Skip to main content

“A reference genome assembly and adaptive trait analysis of Castanea mollissima ‘Vanuxem,’ a source of resistance to chestnut blight in restoration breeding”

Abstract

Forest tree species are increasingly subject to severe mortalities from exotic pests, pathogens, and invasive organisms, accelerated by climate change. Such forest health issues are threatening multiple species and ecosystem sustainability globally. One of the most extreme examples of forest ecosystem disruption is the extirpation of the American chestnut (Castanea dentata) caused by the introduction of chestnut blight and root rot pathogens from Asia. Asian species of chestnut are being employed as donors of disease resistance genes to restore native chestnut species in North America and Europe. To aid in the restoration of threatened chestnut species, we present the assembly of a reference genome for Chinese chestnut (C. mollissima) “Vanuxem,” one of the donors of disease resistance for American chestnut restoration. From the de novo assembly of the complete genome (725.2 Mb in 14,110 contigs), over half of the sequences have been anchored to the 12 genetic linkage groups. The anchoring is validated by genetic maps and in situ hybridization to chromosomes. We demonstrate the value of the genome as a platform for research and species restoration, including signatures of selection differentiating American chestnut from Chinese chestnut to identify important candidate genes for disease resistance, comparisons of genome organization with other woody species, and a genome-wide examination of progress in backcross breeding for blight resistance. This reference assembly should prove of great value in the understanding, improvement, and restoration of chestnut species.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Abbott AG, Zhebentyayeva T, Barakat A, Liu Z (2015) The genetic control of bud-break in trees. Adv Bot Res:201–228

  2. Anagnostakis SL (2012) Chestnut breeding in the United States for disease and insect resistance. Plant Dis 96:1392–1403

    PubMed  Google Scholar 

  3. Anders S, Pyl PT, Huber W (2015) HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169

    CAS  Google Scholar 

  4. Anwar A, She M, Wang K, Riaz B, Ye X (2018) Biological roles of ornithine aminotransferase (OAT) in plant stress tolerance: present progress and future perspectives. Int J Mol Sci 19. https://doi.org/10.3390/ijms19113681

  5. Aranzana MJ, Decroocq V, Dirlewanger E, Eduardo I, Gao ZS, Gasic K, Iezzoni A, Jung S, Peace C, Prieto H, Tao R, Verde I, Abbott AG, Arús P (2019) Prunus genetics and applications after de novo genome sequencing: achievements and prospects. Horticulture Research 6:58

    PubMed  PubMed Central  Google Scholar 

  6. Arentz F (2017) Phytophthora cinnamomi A1: an ancient resident of New Guinea and Australia of Gondwanan origin? For Pathol 47:e12342

    Google Scholar 

  7. Auwera GA, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy-Moonshine A, Jordan T, Shakir K, Roazen D, Thibault J, Banks E, Garimella KV, Altshuler D, Gabriel S, DePristo MA (2013) From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr Protoc Bioinformatics 43

  8. Bacete L, Mélida H, Miedes E, Molina A (2018) Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J 93:614–636

    CAS  PubMed  Google Scholar 

  9. Baier K, Maynard C, Powell W (2012) Early flowering in chestnut species induced under high-Intensity, high-dose light in growth chambers. J Amer Chest Found 26:8–10

  10. Bairoch A, Apweiler R (1998) The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1998. Nucleic Acids Res 26:38–42

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Bao W, Kojima KK, Kohany O (2015) Repbase update, a database of repetitive elements in eukaryotic genomes. Mob DNA 6:11

    PubMed  PubMed Central  Google Scholar 

  12. Barakat A, DiLoreto DS, Zhang Y et al (2009) Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. BMC Plant Biol 9:51

    PubMed  PubMed Central  Google Scholar 

  13. Bielenberg DG, Wang Y(E), Li Z et al (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507

    Google Scholar 

  14. Bodénès C, Chancerel E, Gailing O, Vendramin GG, Bagnoli F, Durand J, Goicoechea PG, Soliani C, Villani F, Mattioni C, Koelewijn H, Murat F, Salse J, Roussel G, Boury C, Alberto F, Kremer A, Plomion C (2012) Comparative mapping in the Fagaceae and beyond with EST-SSRs. BMC Plant Biol 12:153

    PubMed  PubMed Central  Google Scholar 

  15. Bodénès C, Chancerel E, Ehrenmann F, Kremer A, Plomion C (2016) High-density linkage mapping and distribution of segregation distortion regions in the oak genome. DNA Res 23:115–124

