Rescue of American chestnut with extraspecific genes following its destruction by a naturalized pathogen

New Forests

Volumn 48, Issue 2, 2017, Pages 317-336

  Steiner, Kim C ^a   Westbrook, Jared W ^b   Hebard, Frederick V ^c   Georgi, Laura L ^d   Powell, William A ^e   Fitzsimmons, Sara F ^f  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b The American Chestnut Foundation   (United States)

^c American Chestnut Foundation   (United States)

^d American Chestnut Foundation   (United States)

^e STATE UNIVERSITY OF NEW YORK   (United States)

^f American Chestnut Foundation North Central Regional Office   (United States)

Author keywords

Breeding; Castanea dentata; Castanea mollissima; Cryphonectria parasitica; Restoration; Transgenics

Indexed keywords

GENES; IMAGE RECONSTRUCTION; PATHOGENS; RESTORATION;

BREEDING; CASTANEA DENTATA; CASTANEA MOLLISSIMA; CRYPHONECTRIA; TRANSGENICS;

FRUITS;

BREEDING; DISEASE RESISTANCE; FUNGAL DISEASE; FUNGUS; NUT; PATHOGEN; PEST DAMAGE; RESTORATION ECOLOGY; TRANSGENIC PLANT;

CASTANEA DENTATA; CASTANEA MOLLISSIMA; CRYPHONECTRIA PARASITICA; HEXAPODA;

EID: 85006513225     PISSN: 01694286     EISSN: 15735095     Source Type: Journal    
DOI: 10.1007/s11056-016-9561-5     Document Type: Article

References (75)

