Sreedasyam, Avinash; Alarcon, Yanina; Bock, Clive; Boston, Lori Beth; Carlson, Joseph; Cervantes, Kimberly; Clermont, Kristen; Duke, Sara; Krom, Nick; Kubenka, Keith; Mamidi, Sujan; Mattison, Christopher P.; Monteros, Maria J.; Pisani, Cristina; Plott, Christopher; Rajasekar, Shanmugam; Rhein, Hormat Shadgou; Rohla, Charles; Song, Mingzhou; Hilaire, Rolston St.; Shu, Shengqiang; Wells, Lenny; Webber, Jenell; Heerema, Richard J.; Klein, Patricia E.; Conner, Patrick; Wang, Xinwang; Grauke, L. J.; Grimwood, Jane; Schmutz, Jeremy; Randall, Jennifer J.

doi:10.1038/s41467-021-24328-w

Four chromosome scale genomes and a pan-genome annotation to accelerate pecan tree breeding

Journal Article · Mon Jul 05 00:00:00 EDT 2021 · Nature Communications

DOI:https://doi.org/10.1038/s41467-021-24328-w· OSTI ID:1816167

^[1]; ^[2]; Bhattarai, Gaurab ^[3]; ^[4]; ^[4]; ^[5]; Bock, Clive ^[6]; Boston, Lori Beth ^[4]; Carlson, Joseph ^[7]; Cervantes, Kimberly ^[8]; Clermont, Kristen ^[9]; Duke, Sara ^[10]; Krom, Nick ^[11]; Kubenka, Keith ^[12]; Mamidi, Sujan ^[4]; ^[13]; ^[11]; Pisani, Cristina ^[6]; Plott, Christopher ^[4]; Rajasekar, Shanmugam ^[14] more »

HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States). Genome Sequencing Center; OSTI
Texas A & M Univ., College Station, TX (United States). Dept. of Horticultural Science
Univ. of Georgia, Athens, GA (United States). Inst. of Plant Breeding, Genetics & Genomics
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States). Genome Sequencing Center
Noble Research Institute, Ardmore, OK (United States)
USDA Southeastern Fruit and Tree Nut Research Lab.y, Byron, GA (United States)
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
New Mexico State Univ., Las Cruces, NM (United States). Dept. of Entomology, Plant Pathology and Weed Science
USDA-ARS Food Processing and Sensory Quality Research, New Orleans, LA (United States)
USDA-ARS Plains Area Administrative Office, College Station, TX (United States)
Noble Research Institute, Ardmore, OK (United States)
USDA Pecan Breeding and Genetics, College Station, TX (United States)
USDA-ARS Food Processing and Sensory Quality Research, New Orleans, LA (United States)
Univ. of Arizona, Tucson, AZ (United States). Arizona Genomics Inst.
New Mexico State Univ., Las Cruces, NM (United States). Dept. of Computer Science
New Mexico State Univ., Las Cruces, NM (United States). Plant and Environmental Sciences
Univ. of Georgia-Tifton Campus, Tifton, GA (United States). Dept. of Horticulture
USDA Pecan Breeding and Genetics, College Station, TX (United States)
HudsonAlpha Institute for Biotechnology, Huntsville, AL (United States). Genome Sequencing Center; USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)

Genome-enabled biotechnologies have the potential to accelerate breeding efforts in long-lived perennial crop species. Despite the transformative potential of molecular tools in pecan and other outcrossing tree species, highly heterozygous genomes, significant presence–absence gene content variation, and histories of interspecific hybridization have constrained breeding efforts. To overcome these challenges, here, we present diploid genome assemblies and annotations of four outbred pecan genotypes, including a PacBio HiFi chromosome-scale assembly of both haplotypes of the ‘Pawnee’ cultivar. Comparative analysis and pan-genome integration reveal substantial and likely adaptive interspecific genomic introgressions, including an over-retained haplotype introgressed from bitternut hickory into pecan breeding pedigrees. Further, by leveraging our pan-genome presence–absence and functional annotation database among genomes and within the two outbred haplotypes of the ‘Lakota’ genome, we identify candidate genes for pest and pathogen resistance. Combined, these analyses and resources highlight significant progress towards functional and quantitative genomics in highly diverse and outbred crops.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Oak Ridge Associated Univ., Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231; SC0014664

OSTI ID:: 1816167

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 12; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