    PubMed  PubMed Central  Google Scholar 

  16. broadinstitute broadinstitute/picard. In: GitHub. https://github.com/broadinstitute/picard. Accessed 19 Dec 2019

  17. Cahill DM, McComb JA (1992) A comparison of changes in phenylalanine ammonia-lyase activity, lignin and phenolic synthesis in the roots of Eucalyptus calophylla (field resistant) and E. marginata (susceptible) when infected with Phytophthora cinnamomi. Physiol Mol Plant Pathol 40:315–332

    CAS  Google Scholar 

  18. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinformatics 10:421

    PubMed  PubMed Central  Google Scholar 

  19. Campoy JA, Ruiz D, Egea J, Rees DJG, Celton JM, Martínez-Gómez P (2011) Inheritance of flowering time in apricot (Prunus armeniaca L.) and analysis of linked quantitative trait loci (QTLs) using simple sequence repeat (SSR) markers. Plant Mol Biol Report 29:404–410

    CAS  Google Scholar 

  20. Casasoli M, Derory J, Morera-Dutrey C, Brendel O, Porth I, Guehl JM, Villani F, Kremer A (2006) Comparison of quantitative trait loci for adaptive traits between oak and chestnut based on an expressed sequence tag consensus map. Genetics 172:533–546

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Characterization TFPCFGG, The French–Italian Public Consortium for Grapevine Genome Characterization (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Google Scholar 

  22. Clarke JD (2009) Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb Protoc 2009:db.prot5177

    Google Scholar 

  23. Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728

    CAS  PubMed  Google Scholar 

  24. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Delgado-Cerrone L, Alvarez A, Mena E, Ponce de León I, Montesano M (2018) Genome-wide analysis of the soybean CRK-family and transcriptional regulation by biotic stress signals triggering plant immunity. PLoS One 13:e0207438

    PubMed  PubMed Central  Google Scholar 

  26. Derory J, Scotti-Saintagne C, Bertocchi E, le Dantec L, Graignic N, Jauffres A, Casasoli M, Chancerel E, Bodenes C, Alberto F, Kremer A (2010) Contrasting relations between diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity 105:401–411

    CAS  PubMed  Google Scholar 

  27. Diskin M, Steiner KC, Hebard FV (2006) Recovery of American chestnut characteristics following hybridization and backcross breeding to restore blight-ravaged Castanea dentata. For Ecol Manag 223:439–447

    Google Scholar 

  28. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15–21

    CAS  Google Scholar 

  29. Eddy SR (2011) Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:157

    PubMed  PubMed Central  Google Scholar 

  31. Endelman JB, Plomion C (2014) LPmerge: an R package for merging genetic maps by linear programming. Bioinformatics 30:1623–1624

    CAS  PubMed  Google Scholar 

  32. Engelbrecht J, van den Berg N (2013) Expression of defence-related genes against Phytophthora cinnamomi in five avocado rootstocks. S Afr J Sci 109:1–8

    Google Scholar 

  33. Fan S, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR, Holland D, Abbott AG (2010) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol 185:917–930

    PubMed  Google Scholar 

  34. Fan S, Georgi L, Hebard FV, et al (2020) Mapping QTLs for blight resistance and morphological and phenological traits in chestnut (Castanea spp.). (in prep)

  35. Fang G-C, Blackmon BP, Staton ME, Nelson CD, Kubisiak TL, Olukolu BA, Henry D, Zhebentyayeva T, 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 Genet Genomes 9:525–537

    Google Scholar 

  36. Freinkel S (2009) American chestnut: the life, death, and rebirth of a perfect tree. Univ of California Press

  37. Gabay G, Dahan Y, Izhaki Y, Faigenboim A, Ben-Ari G, Elkind Y, Flaishman MA (2018) High-resolution genetic linkage map of European pear (Pyrus communis) and QTL fine-mapping of vegetative budbreak time. BMC Plant Biol 18:175

    PubMed  PubMed Central  Google Scholar 

  38. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    CAS  PubMed  Google Scholar 

  39. Gremme G, Brendel V, Sparks ME, Kurtz S (2005) Engineering a software tool for gene structure prediction in higher organisms. Inf Softw Technol 47:965–978

    Google Scholar 

  40. Groover A, Cronk Q (eds) (2017) Comparative and evolutionary genomics of angiosperm trees. Springer, Cham

    Google Scholar 

  41. Hamann T (2015) The plant cell wall integrity maintenance mechanism—concepts for organization and mode of action. Plant Cell Physiol 56:215–223

    CAS  PubMed  Google Scholar 

  42. Hebard FV (1994) Inheritance of juvenile leaf and stem morphological traits in crosses of Chinese and American chestnut. J Hered 85:440–446

    Google Scholar 

  43. Hebard FV (2005) The backcross breeding program of the American Chestnut Foundation. In Proc. of Restoration of American Chestnut to Forest Lands Conference. Steiner, K.C. and J.E. Carlson (eds.)