1. Anagnostakis SL (2012) Chestnut breeding in the United States for disease and insect resistance. Plant Dis 96:1392–1403
2. Baier KM (2010) Interspecific suppression subtractive hybridization identifies a differentially expressed Chinese chestnut (Castanea mollissima) laccase-like gene. M.S. thesis, State University of New York College of Environmental Science and Forestry, Syracuse, NY
3. Barakat A et al (2012) Chestnut resistance to the blight disease: insights from transcriptome analysis. BMC Plant Biol 12:38
4. Beavis WD (1994) The power and deceit of QTL experiments: Lessons from comparative QTL studies. In: DB Wilkinson (ed) 49th Annual corn and sorghum research conference American seed trade association, Chicago, IL, pp 250–266
5. Burnham CR (1981) Blight resistant American chestnut: there’s hope. Plant Dis 65:459–460
6. Burnham CR (1988) The restoration of the American chestnut. Am Sci 76:478–487
7. Burnham CR, Rutter PA, French DW (1986) Breeding blight-resistant chestnuts. Plant Breed Rev 4:347–397
8. Chen C, Sun Q, Narayanan B, Nuss DL, Herzberg O (2010) Structure of oxalacetate acetylhydrolase, a virulence factor of the chestnut blight fungus. J Biol Chem 285:26685–26696
9. Clapper RB (1952) Relative blight resistance of some chestnut species and hybrids. J For 50:453–455
10. Clark SL, Schlarbaum SE, Saxton AM, Hebard FV (2016) Establishment of American chestnuts (Castanea dentata) bred for blight (Cryphonectria parasitica) resistance: influence of breeding and nursery grading. N For 47:243–270
11. Crandall BS, Gravatt GF, Ryan MM (1945) Root disease of Castanea species and some coniferous and broadleaf nursery stocks, caused by Phytophthora cinnamomi. Phytopathology 35:162–180
12. D’Amico KM, Horton TR, Maynard CA, Stehman SV, Oakes AD, Powell WA (2014) Assessing ectomycorrhizal associations on transgenic American chestnut compared to the wild-type, a conventionally-bred hybrid, and related Fagaceae species. Appl Environ Microbiol 81:100–108
13. Dalgleish HJ, Nelson CD, Scrivani JA, Jacobs DF (2016) Consequences of shifts in abundance and distribution of American chestnut for restoration of a foundation forest tree. Forests 7(1):9
14. 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
15. Donaldson PA, Anderson T, Lane BG, Davidson AL, Simmonds DH (2001) Soybean plants expressing an active oligomeric oxalate oxidase from the wheat gf-2.8 (germin) gene are resistant to the oxalate-secreting pathogen Sclerotina sclerotiorum. Physiol Mol Plant Pathol 59:297–307
16. Dong X et al (2008) Expressing a gene encoding wheat oxalate oxidase enhances resistance to Sclerotinia sclerotiorum in oilseed rape (Brassica napus). Planta 228:331–340
17. El-Kassaby YA, Lstiburek M (2009) Breeding without breeding. Genet Res 91:111–120
18. Fang G-C, Blackmon BP, Staton ME, Nelson CD, Kubisiak TL, Olukolu BA, Henry D, Zhebentyayeva T, Saski CA, Cheng C-H, Monsanto M, Ficklin S, Atkins M, Georgi LL, Barakat A, Wheeler N, Carlson JE, Sederoff R, Abbott AG (2012) A physical map of the Chinese chestnut (Castanea mollissima) genome, and its integration with the genetic map. Tree Genet Genomes 9:525–537
19. Fieldler CE, McKinney ST (2014) Forest structure, health, and mortality in two Rocky Mountain whitebark pine ecosystems: implications for restoration. Nat Areas J 34:290–299
20. Flower CE, Knight KS, Gonzalez-Meler MA (2013) Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash (Fraxinus spp.) mortality on forest carbon cycling and successional dynamics in the eastern United States. Biol Invasions 15:931–944
21. Gingrich SF (1967) Measuring and evaluating stocking and stand density in uplant hardwood forests in the central states. For Sci 13:38–53
22. Grattapaglia D, Resende MDV (2011) Genomic selection in forest tree breeding. Tree Genet Genomes 7:241–255
23. Gravatt F (1949) Chestnut blight in Asia and North America. Unasylva 3:2–7
24. Graves AH (1950) Relative blight resistance in species and hybrids of Castanea. Phytopathology 40:1125–1131
25. Griffin, GJ, Elkins JR, McCurdy D, Griffin SL (2006) Integrated use of resistance, hypovirulence, and forest management to control blight in American chestnut. In: Steiner, KC and JE Carlson (eds) Restoration of American chestnut to forest lands, pp 97–107. Proceedings of a conference and workshop, May 2006, The North Carolina Arboretum. United States National Park Service Natural Resources Report NPS/NCR/CUE/NRR-2006/001