Affinities of a Mexican Endemic, Carya Palmeri, with American and Asian Hickories Stone, Donald E. American Journal of Botany, Vol. 49, Issue 3 https://doi.org/10.1002/j.1537-2197.1962.tb14930.x	journal	March 1962
Pecan food potential in prehistoric North America Hal, Grant D. Economic Botany, Vol. 54, Issue 1 https://doi.org/10.1007/BF02866604	journal	January 2000
A first linkage map of pecan cultivars based on RAPD and AFLP markers Beedanagari, Sudheer R.; Dove, Sue K.; Wood, Bruce W. Theoretical and Applied Genetics, Vol. 110, Issue 6 https://doi.org/10.1007/s00122-005-1944-5	journal	March 2005
Aphid resistance in Capsicum maps to a locus containing LRR-RLK gene analogues Sun, Mengjing; Voorrips, Roeland E.; van’t Westende, Wendy Theoretical and Applied Genetics, Vol. 133, Issue 1 https://doi.org/10.1007/s00122-019-03453-7	journal	October 2019
Geographic patterns of genetic variation in native pecans Grauke, L. J.; Mendoza-Herrera, Maria Azucena; Miller, Allison J. Tree Genetics & Genomes, Vol. 7, Issue 5 https://doi.org/10.1007/s11295-011-0384-4	journal	March 2011
Apple, from genome to breeding Troggio, M.; Gleave, A.; Salvi, S. Tree Genetics & Genomes, Vol. 8, Issue 3 https://doi.org/10.1007/s11295-012-0492-9	journal	May 2012
Genotyping by sequencing (GBS) and SNP marker analysis of diverse accessions of pecan (Carya illinoinensis) Bentley, Nolan; Grauke, L. J.; Klein, Patricia Tree Genetics & Genomes, Vol. 15, Issue 1 https://doi.org/10.1007/s11295-018-1314-5	journal	January 2019
Linkage mapping and QTL analysis of pecan (Carya illinoinensis) full-siblings using genotyping-by-sequencing Bentley, Nolan; Grauke, L. J.; Ruhlman, Erin Tree Genetics & Genomes, Vol. 16, Issue 6 https://doi.org/10.1007/s11295-020-01476-6	journal	November 2020
Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments Durand, Neva C.; Shamim, Muhammad S.; Machol, Ido Cell Systems, Vol. 3, Issue 1 https://doi.org/10.1016/j.cels.2016.07.002	journal	July 2016
Biotechnology in the developing world: a case for increased investments in orphan crops Naylor, Rosamond L.; Falcon, Walter P.; Goodman, Robert M. Food Policy, Vol. 29, Issue 1 https://doi.org/10.1016/j.foodpol.2004.01.002	journal	February 2004
Priming plant resistance by activation of redox-sensitive genes González-Bosch, Carmen Free Radical Biology and Medicine, Vol. 122 https://doi.org/10.1016/j.freeradbiomed.2017.12.028	journal	July 2018
Clinical and Molecular Characterization of Walnut and Pecan Allergy (NUT CRACKER Study) Elizur, Arnon; Appel, Michael Y.; Nachshon, Liat The Journal of Allergy and Clinical Immunology: In Practice, Vol. 8, Issue 1 https://doi.org/10.1016/j.jaip.2019.08.038	journal	January 2020
Hide-and-Seek: Chitin-Triggered Plant Immunity and Fungal Counterstrategies Gong, Ben-Qiang; Wang, Feng-Zhu; Li, Jian-Feng Trends in Plant Science, Vol. 25, Issue 8 https://doi.org/10.1016/j.tplants.2020.03.006	journal	August 2020
The Sorghum bicolor genome and the diversification of grasses Paterson, Andrew H.; Bowers, John E.; Bruggmann, Rémy Nature, Vol. 457, Issue 7229 https://doi.org/10.1038/nature07723	journal	January 2009
Genome sequence of the palaeopolyploid soybean Schmutz, Jeremy; Cannon, Steven B.; Schlueter, Jessica Nature, Vol. 463, Issue 7278 https://doi.org/10.1038/nature08670	journal	January 2010
Fast gapped-read alignment with Bowtie 2 Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 9, Issue 4 https://doi.org/10.1038/nmeth.1923	journal	March 2012
Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data Chin, Chen-Shan; Alexander, David H.; Marks, Patrick Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2474	journal	May 2013
Fast and sensitive protein alignment using DIAMOND Buchfink, Benjamin; Xie, Chao; Huson, Daniel H. Nature Methods, Vol. 12, Issue 1 https://doi.org/10.1038/nmeth.3176	journal	November 2014
MECAT: fast mapping, error correction, and de novo assembly for single-molecule sequencing reads Xiao, Chuan-Le; Chen, Ying; Xie, Shang-Qian Nature Methods, Vol. 14, Issue 11 https://doi.org/10.1038/nmeth.4432	journal	September 2017