  44. Hoff KJ, Lange S, Lomsadze A, Borodovsky M, Stanke M (2016) BRAKER1: unsupervised RNA-Seq-based genome annotation with GeneMark-ET and AUGUSTUS. Bioinformatics 32:767–769

    CAS  PubMed  Google Scholar 

  45. Hung C-Y, Aspesi P Jr, Hunter MR et al (2014) Phosphoinositide-signaling is one component of a robust plant defense response. Front Plant Sci 5:267

    PubMed  PubMed Central  Google Scholar 

  46. International Peach Genome Initiative, Verde I, Abbott AG et al (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–494

    Google Scholar 

  47. Islam-Faridi MN, Childs KL, Klein PE, Hodnett G, Menz MA, Klein RR, Rooney WL, Mullet JE, Stelly DM, Price HJ (2002) A molecular cytogenetic map of sorghum chromosome 1. Fluorescence in situ hybridization analysis with mapped bacterial artificial chromosomes. Genetics 161:345–353

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Islam-Faridi MN, Nelson CD, DiFazio SP et al (2009) Cytogenetic analysis of Populus trichocarpa--ribosomal DNA, telomere repeat sequence, and marker-selected BACs. Cytogenet Genome Res 125:74–80

    CAS  PubMed  Google Scholar 

  49. Jewell DC, Islam-Faridi N (1994) A technique for somatic chromosome preparation and C-banding of maize. The Maize Handbook:484–493

  50. Jiang H, Lei R, Ding S-W, Zhu S (2014) Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics 15:182

    PubMed  PubMed Central  Google Scholar 

  51. Jiao W-B, Schneeberger K (2017) The impact of third generation genomic technologies on plant genome assembly. Curr Opin Plant Biol 36:64–70

    CAS  PubMed  Google Scholar 

  52. Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731

    CAS  PubMed  Google Scholar 

  54. Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. Arabidopsis Book 9:e0153

    PubMed  PubMed Central  Google Scholar 

  55. Kaye Y, Golani Y, Singer Y, Leshem Y, Cohen G, Ercetin M, Gillaspy G, Levine A (2011) Inositol polyphosphate 5-phosphatase7 regulates the production of reactive oxygen species and salt tolerance in Arabidopsis. Plant Physiol 157:229–241

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Korneliussen TS, Albrechtsen A, Nielsen R (2014) ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15:356

    PubMed  PubMed Central  Google Scholar 

  57. Kremer A, Casasoli M, Barreneche T et al (2007) Comparative genetic mapping in Fagaceae. In: Kole CR (ed) Genome Mapping & Molecular Breeding in plants, Vol. 7: Forest trees. Springer, Heidelberg, pp 161–187

    Google Scholar 

  58. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19:1639–1645

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Kubisiak TL, Hebard FV, Nelson CD, Zhang J, Bernatzky R, Huang H, Anagnostakis SL, Doudrick RL (1997) Molecular mapping of resistance to blight in an interspecific cross in the genus castanea. Phytopathology 87:751–759

    CAS  PubMed  Google Scholar 

  60. Kubisiak TL, Nelson CD, Staton ME, Zhebentyayeva T, Smith C, Olukolu BA, Fang GC, Hebard FV, Anagnostakis S, Wheeler N, Sisco PH, Abbott AG, Sederoff RR (2013) A transcriptome-based genetic map of Chinese chestnut (Castanea mollissima) and identification of regions of segmental homology with peach (Prunus persica). Tree Genet Genomes 9:557–571

    Google Scholar 

  61. LaBonte NR, Zhao P, Woeste K (2018) Signatures of selection in the genomes of Chinese chestnut (Castanea mollissima Blume): the roots of nut tree domestication. Front Plant Sci 9