26. Griffin GJ, Hebard FV, Wendt RW, Elkins JR (1983) Survival of American chestnut trees: evaluation of blight resistance and hypovirulence in Endothia parasitica. Phytopathology 73:1084–1092
27. Havir EA, Anagnostakis SL (1983) Oxalate production by virulent but not by hypovirulent strains of Endothia parasitica. Physiol Plant Pathol 23:369–376
28. Havir EA, Anagnostakis SL (1985) Oxaloacetate acetylhydrolase activity in virulent and hypovirulent strains of Endothia (Cryphonectria) parasitica. Physiol Plant Pathol 26:1–9
29. He X, Miyasaka SC, Fitch MMM, Khuri S, Zhu YJ (2013) Taro (Colocasia esculenta) transformed with a wheat oxalate oxidase gene for improved resistance to taro pathogen Phytophthora colocasiae. HortScience 48:22–27
30. Hebard FV (1994) The American Chestnut Foundation breeding plan: beginning and intermediate steps. J Am Chestnut Found 8(1):21–28
31. Hebard FV (2002) Meadowview notes 2001–2002. J Am Chestnut Found 16(1):7–18
32. Hebard FV (2004) Research objectives of the American Chestnut Foundation, 2004–2014. J Am Chestnut Found 18(2):13–19
33. Hebard FV (2006) The backcross breeding program of The American Chestnut Foundation. In: Steiner KC, Carlson JE (eds) Restoration of American chestnut to forest lands, pp 61–77. Proceedings of a conference and workshop, May 2006, The North Carolina Arboretum. United States National Park Service Natural Resources Report NPS/NCR/CUE/NRR-2006/001
34. Hebard FV (2012) The American Chestnut Foundation breeding program. In: Sniezko RA et al (eds) Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: disease and insect resistance in forest trees, pp 221–234. USDA Forest Service General Technical Report PSW-GTR-240, 372 pp
35. Hebard FV, Shain L (1988) Effects of virulent and hypovirulent Endothia parasitica and their metabolites on ethylene production by bark of American and Chinese chestnut and scarlet oak. Phytopathology 78:841–845
36. Hebard FV, Griffin GJ, Elkins JR (1984) Developmental histopathology of cankers incited by virulent and hypovirulent Endothia parasitica on susceptible and resistant chestnut trees. Phytopathology 74:140–149
37. Hepting GH (1974) Death of the American chestnut. J For Hist 18:60–67
38. Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133:170–181
39. Jacobs DF, Dalgleish HJ, Nelson CD (2013) A conceptual framework for restoration of threatened plants: the effective model of American chestnut (Castanea dentata) reintroduction. N Phytol 197:378–393
40. Jaynes RA (1978) Selecting and breeding blight-resistant chestnut trees. In: Proceedings of the American Chestnut symposium, Morgantown, WV, pp 4–6
41. Jeffers SN, Meadows IM, James JB, Sisco PH (2012) Resistance to Phytophthora cinnamomi among seedlings from backcross families of hybrid American chestnut. In: Sniezko RA et al (eds) Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: disease and insect resistance in forest trees, pp 194–195. USDA Forest Service Gen Tech Rep PSW-GTR-240, 372 pp
42. Jones C, Griffin GJ, Elkins JR (1980) Association of climatic stress with blight on Chinese chestnut in the eastern United States. Plant Dis 64:1001–1004
43. Kim KS, Min JY, Dickman MB (2008) Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant Microbe Interact 21:605–612
44. Kubisiak TL, Hebard FV, Nelson CD, Jhang 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
45. Kubisiak TL, Nelson CD, Staton ME, Zhebentyayeva T, Smith C, Olukolu BA, Fang G-C, 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 segmental homology with peach (Prunus persica). Tree Genet Genomes 9:557–571
46. Liang H, Maynard CA, Allen RD, Powell WA (2001) Increased Septoria musiva resistance in transgenic hybrid poplar leaves expressing a wheat oxalate oxidase gene. Plant Mol Biol 45:619–629
47. Livingstone DM, Hampton JL, Phipps PM, Grabau EA (2005) Enhancing resistance to Sclerotinia minor in peanut by expressing a barley oxalate oxidase gene. Plant Physiol 137:1354–1362
48. Lstiburek M, Hodge GR, Lachout P (2015) Uncovering genetic information from commercial forest plantations—making up for lost time using “breeding without breeding”. Tree Genet Genomes 11: Article 55
49. Maynard CA, Polin LD, LaPierre S, Rothrock RE, Powell WA (2006) American chestnut (Castanea dentata (Marsh.) Borkh.). In: Wang K (ed) Agrobacterium protocols, 2nd edn. Methods in molecular biology book series #344. Humana Press, Inc., Totowa, NJ, pp 239–251
