Skip to main content

Advertisement

Log in

Prospects for developing durable resistance in populations of forest trees

  • Review
  • Published:
New Forests Aims and scope Submit manuscript

Abstract

Long-lived tree species face a myriad of biotic and abiotic threats over their lifetime, some of the most serious being the presence of non-native diseases or pests capable of killing greater than 95% of trees that are exposed to them. Fortunately, the genetic diversity in many of the affected species also includes some individuals and populations with genetic resistance. Over the last 50 years, applied resistance programs have been undertaken in a range of tree species in the U.S. and resistant parent trees have been selected, tested in seedling inoculation trials and in field trials, selections placed into seed orchards, and the resulting seed used for reforestation and restoration. Both major gene resistance (MGR) and quantitative resistance (QR) have been documented in these resistance programs. However, for each resistance program the question arises whether the resistance will be durable, permitting the species to be used in managed plantations, urban plantings or in native forest restoration over the long-term. Field plantings to-date indicate that in some cases virulence to MGR can arise relatively quickly and QR appears to offer the best opportunity for durability. Ultimately, more time and plantings will be needed to discern if resistance is durable in affected tree species. Changes in climate may alter dynamics that could influence durability of resistance. However, even in the case of virulence to MGR, the pathogen or pest may not spread throughout the range of plantings, and genetic resistance will likely continue to be an invaluable tool for species affected by diseases and pests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Availability of data and material

Not applicable.

Code availability

Not applicable.

References

  • Amerson HV, Nelson CD, Kubisiak TL, Kuhlman EG, Garcia SA (2015) Identification of nine pathotype-specific genes conferring resistance to Fusiform rust in loblolly pine (Pinus taeda L.). Forests 6:2739–2761. https://doi.org/10.3390/f6082739

    Article  Google Scholar 

  • Aukema JE, Leung B, Kovacs K, Chivers C, Britton KO, Englin J et al (2011) Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6:e24587. https://doi.org/10.1371/journal.pone.0024587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betlejewski F, Goheen DJ, Angwin PA, Sniezko RA (2011) Port-Orford-cedar root disease. Forest Pest Leaflet 131. U.S. Department of Agriculture, Forest Service, Washington, DC. https://www.fs.usda.gov/Internet/FSE_DOCUMENTS/stelprdb5346825.pdf

  • Bonello P, Campbell FT, Cipollini D, Conrad AO, Farinas C, Gandhi KJK et al (2020) Invasive tree pests devastate ecosystems-A proposed new response framework. Front for Glob Chang 3:2. https://doi.org/10.3389/ffgc.2020.00002

    Article  Google Scholar 

  • Bridgwater F, Kubisiak T, Byram T, Mckeand S (2004) Risk assessment with current deployment strategies for fusiform rust-resistant loblolly and slash pines. South J Appl for 29(2):80–87

    Article  Google Scholar 

  • Brown JKM (2015) Durable resistance of crops to disease: a Darwinian perspective. Rev Phytopathol 53:513–539

    Article  CAS  Google Scholar 

  • Buggs RJA (2020) Changing perceptions of tree resistance research. Plants People Planet 2:2–4. https://doi.org/10.1002/ppp3.10089

    Article  Google Scholar 

  • Chandrashekar M, Heather WA (1981) Temperature sensitivity of Populus spp. to races of Melampsora larici-populina. Phytopathology 71:421–424

    Article  Google Scholar 

  • Corwin JA, Kliebenstein DJ (2017) Quantitative resistance: more than just perception of a pathogen. Plant Cell 29:655–665

    Article  PubMed  PubMed Central  Google Scholar 

  • Cowger C, Brown JKM (2019) Durability of quantitative resistance in crops: greater than we know? Annu Rev Phytopathol 57:253–277. https://doi.org/10.1146/annurev-phyto-082718-100016

    Article  CAS  PubMed  Google Scholar 

  • Dudley NS, Jones TC, James RL, Sniezko RA, Cannon P, Borthakur D (2015) Applied disease screening and selection program for resistance to vascular wilt in Hawaiian Acacia koa. South for 77:65–73

    Article  Google Scholar 

  • Farjon A (2013) Chamaecyparis lawsoniana. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. <www.iucnredlist.org>. Downloaded on 13 July 2013