  62. Labuschagné IF, Louw JH, Schmidt K, Sadie A (2003) Budbreak number in apple seedlings as selection criterion for improved adaptability to mild winter climates. HortScience 38:1186–1190

    Google Scholar 

  63. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis information resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210

    CAS  PubMed  Google Scholar 

  64. Lang P, Dane F, Kubisiak TL, Huang H (2007) Molecular evidence for an Asian origin and a unique westward migration of species in the genus Castanea via Europe to North America. Mol Phylogenet Evol 43:49–59

    CAS  PubMed  Google Scholar 

  65. Lee DS, Kim YC, Kwon SJ, Ryu CM, Park OK (2017) The Arabidopsis cysteine-rich receptor-like kinase CRK36 regulates immunity through interaction with the cytoplasmic kinase BIK1. Front Plant Sci 8:1856

    PubMed  PubMed Central  Google Scholar 

  66. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Liu Z, Zhu H, Abbott A (2015) Dormancy behaviors and underlying regulatory mechanisms: from perspective of pathways to epigenetic regulation. Advances in Plant Dormancy 75–105

  68. Luo M-C, You FM, Li P, Wang JR, Zhu T, Dandekar AM, Leslie CA, Aradhya M, McGuire PE, Dvorak J (2015) Synteny analysis in Rosids with a walnut physical map reveals slow genome evolution in long-lived woody perennials. BMC Genomics 16:707

    PubMed  PubMed Central  Google Scholar 

  69. Madoui M-A, Engelen S, Cruaud C, Belser C, Bertrand L, Alberti A, Lemainque A, Wincker P, Aury JM (2015) Genome assembly using nanopore-guided long and error-free DNA reads. BMC Genomics 16:327

    PubMed  PubMed Central  Google Scholar 

  70. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Miedes E, Vanholme R, Boerjan W, Molina A (2014) The role of the secondary cell wall in plant resistance to pathogens. Front Plant Sci 5:358

    PubMed  PubMed Central  Google Scholar 

  72. Naveed ZA, Huguet-Tapia JC, Ali GS (2019) Transcriptome profile of Carrizo citrange roots in response to Phytophthora parasitica infection. J Plant Interact 14:187–204

    CAS  Google Scholar 

  73. Nelson CD, Powell WA, Maynard CA, et al (2014) the forest health initiative, american chestnut (castanea dentata) as a model for forest tree restoration: biological research program. acta horticulturae 179–189

  74. Nielsen R, Korneliussen T, Albrechtsen A, Li Y, Wang J (2012) SNP calling, genotype calling, and sample allele frequency estimation from new-generation sequencing data. PLoS One 7:e37558

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Olukolu BA, Nelson CD, Abbott AG (2012) Mapping resistance to Phytophthora cinnamomi in chestnut (Castanea sp.). In: In: Sniezko, Richard A.; Yanchuk, Alvin D.; Kliejunas, John T.; Palmieri, Katharine M.; Alexander, Janice M.; Frankel, Susan J., tech. coords. Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: Disease and insect resistance in forest trees. Gen. Tech. Rep. PSW-GTR-240. Albany, CA: Pacific Southwest Research Station, Forest Service, US Department of Agriculture. p. 177. p 177

  76. Pereira-Lorenzo S, Costa R, Anagnostakis S, et al (2016) Interspecific hybridization of chestnut. Polyploidy and hybridization for crop improvement Boca Raton 377–407

  77. Plomion C, Aury J-M, Amselem J, Leroy T, Murat F, Duplessis S, Faye S, Francillonne N, Labadie K, le Provost G, Lesur I, Bartholomé J, Faivre-Rampant P, Kohler A, Leplé JC, Chantret N, Chen J, Diévart A, Alaeitabar T, Barbe V, Belser C, Bergès H, Bodénès C, Bogeat-Triboulot MB, Bouffaud ML, Brachi B, Chancerel E, Cohen D, Couloux A, da Silva C, Dossat C, Ehrenmann F, Gaspin C, Grima-Pettenati J, Guichoux E, Hecker A, Herrmann S, Hugueney P, Hummel I, Klopp C, Lalanne C, Lascoux M, Lasserre E, Lemainque A, Desprez-Loustau ML, Luyten I, Madoui MA, Mangenot S, Marchal C, Maumus F, Mercier J, Michotey C, Panaud O, Picault N, Rouhier N, Rué O, Rustenholz C, Salin F, Soler M, Tarkka M, Velt A, Zanne AE, Martin F, Wincker P, Quesneville H, Kremer A, Salse J (2018) Oak genome reveals facets of long lifespan. Nat Plants 4:440–452