The genomic landscape of molecular responses to natural drought stress in Panicum hallii Lovell, John T.; Jenkins, Jerry; Lowry, David B. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07669-x	journal	December 2018
Rapid improvement of domestication traits in an orphan crop by genome editing Lemmon, Zachary H.; Reem, Nathan T.; Dalrymple, Justin Nature Plants, Vol. 4, Issue 10 https://doi.org/10.1038/s41477-018-0259-x	journal	October 2018
Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass Lovell, John T.; MacQueen, Alice H.; Mamidi, Sujan Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-020-03127-1	journal	January 2021
Massive haplotypes underlie ecotypic differentiation in sunflowers Todesco, Marco; Owens, Gregory L.; Bercovich, Natalia Nature, Vol. 584, Issue 7822 https://doi.org/10.1038/s41586-020-2467-6	journal	July 2020
A genome resource for green millet Setaria viridis enables discovery of agronomically valuable loci Mamidi, Sujan; Healey, Adam; Huang, Pu Nature Biotechnology, Vol. 38, Issue 10 https://doi.org/10.1038/s41587-020-0681-2	journal	October 2020
Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm Cheng, Haoyu; Concepcion, Gregory T.; Feng, Xiaowen Nature Methods, Vol. 18, Issue 2 https://doi.org/10.1038/s41592-020-01056-5	journal	February 2021
Sequence and gene expression evolution of paralogous genes in willows Harikrishnan, Srilakshmy L.; Pucholt, Pascal; Berlin, Sofia Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep18662	journal	December 2015
Investigation of the bottleneck leading to the domestication of maize Eyre-Walker, A.; Gaut, R. L.; Hilton, H. Proceedings of the National Academy of Sciences, Vol. 95, Issue 8 https://doi.org/10.1073/pnas.95.8.4441	journal	April 1998
Challenges of managing disease in tall orchard trees - pecan scab, a case study. Bock, C. H. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, Vol. 12, Issue 008 https://doi.org/10.1079/PAVSNNR201712008	journal	April 2017
Chitin and chitin-related compounds in plant–fungal interactions Pusztahelyi, Tünde Mycology, Vol. 9, Issue 3 https://doi.org/10.1080/21501203.2018.1473299	journal	May 2018
Redox Regulation in Plant Immune Function Frederickson Matika, Debra E.; Loake, Gary J. Antioxidants & Redox Signaling, Vol. 21, Issue 9 https://doi.org/10.1089/ars.2013.5679	journal	September 2014
GMAP: a genomic mapping and alignment program for mRNA and EST sequences Wu, T. D.; Watanabe, C. K. Bioinformatics, Vol. 21, Issue 9 https://doi.org/10.1093/bioinformatics/bti310	journal	February 2005
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data Li, H. Bioinformatics, Vol. 27, Issue 21 https://doi.org/10.1093/bioinformatics/btr509	journal	September 2011
A high-performance computing toolset for relatedness and principal component analysis of SNP data Zheng, X.; Levine, D.; Shen, J. Bioinformatics, Vol. 28, Issue 24 https://doi.org/10.1093/bioinformatics/bts606	journal	October 2012
STAR: ultrafast universal RNA-seq aligner Dobin, Alexander; Davis, Carrie A.; Schlesinger, Felix Bioinformatics, Vol. 29, Issue 1 https://doi.org/10.1093/bioinformatics/bts635	journal	October 2012
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
HTSeq--a Python framework to work with high-throughput sequencing data Anders, S.; Pyl, P. T.; Huber, W. Bioinformatics, Vol. 31, Issue 2 https://doi.org/10.1093/bioinformatics/btu638	journal	September 2014
Southern Pecan Leaf Phylloxera (Homoptera: Phylloxeridae): Clonal Resistance and Technique for Evaluation1 Calcote, V. R. Environmental Entomology, Vol. 12, Issue 3 https://doi.org/10.1093/ee/12.3.916	journal	June 1983
High-quality chromosome-scale assembly of the walnut (Juglans regia L.) reference genome Marrano, Annarita; Britton, Monica; Zaini, Paulo A. GigaScience, Vol. 9, Issue 5 https://doi.org/10.1093/gigascience/giaa050	journal	May 2020
Tree Species Used as Hosts by Pecan Weevil (Coleoptera: Curculionidae) Ring, D. R.; Grauke, L. J.; Payne, J. A. Journal of Economic Entomology, Vol. 84, Issue 6 https://doi.org/10.1093/jee/84.6.1782	journal	December 1991