  • Fei S, Morin RS, Oswalt CM, Liebhold AM (2019) Biomass losses resulting from insect and disease invasions in US forests. Proc Natl Acad Sci USA 116(35):17371–17376. https://doi.org/10.1073/pnas.1820601116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geils BW, Hummer KE, Hunt RS (2010) White pines, Ribes, and blister rust: a review and synthesis. Forest Pathol 40:147–185

    Article  Google Scholar 

  • Hansen EM, Reeser P, Sutton W, Sniezko RA (2012) Methods for screening Port-Orford-cedar for resistance to Phytophthora lateralis. In: Sniezko RA, Yanchuk AD, Kliejunas GT, Palmieri KM, Alexander JM, Frankel SJ (eds) Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: disease and insect resistance in forest trees. General Technical Report PSW-GTR- 240. Albany, CA: Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture. pp 181–188

  • Kearns HSJ, Ferguson BA, Schwandt JW (2012) Performance of rust-resistant western white pine in operational plantations in northern Idaho: 1995–2006. Report No. 12–03. USDA Forest Service, Northern Region, Forest Health Protection; Missoula, Montana. 27

  • Hoff R, Bingham RT, McDonald GI (1980) Relative blister rust resistance of white pines. Eur J for Pathol 10:307–316. https://doi.org/10.1111/j.1439-0329.1980.tb00042.x

    Article  Google Scholar 

  • Hunt RS (2004) Environmental and inoculum-source effects on resistance of Idaho F2 western white pine in British Columbia. For Pathol 26:351–357. https://doi.org/10.1080/07060660409507152

    Article  Google Scholar 

  • Hunt RS (2005) Effect of plant age and length of growing season on the development of blister rust cankers in western white pine. Can J Plant Path 27:453–457. https://doi.org/10.1080/07060660509507245

    Article  Google Scholar 

  • Hunt RS, Murray M, Reich R, Rusch D, Woods A, Zeglen S (2018) Persistence of major gene resistance in western white pine (Pinus monticola) in British Columbia. In: Schoettle AW, Sniezko RA, Kliejunas JT (eds) Proceedings of the IUFRO joint conference: Genetics of five-needle pines, rusts of forest trees, and Strobusphere; 2014 June 15–20; Fort Collins, CO. Proc. RMRS-P-76. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. 149–150

  • Johnson R (1984) A critical analysis of durable resistance. Ann Rev Phytopathol 22:309–330

    Article  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kegley A, Sniezko RA (2004) Variation in blister rust resistance among 226 Pinus monticola and 217 P. lambertiana seedling families in the Pacific Northwest. In: Breeding and genetic resources of five-needle pines: growth, adaptability, and pest resistance; 2001 July 23–27; Medford, OR, USA. Edited by Sniezko RA, Samman S, Schlarbaum SE, and Kriebel HB. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO. pp 209–226

  • Kinloch BB Jr (2003) White pine blister rust in North America: past and prognosis. Phytopathology 93:1044–1047

    Article  PubMed  Google Scholar 

  • Kinloch BB Jr, Parks GK, Fowler CW (1970) White pine blister rust: simply inherited resistance in sugar pine. Science 167(3915):193–195. https://doi.org/10.1126/science.167.3915.193

    Article  PubMed  Google Scholar 

  • Kinloch BB Jr, Sniezko RA, Barnes GD, Greathouse TE (1999) A major gene for resistance to white pine blister rust in western white pine from the western Cascade Range. Phytopathology 889:861–867

    Article  Google Scholar 

  • Kinloch BB Jr, Sniezko RA, Dupper GE (2003) Origin and distribution of Cr2, a gene for resistance to white pine blister rust in natural populations of western white pine. Phytopathology 93:691–694

    Article  CAS  PubMed  Google Scholar 

  • Kinloch BB Jr, Sniezko RA, Dupper GE (2004) Virulence gene distribution and dynamics of the white pine blister rust pathogen in western North America. Phytopathology 94:751–758

    Article  CAS  PubMed  Google Scholar 

  • Kinloch BB Jr, Burton D, Davis DA, Westfall RD, Dunlap J, Vogler D (2012) Strong partial resistance to white pine blister rust in sugar pine. In: Sniezko RA, Yanchuck A, Kliejunas J et al. 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 PSWGTR-240. Albany, CA: U.S. Department of Agriculture, Forest Service, Pacific Southwest Research Station: 80–91