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Raaymakers TM, Van den Ackerveken G (2016) Extracellular recognition of Oomycetes during biotrophic infection of plants. Front Plant Sci 7:906

    PubMed  PubMed Central  Google Scholar 

  80. Raes J, Rohde A, Christensen JH, van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Ramos AM, Usié A, Barbosa P, Barros PM, Capote T, Chaves I, Simões F, Abreu I, Carrasquinho I, Faro C, Guimarães JB, Mendonça D, Nóbrega F, Rodrigues L, Saibo NJM, Varela MC, Egas C, Matos J, Miguel CM, Oliveira MM, Ricardo CP, Gonçalves S (2018) The draft genome sequence of cork oak. Sci Data 5:180069

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Ribeiro T, Loureiro J, Santos C, Morais-Cecílio L (2011) Evolution of rDNA FISH patterns in the Fagaceae. Tree Genet Genomes 7:1113–1122

    Google Scholar 

  83. Robinson SM, Bostock RM (2014) β-Glucans and eicosapolyenoic acids as MAMPs in plant-oomycete interactions: past and present. Front. Plant Sci 5:797

    Google Scholar 

  84. Santos C, Nelson CD, Zhebentyayeva T, Machado H, Gomes-Laranjo J, Costa RL (2017) First interspecific genetic linkage map for Castanea sativa x Castanea crenata revealed QTLs for resistance to Phytophthora cinnamomi. PLoS One 12:e0184381

    PubMed  PubMed Central  Google Scholar 

  85. Scotti-Saintagne C, Bodénès C, Barreneche T et al (2004) Detection of quantitative trait loci controlling bud burst and height growth in Quercus robur L. Theor Appl Genet 109:1648–1659

    CAS  PubMed  Google Scholar 

  86. Serrazina S, Santos C, Machado H, Pesquita C, Vicentini R, Pais MS, Sebastiana M, Costa R (2015) Castanea root transcriptome in response to Phytophthora cinnamomi challenge. Tree Genet Genomes 11

  87. Shi R, Sun Y-H, Li Q, Heber S, Sederoff R, Chiang VL (2010) Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant Cell Physiol 51:144–163

    CAS  PubMed  Google Scholar 

  88. Shim D, Ko J-H, Kim W-C, Wang Q, Keathley DE, Han KH (2014) A molecular framework for seasonal growth-dormancy regulation in perennial plants. Hortic Res 1:14059

    PubMed  PubMed Central  Google Scholar 

  89. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212

    PubMed  Google Scholar 

  90. Smit AFA, Hubley R, Green P (2015) RepeatMasker Open-4.0. 2013--2015

  91. Solovyev V (2004) Statistical approaches in eukaryotic gene prediction. Handbook of Statistical Genetics

    Google Scholar 

  92. 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

    PubMed  PubMed Central  Google Scholar 

  93. Steiner KC, Westbrook JW, Hebard FV, Georgi LL, Powell WA, Fitzsimmons SF (2017) Rescue of American chestnut with extraspecific genes following its destruction by a naturalized pathogen. New For 48:317–336

    Google Scholar 

  94. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293

    PubMed  PubMed Central  Google Scholar 

  96. Teixeira MA, Rajewski A, He J, Castaneda OG, Litt A, Kaloshian I (2018) Classification and phylogenetic analyses of the Arabidopsis and tomato G-type lectin receptor kinases. BMC Genomics 19:239

    PubMed  PubMed Central  Google Scholar 

  97. Tennessen JA, Madeoy J, Akey JM (2010) Signatures of positive selection apparent in a small sample of human exomes. Genome Res 20:1327–1334

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Toljamo A, Blande D, Kärenlampi S, Kokko H (2016) Reprogramming of strawberry (Fragaria vesca) root transcriptome in response to Phytophthora cactorum. PLoS One 11:e0161078

    PubMed  PubMed Central  Google Scholar 

  99. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & gray). Science 313:1596–1604

    CAS  PubMed  Google Scholar 

  100. Tuskan GA, Groover AT, Schmutz J, DiFazio SP, Myburg A, Grattapaglia D, Smart LB, Yin T, Aury JM, Kremer A, Leroy T, le Provost G, Plomion C, Carlson JE, Randall J, Westbrook J, Grimwood J, Muchero W, Jacobson D, Michener JK (2018) Hardwood tree genomics: unlocking woody plant biology. Front Plant Sci 9:1799