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies Haas, B. J. Nucleic Acids Research, Vol. 31, Issue 19 https://doi.org/10.1093/nar/gkg770	journal	October 2003
The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools Lamesch, Philippe; Berardini, Tanya Z.; Li, Donghui Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1090	journal	December 2011
MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity Wang, Y.; Tang, H.; DeBarry, J. D. Nucleic Acids Research, Vol. 40, Issue 7 https://doi.org/10.1093/nar/gkr1293	journal	January 2012
UniProt: a worldwide hub of protein knowledge Consortium, The UniProt Nucleic Acids Research https://doi.org/10.1093/nar/gky1049		November 2018
Fine-Scale Population Genetic Structure and Within-Tree Distribution of Mating Types of Venturia effusa , Cause of Pecan Scab in the United States Bock, Clive H.; Young, Carolyn A.; Stevenson, Katherine L. Phytopathology®, Vol. 108, Issue 11 https://doi.org/10.1094/PHYTO-02-18-0068-R	journal	November 2018
Ab initio Gene Finding in Drosophila Genomic DNA Salamov, Asaf A.; Solovyev, Victor V. Genome Research, Vol. 10, Issue 4, p. 516-522 https://doi.org/10.1101/gr.10.4.516	journal	April 2000
VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing Koboldt, D. C.; Zhang, Q.; Larson, D. E. Genome Research, Vol. 22, Issue 3 https://doi.org/10.1101/gr.129684.111	journal	February 2012
Computational Inference of Homologous Gene Structures in the Human Genome Yeh, R. -F.; Lim, L. P.; Burge, C. B. Genome Research, Vol. 11, Issue 5 https://doi.org/10.1101/gr.175701	journal	May 2001
Fast and accurate de novo genome assembly from long uncorrected reads Vaser, Robert; Sović, Ivan; Nagarajan, Niranjan Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.214270.116	journal	January 2017
BLAT---The BLAST-Like Alignment Tool Kent, W. J. Genome Research, Vol. 12, Issue 4 https://doi.org/10.1101/gr.229202	journal	March 2002
Close Split of Sorghum and Maize Genome Progenitors Swigonova, Z. Genome Research, Vol. 14, Issue 10a https://doi.org/10.1101/gr.2332504	journal	September 2004
Tree nut allergies: Allergen homology, cross-reactivity, and implications for therapy Smeekens, J. M.; Bagley, K.; Kulis, M. Clinical & Experimental Allergy, Vol. 48, Issue 7 https://doi.org/10.1111/cea.13163	journal	June 2018
Limber pine ( Pinus flexilis James) genetic map constructed by exome‐seq provides insight into the evolution of disease resistance and a genomic resource for genomics‐based breeding Liu, Jun‐Jun; Schoettle, Anna W.; Sniezko, Richard A. The Plant Journal, Vol. 98, Issue 4 https://doi.org/10.1111/tpj.14270	journal	March 2019
The B73 Maize Genome: Complexity, Diversity, and Dynamics Schnable, P. S.; Ware, D.; Fulton, R. S. Science, Vol. 326, Issue 5956, p. 1112-1115 https://doi.org/10.1126/science.1178534	journal	November 2009
Seed Banks and Molecular Maps: Unlocking Genetic Potential from the Wild Tanksley, Steven D.; McCouch, Susan R. Science, Vol. 277, Issue 5329 https://doi.org/10.1126/science.277.5329.1063	journal	August 1997
A Bountiful Harvest: Genomic Insights into Crop Domestication Phenotypes Olsen, Kenneth M.; Wendel, Jonathan F. Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120048	journal	April 2013
Automated generation of heuristics for biological sequence comparison Slater, Guy St C.; Birney, Ewan BMC Bioinformatics, Vol. 6, Issue 1 https://doi.org/10.1186/1471-2105-6-31	journal	February 2005
Synteny analysis in Rosids with a walnut physical map reveals slow genome evolution in long-lived woody perennials Luo, Ming-Cheng; You, Frank M.; Li, Pingchuan BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1906-5	journal	September 2015
Genome sequence of the model rice variety KitaakeX Jain, Rashmi; Jenkins, Jerry; Shu, Shengqiang BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-6262-4	journal	November 2019
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014
OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy Emms, David M.; Kelly, Steven Genome Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s13059-015-0721-2	journal	August 2015
A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa Hofmeister, Brigitte T.; Denkena, Johanna; Colomé-Tatché, Maria Genome Biology, Vol. 21, Issue 1 https://doi.org/10.1186/s13059-020-02162-5	journal	October 2020
A Hidden Markov Model Approach for Simultaneously Estimating Local Ancestry and Admixture Time Using Next Generation Sequence Data in Samples of Arbitrary Ploidy Corbett-Detig, Russell; Nielsen, Rasmus PLOS Genetics, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pgen.1006529	journal	January 2017
R/qtl2: Software for Mapping Quantitative Trait Loci with High-Dimensional Data and Multiparent Populations Broman, Karl W.; Gatti, Daniel M.; Simecek, Petr Genetics, Vol. 211, Issue 2 https://doi.org/10.1534/genetics.118.301595	journal	December 2018
DNA Identification Confirms Pecan Weevil (Coleoptera: Curculionidae) Infestation of Carpathian Walnut Harris, Marvin K.; Hunt, Kenneth L.; Cognato, Anthony I. Journal of Economic Entomology, Vol. 103, Issue 4 https://doi.org/10.1603/EC10134	journal	August 2010
The Forest and the Trees: Applications for Molecular Markers in the Repository and Pecan Breeding Program Grauke, L. J.; Klein, R.; Grusak, M. A. Acta Horticulturae, Issue 1070 https://doi.org/10.17660/ActaHortic.2015.1070.12	journal	February 2015
dbscan : Fast Density-Based Clustering with R Hahsler, Michael; Piekenbrock, Matthew; Doran, Derek Journal of Statistical Software, Vol. 91, Issue 1 https://doi.org/10.18637/jss.v091.i01	journal	January 2019
‘Pawnee’ Pecan Thompson, T. E.; Hunter, R. E. HortScience, Vol. 20, Issue 4 https://doi.org/10.21273/HORTSCI.20.4.776	journal	August 1985
Genetic Resistance to Scab Disease in Pecan Thompson, Tommy E.; Grauke, L. J. HortScience, Vol. 29, Issue 9 https://doi.org/10.21273/HORTSCI.29.9.1078	journal	September 1994
Pathogenic Variation of Cladosporium caryigenum Isolates and Corresponding Differential Resistance in Pecan Conner, Patrick J.; Stevenson, Katherine L. HortScience, Vol. 39, Issue 3 https://doi.org/10.21273/HORTSCI.39.3.553	journal	June 2004
‘Lakota’ Pecan Thompson, Tommy E.; Grauke, L. J.; Reid, William HortScience, Vol. 43, Issue 1 https://doi.org/10.21273/HORTSCI.43.1.250	journal	February 2008
Crop Vulnerability: Carya Grauke, L. J.; Wood, Bruce W.; Harris, Marvin K. HortScience, Vol. 51, Issue 6 https://doi.org/10.21273/HORTSCI.51.6.653	journal	June 2016
Performance of 19 Pecan Cultivars and Selections in Southern Georgia Conner, Patrick J. HortTechnology, Vol. 24, Issue 3 https://doi.org/10.21273/HORTTECH.24.3.407	journal	June 2014
Developing Microsatellite DNA Markers in Pecan Grauke, L. J.; Iqbal, Muhammad J.; Reddy, Avutu S. Journal of the American Society for Horticultural Science, Vol. 128, Issue 3 https://doi.org/10.21273/JASHS.128.3.0374	journal	May 2003
QTL Mapping by SLAF-seq and Expression Analysis of Candidate Genes for Aphid Resistance in Cucumber Liang, Danna; Chen, Minyang; Qi, Xiaohua Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01000	journal	July 2016
The Road to Resistance in Forest Trees Naidoo, Sanushka; Slippers, Bernard; Plett, Jonathan M. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00273	journal	March 2019
Relative Susceptibility of Pecan Germplasm to Blackmargined Aphid Skrivanek, Sarah; Grauke, L. J.; Martin, Dan Southwestern Entomologist, Vol. 38, Issue 1 https://doi.org/10.3958/059.038.0105	journal	March 2013
The genus Carya in Mexico Manning, W. E. Journal of the Arnold Arboretum., Vol. 30 https://doi.org/10.5962/bhl.part.18053	journal	January 1949

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Additional file 1 of Insight into the CBL and CIPK gene families in pecan (Carya illinoinensis): identification, evolution and expression patterns in drought response Zhu, Kaikai; Fan, Pinghua; Liu, Hui figshare https://doi.org/10.6084/m9.figshare.19682099	dataset	January 2022

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