  • Kinloch BB Jr, Sniezko RA, Savin DP, Danchok R, Kegley A, Burton D, Dunlap J (2018) Patterns of variation in blister rust resistance in sugar pine (Pinus lambertiana). In: Schoettle AW, Sniezko RA, Kliejunas JT (eds) Proceedings of the IUFRO joint conference: Genetics of five-needle pines, rusts of forest trees, and Strobusphere; 2014 June 15–20; Fort Collins, CO. Proc. RMRS-P-76. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. 124–128. https://www.fs.usda.gov/treesearch/pubs/56712

  • Koch J, Pearson DE, Huebner CD, Young MK, Sniezko RA (2021) Restoration of landscapes and habitats affected by established invasive species. Chapter 8. pp 185–202. In: Poland TM, Patel-Weynand T, Finch DM, Miniat CF, Hayes DC, Lopez VM (eds) Invasive species in forests and rangelands of the United States: a comprehensive science synthesis for the United States forest sector. Springer, Heidelberg, Germany. 455 https://doi.org/10.1007/978-3-030-45367-1

  • Koester H, Savin DP, Buss M, Sniezko RA (2018) White pine blister rust hazard rating for 265 sites in southern Oregon, USA. In: Schoettle AW, Sniezko RA, Kliejunas JT (eds) Proceedings of the IUFRO joint conference: Genetics of five-needle pines, rusts of forest trees, and Strobusphere; 2014 June 15–20; Fort Collins, CO. Proc. RMRS-P-76. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station. pp 173–180. https://www.fs.usda.gov/treesearch/pubs/56733

  • Kovalchuk A, Kerio S, Oghenekaro AO, Jaber E, Raffaello T, Asiegbu FO (2013) Antimicrobial defences and resistance in forest trees: challenges and perspectives in a genomics era. Annu Rev Phytopathol 51:221–244. https://doi.org/10.1146/annurev-phyto-082712-102307

    Article  CAS  PubMed  Google Scholar 

  • Kusch S, Panstruga R (2017) mlo-based resistance: an apparently universal ‘weapon’ to defeat powdery mildew disease. Mol Plant Microbe Interact 30:179–189

    Article  CAS  PubMed  Google Scholar 

  • La Y-J (2009) Korean successes in controlling blister rust of Korean pine. In: Breeding and Genetic Resources of Five-Needle Pines Conference, Yangyang, Republic of Korea, 2008 September 22–26. Ed. By Noshad D, Noh E, King J, Sniezko RA. Yangyang: Korea Forest Research Institute. pp 1–9

  • Lovett GM, Weiss A, Liebhold AM, Holmes TP, Leung B, Lambert KF et al (2016) Nonnative forest insects and pathogens in the United States: impacts and policy options. Ecol Appl 26:1437–1455. https://doi.org/10.1890/15-1176

    Article  PubMed  PubMed Central  Google Scholar 

  • Lu P, Colombo SJ, Sinclair RW (2007) Cold hardiness of interspecific hybrids between Pinus strobus and P. wallichiana measured by post-freezing needle electrolyte leakage. Tree Physiol 27:243–250. https://doi.org/10.1093/treephys/27.2.243

    Article  PubMed  Google Scholar 

  • Luo M, Xie L, Chakraborty S, Wang A, Matny O, Jugovich M et al (2021) A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat Biotechnol 39:561–566. https://doi.org/10.1038/s41587-020-00770-x

    Article  CAS  PubMed  Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379. https://doi.org/10.1146/annurev.phyto.40.120501.101443

    Article  CAS  PubMed  Google Scholar 

  • McDonald GI, Zambino P, Sniezko RA (2004) Breeding rust-resistant five-needle pines in the western United States: lessons from the past and a look to the future. In: Breeding and genetic resources of five-needle pines: growth, adaptability, and pest resistance; 2001 July 23–27; Medford, OR, USA. Edited by Sniezko RA, Samman S, Schlarbaum SE, Kriebel HB. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO. pp 28–50

  • Mundt CC (2014) Durable resistance: a key to sustainable management of pathogens and pests. Infect Genet Evol 27:446–455. https://doi.org/10.1016/j.meegid.2014.01.011