    PubMed  PubMed Central  Google Scholar 

  101. Vaattovaara A, Brandt B, Rajaraman S, Safronov O, Veidenberg A, Luklová M, Kangasjärvi J, Löytynoja A, Hothorn M, Salojärvi J, Wrzaczek M (2019) Mechanistic insights into the evolution of DUF26-containing proteins in land plants. Commun Biol 2:56

    PubMed  PubMed Central  Google Scholar 

  102. van den Berg N, Christie JB, Aveling TAS, Engelbrecht J (2018) Callose and β-1,3-glucanase inhibit Phytophthora cinnamomi in a resistant avocado rootstock. Plant Pathol 67:1150–1160

    Google Scholar 

  103. Veillet F, Gaillard C, Coutos-Thévenot P, La Camera S (2016) Targeting the AtCWIN1 gene to explore the role of invertases in sucrose transport in roots and during Botrytis cinerea infection. Front Plant Sci 7

  104. Verde I, Jenkins J, Dondini L, et al (2017) The peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics 18

  105. Westbrook JW, Zhang Q, Mandal MK, et al (2019) Genomic selection analyses reveal tradeoff between chestnut blight tolerance and genome inheritance from American chestnut (Castanea dentata) in (C. dentatax Prunus) x C. dentata backcross populations

  106. Wilkinson L (2011) ggplot2: elegant graphics for data analysis by WICKHAM, H. Biometrics 67:678–679

    Google Scholar 

  107. Williams SP, Gillaspy GE, Perera IY (2015) Biosynthesis and possible functions of inositol pyrophosphates in plants. Front Plant Sci 6:67

    PubMed  PubMed Central  Google Scholar 

  108. Xing Y, Liu Y, Zhang Q, Nie X, Sun Y, Zhang Z, Li H, Fang K, Wang G, Huang H, Bisseling T, Cao Q, Qin L (2019) Hybrid de novo genome assembly of Chinese chestnut (Castanea mollissima). Gigascience 8. https://doi.org/10.1093/gigascience/giz112

  109. Zentmyer GA (1988) Origin and distribution of four species of Phytophthora. Trans Br Mycol Soc 91:367–378

    Google Scholar 

  110. Zhebentyayeva T, Chandra A, Abbott AG, et al (2012) Genetic and genomic resources for mapping resistance to Phytophthora cinnamomi in chestnut. In: V International Chestnut Symposium 1019. pp 263–270

  111. Zhebentyayeva TN, Sisco PH, Georgi LL, Jeffers SN, Perkins MT, James JB, Hebard FV, Saski C, Nelson CD, Abbott AG (2019) Dissecting resistance to Phytophthora cinnamomi in interspecific hybrid chestnut crosses using sequence-based genotyping and QTL mapping. Phytopathology 109:1594–1604

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This project was funded by the Forest Health Initiative (https://foresthealthinitiative.org/) through grant # 137RFP#2008-011 to JEC. Support was also provided by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture grant 2016-67013-24581 to The American Chestnut Foundation. Additional support was provided through several grants-in-aid to JEC from The American Chestnut Foundation and to JEC and MES through the USDA National Institute of Food and Agriculture Federal Appropriations under Project PEN04532 (Accession number 1000326) and NE-1833, respectively. Construction of saturated genetic maps and root RNAseq dataset was partially supported by the Foundation for the Carolinas. Bioinformatics was supported by National Science Foundation (NSF) Award #1444573, “Standards and Cyberinfrastructure that Enable ‘Big-Data’ Driven Discovery for Tree Crop Research” (MES; PI Main). Emily Bellis was supported by NSF Postdoctoral Research Fellowships in Biology Grant No. 1711950. Rooksana Noorai was supported by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health under grant number P20GM109094.

We would like to thank Webb Miller, Ronald Sederoff, John Davis, Claude dePamphilis, Joshua Der, and Nicholas Wheeler for their enthusiastic guidance and assistance. We thank Qi Sun, Computational Biology Service Unit, Life Sciences Core Laboratories Center at Cornell University for conducting the initial MDS analysis.