50. McKay JW, Jaynes RA (1969) Chestnuts. In: Jaynes RA (ed) Handbook on North American nut trees. Northern Nut Growers’ Association, Knoxville, pp 264–286
51. Merkle SA, Wiecko AT, Watson-Pauley BA (1991) Somatic embryogenesis in American chestnut. Can J For Res 21:1698–1701
52. Meuwissen TH, Hayes BJ, Goddard ME (2001) Prediction of total genetic value using genome-wide dense marker maps. Genetics 157:1819–1829
53. Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338
54. Namkoong G (1991) Maintaining genetic diversity in breeding for resistance in forest trees. Ann Rev Phytopathol 29:325–342
55. Nelson CD, Powell WA, Merkle SA, Carlson JE, Hebard FV, Islam-Faridi N, Staton ME, Georgi L (2014) Chestnut. In: Ramawat K (ed) Tree biotechnology, chapter 1. CRC Press, Boca Raton, pp 3–35
56. Newhouse JR (1990) Chestnut blight. Sci Am 262(1):106–111
57. Newhouse AE, McGuigan LD, Baier KA, Valletta KE, Rottmann WH, Tschaplinski TJ, Maynard CA, Powell WA (2014) Transgenic American chestnuts show enhanced blight resistance and transmit the trait to T1 progeny. Plant Sci 228:88–97
58. Nyland RD (1996) Silviculture concepts and applications. The McGraw-Hill Companies, New York, p 633
59. Paillet FL (2002) Chestnut: history and ecology of a transformed species. J Biogeogr 29:1517–1530
60. Partridge-Telenko DE, Hu J, Livingstone DM, Shew BB, Phipps PM, Grabau EA (2011) Sclerotinia blight resistance in Virginia-type peanut transformed with a barley oxalate oxidase gene. Phytopathology 101:786–793
61. Pautasso M, Aas G, Queloz V, Holdenrieder O (2013) European ash (Fraxinus excelsior) dieback—a conservation biology challenge. Biol Conserv 158:37–49
62. Polin LD, Liang H, Rothrock R, Nishii M, Diehl D, Newhouse A, Nairn CJ, Powell WA, Maynard CA (2006) Agrobacterium-mediated transformation of American chestnut (Castanea dentata (Marsh.) Borkh.) somatic embryos. Plant Cell Tissue Organ Cult 84:69–79
63. Rizzo DM, Garbelotto M, Hansen EM (2005) Phytophthora ramorum: integrative research and management of an emerging pathogen in California and Oregon forests. Ann Rev Phytopathol 43:309–335
64. Schneider M, Droz E, Malnoë P, Chatot C, Bonnel E, Métraux JP (2002) Transgenic potato plants expressing oxalate oxidase have increased resistance to oomycete and bacterial pathogens. Potato Res 45:177–185
65. Sisco PH, Kubisiak TL, Casasoli M, Barreneche T, Kremer A, Clark C, Sederoff RR, Hebard FV, Villani F (2005) An improved genetic map for Castanea mollissima/Castanea dentata and its relationship to the genetic map of Castanea sativa. Acta Hortic 693:491–496
66. Sniezko RA, Yanchuk AD, Kliejunas JT, Palmieri KM, Alexander JM, Frankel SJ (Technical Coordinators) (2012) 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. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, CA, p 372
67. Staton ME, Zhebentyayeva T, Olukolu B, Fang GC, Nelson CD, 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: Article 744
68. Stephenson SL (1986) Changes in a former chestnut-dominated forest after a half century of succession. Am Midl Nat 116:173–179
69. Stephenson SL, Adams HS, Lipford ML (1991) The present distribution of chestnut in the upland forest communities of Virginia. Bull Torrey Bot Club 118:24–32
70. Tarcali G, Radocz L (2009) Experiences of a study trip in China on the research of chestnut blight fungus and gall wasp. Analele Universităţii din Oradea, Fascicula: Protecţia Mediului 14:410–419
71. Walz A, Zingen-Sell I, Loeffler M, Sauer M (2008) Expression of an oxalate oxidase gene in tomato and severity of disease caused by Botrytis cinerea and Sclerotinia sclerotiorum. Plant Pathol 57:453–458
72. Wheeler NC, Steiner KC, Schlarbaum SE, Neale DB (2015) The evolution of forest genetic and tree improvement research in the United States. J For 113:500–510
73. Yan B, Li Z, Huang H, Qin L (2007) Genetic diversity and population differentiation of chestnut blight fungus. Biochem Genet 45:487–506
74. Zhang B, Oakes AD, Newhouse AE, Baier KM, Maynard CA, Powell WA (2013) A threshold level of oxalate oxidase transgene expression reduces Cryphonectria parasitica-induced necrosis in a transgenic American chestnut (Castanea dentata) leaf bioassay. Transgenic Res 22:973–982
75. Zhebentyayeva T et al (2013) Genetic and genomic resources for mapping resistance to Phytophthora cinnamomi in chestnut. Acta Hortic 1019:263–270