    Article  PubMed  Google Scholar 

  • Naidoo S, Slippers B, Plett JM, Coles D, Oates CN (2019) The road to resistance in forest trees. Front Plant Sci 10:273. https://doi.org/10.3389/fpls.2019.00273

    Article  PubMed  PubMed Central  Google Scholar 

  • National Academies of Sciences, Engineering, and Medicine (2019) Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC. The National Academies Press. https://doi.org/10.17226/25221

  • Nelson CD, Koch JL (2017) Institute of forest tree breeding: improvement and gene conservation of iconic tree species in the 21st century. In: Sniezko, Richard A, Man G, Hipkins V, Woeste K, Gwaze D, Kliejunas JT, McTeague BA, tech. cords. Gene conservation of tree species—banking on the future. Proceedings of a workshop. Gen. Tech. Rep. PNW-GTR-963. Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station: 24–27

  • Nelson R, Wiesner-Hanks T, Wisser R, Balint-Kurti P (2018) Navigating complexity to breed disease-resistant crops. Nat Rev Genet 19:21–33. https://doi.org/10.1038/nrg.2017.82

    Article  CAS  PubMed  Google Scholar 

  • Pavan S, Jacobsen E, Visser RGF, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1. https://doi.org/10.1007/s11032-009-9323-6

    Article  PubMed  Google Scholar 

  • Pike CC, Koch J, Nelson CD (2021) Breeding for resistance to tree pests: successes, challenges, and a guide to the future. J for 119:96–105. https://doi.org/10.1093/jofore/fvaa049

    Article  Google Scholar 

  • Powell WA, Newhouse AE, Coffey V (2019) Developing blight-tolerant American chestnut trees. Cold Spring Harb Perspect Biol 11:a0345

    Article  Google Scholar 

  • Ribeiro do Vale FX, Parlevliet JE, Zambolim L (2001) Concepts in plant disease resistance. Fitopatol Bras 26:577–589

    Article  Google Scholar 

  • Showalter DN, Raffa KF, Sniezko RA, Herms DA, Liebhold AM, Smith JA et al (2018) Strategic development of tree resistance against forest pathogen and insect invasions in defense-free space. Front Ecol Evol 6:124. https://doi.org/10.3389/fevo.2018.00124

    Article  Google Scholar 

  • Singh SJ, Heather WA (1983) Temperature-light effects on resistance of poplar cultivars to Melampsora medusae THÜM. Euphytica 32:111–120. https://doi.org/10.1007/BF00036870

    Article  Google Scholar 

  • Sniezko RA, Koch J (2017) Breeding trees resistant to insects and diseases—putting theory into application. Biol Invas 19:3377–3400. https://doi.org/10.1007/s10530-017-1482-5

    Article  Google Scholar 

  • Sniezko RA, Kegley A, Danchok R, Long S (2007) Variation in resistance to white pine blister rust among whitebark pine families from Oregon and Washington—early results and implications for conservation. In: Goheen EM, Sniezko RA, tech. coords. Proceedings of the conference whitebark pine: a Pacific Coast perspective. 2006 August 27–31. Ashland, OR. R6-NR-FHP-2007–01. Portland, OR: Pacific Northwest Region, Forest Service, U.S. Department of Agriculture; pp 82–97

  • Sniezko RA, Kegley AJ, Danchok R (2008) White pine blister rust resistance in North American, Asian, and European species—results from artificial inoculation trials in Oregon. Ann for Res 51:53–66

    Google Scholar 

  • Sniezko RA, Mahalovich MF, Schoettle AW, Vogler DR (2011) Past and current investigations of the genetic resistance to Cronartium ribicola in high-elevation five-needle pines. In: Keane RE, Tomback DF, Murray MP, Smith CM (eds) The future of high-elevation, five-needle white pines in western North America: proceedings of the high five symposium. Proceedings RMRS-P-63. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station: pp. 246–264

  • Sniezko RA, Hamiln J, Hansen E, Lucas S (2012a) Nine year survival of 16 Phytophthora lateralis resistant and susceptible Port-Orford-cedar families in a southern Oregon field trial. pp 348–355. In: Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: Disease and insect resistance in forest trees. Edited by Sniezko RA, Yanchuk AD, Kliejunas JT, Palmieri KM, Alexander JM, Frankel SJ, and tech. coords (2012). Gen Tech Rep PSW-GTR-240. Albany, CA. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture. p 372