Author information

Affiliations

Authors

Contributions

Margaret Staton contributed to bioinformatics, data analysis, and website development activities, including gene functional and structural annotation and comparative genomics, as well as being a major contributor to project design, obtaining grant support, and writing the manuscript; Charles Addo-Quaye conducted the sequence data QC and did all of the initial de novo sequence assemblies with Illumina and 454 sequence data and post-assembly analyses resulting in version 1.1 released to the public in January 2014; Nathaniel Cannon planned and conducted the hybrid de novo genome assemblies, conducted manual contig gap filling and merging, conducted the initial contig anchoring and whole-genome analyses, and participated in preparation of the manuscript; Jiali Yu assisted in anchoring scaffolds to chromosome positions, comparative genomics, and RNA sequence mapping and assembly and in manuscript writing; Tetyana Zhebentyayeva analyzed physical map contigs, selected BACs for FISH, constructed six saturated genetic maps for genome assembly, delineated QTL intervals for resistance to P. cinnamomi, participated in Tajima’s D and nucleotide diversity analyses, identified candidate genes, and contributed to writing; Matthew Huff contributed to the gene functional analysis and structural annotation and comparative genomics; Nurul Islam-Faridi conducted all in situ hybridization experiments and analysis; Shenghua Fan provided reference genetic map for genome assembly and QTL interval analysis for blight resistance in linkage group B for the coevolution study; Laura L. Georgi provided plant materials and phenotypic data, conducted crosses and inoculations, and was a PI on the USDA grant; C. Dana Nelson performed contig anchoring to the genetic maps, supervised the chestnut genetic linkage mapping and QTL analyses, and assisted in writing the manuscript; Emily Bellis produced and analyzed Tajima’s D data; Nathan Henry provided bioinformatics support, assisted in the website development and curation, and conducted the data analyses for figures and tables in the manuscript; Daniela I Drautz-Moses conducted the DNA and RNA sequencing and advised on sample collection and sequence analysis; Rooksana Noorai assembled and annotated the chestnut root transcriptome, leading to candidate gene identification; Stephen Ficklin provided data and analyses for the integrated genetic-physical map, BAC-end sequences, which led to the initial genome assemblies, as well as assisting in initial web portal development; Christopher Saski led BAC library construction, provided BAC-end sequence data, and provided oversight of and insights from the integrated genetic-physical map construction; Mihir Mandal prepared multi-tissue RNAs from Chinese chestnut seedlings, constructed cDNA libraries for sequencing, and assisted in RNA sequence data analyses; Tyler K Wagner and Nicole Zembower provided technical support in the lab and field throughout the project; Catherine Bodénès performed genetic linkage mapping and QTL analyses for bud burst on Quercus; Jason Holliday provided project design and RNA sequencing resources; Jared Westbrook led the USDA project supporting the hybrid de novo assembly and gap filling, as well as providing input on current TACF breeding and chestnut restoration efforts; Jesse Lasky helped plan analyses and contributed to interpreting results and writing the paper; Frederick Hebard led the TACF backcross breeding program, provided plant materials and phenotypic data, conducted crosses and inoculations, and was PI on the USDA grant; Stephan Schuster contributed to planning the sequencing and assembly approach, supervised the DNA and RNA sequencing, and assisted in proposal writing; Albert G Abbott advised on genetic mapping, participated in Tajima’s D analyses, organized the writing team, and made major contributions to manuscript preparation; John E Carlson obtained funding, provided overall project design and leadership, contributed to data analyses, and helped to prepare the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to John E. Carlson.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Data archiving statement

The chestnut genome versions 1.1, 3.2, and 4.2 are available at https://hardwoodgenomics.org. The website contains links to download the contigs, the anchored contig locations, and predicted genes, transcripts, and proteins and associated functional annotations. A J-Browse implementation for the whole genome is located at the URL https://hardwoodgenomics.org/tools/jbrowse/?data=chinese_chestnut. The raw and assembled sequences are also available at the NCBI BioProject No. PRJNA46687.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Submitting author Staton, Margaret

Communicated by M. Troggio

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Staton, M., Addo-Quaye, C., Cannon, N. et al. “A reference genome assembly and adaptive trait analysis of Castanea mollissima ‘Vanuxem,’ a source of resistance to chestnut blight in restoration breeding”. Tree Genetics & Genomes 16, 57 (2020). https://doi.org/10.1007/s11295-020-01454-y

Download citation

Keywords

  • Chestnut
  • Genome
  • In situ hybridization
  • Disease resistance
  • Chestnut blight
  • Phytophthora root rot