  • Sniezko RA, Hamlin J, Hansen EM (2012b) Operational program to develop Phytophthora lateralis-resistant populations of Port-Orford-cedar (Chamaecyparis lawsoniana). pp 65–79. In: Proceedings of the fourth international workshop on the genetics of host-parasite interactions in forestry: Disease and insect resistance in forest trees. Edited by Sniezko RA, Yanchuk AD, Kliejunas JT, Palmieri KM, Alexander JM, Frankel SJ, and tech. coords (2012). Gen Tech Rep PSW-GTR-240. Albany, CA. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture. p 372

  • Sniezko RA, Smith J, Liu J-J, Hamelin RC (2014) Genetic resistance to Fusiform rust in southern pines and white pine blister rust in white pines—a contrasting tale of two rust pathosystems—current status and future prospects. Forests 5:2050–2083. https://doi.org/10.3390/f5092050

    Article  Google Scholar 

  • Sniezko RA, Johnson JS, Savin DP (2020a) Assessing the durability, stability, and usability of genetic resistance to a non-native fungal pathogen in two pine species. Plants People Planet 2:57–68. https://doi.org/10.1002/ppp3.49

    Article  Google Scholar 

  • Sniezko RA, Johnson JS, Reeser P, Kegley A, Hansen EM, Sutton W, Savin DP (2020b) Genetic resistance to Phytophthora lateralis in Port-Orford-cedar (Chamaecyparis lawsoniana)—Basic building blocks for a resistance program. Plants People Planet 2:69–83. https://doi.org/10.1002/ppp3.10081

    Article  Google Scholar 

  • Thakur AK, Kumar P, Parmar N, Shandil RK, Aggarwal G, Srivastava GADK (2021) Achievements and prospects of genetic engineering in poplar: a review. New for. https://doi.org/10.1007/s11056-021-09836-3

    Article  Google Scholar 

  • Tomback DF, Achuff P (2010) Blister rust and western forest biodiversity: ecology, values and outlook for white pines. Forest Pathol 40:186–225. https://doi.org/10.1111/j.1439-0329.2010.00655.x

    Article  Google Scholar 

  • Wang Y, Bao Z, Zhu Y, Hua J (2009) Analysis of temperature modulation of plant defense against biotrophic microbes. Mol Plant Microbe Interact 22:498–506. https://doi.org/10.1094/MPMI-22-5-0498

    Article  CAS  PubMed  Google Scholar 

  • Weiss M, Sniezko RA, Puiu D, Crepeau MW, Stevens K, Salzberg SL et al (2020) Genomic basis of white pine blister rust quantitative disease resistance and its relationship with qualitative resistance. Plant J 104:365–376. https://doi.org/10.1111/tpj.14928

    Article  CAS  PubMed  Google Scholar 

  • Westbrook JW, Holliday JA, Newhouse AE, Powell WA (2020) A plan to diversify a transgenic blight-tolerant American chestnut population using citizen science. Plants People Planet 2:84–95. https://doi.org/10.1002/ppp3.10061

    Article  Google Scholar 

  • Westwood M, Oldfield S, Jerome D, Romero-Severson J (2017) Fraxinus pennsylvanica. The IUCN Red List of Threatened Species 2017:e.T61918934A61919002. https://doi.org/10.2305/IUCN.UK.2017-2.RLTS.T61918934A61919002.en. Downloaded on 18 May 2021

  • Yin K, Qiu J-L (2019) Genome editing for plant disease resistance: applications and perspectives. Phil Trans R Soc B 374:20180322. https://doi.org/10.1098/rstb.2018.0322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang XY, Lu Q, Sniezko RA, Song RQ, Man G (2010) Blister rusts in China: hosts, pathogens, and management. For Pathol 40:369–381

    Article  Google Scholar 

Download references

Acknowledgements

This paper came about as a perspective in contributing to the 2021 conference Society and Policy Influences on Biotechnology Risk Assessment for Restoration of Threatened Forest Tree Species. I thank the organizers Drs. Douglas Jacob and Kas Dumerose for the invitation to present and contribute to this special issue emanating from the conference. The USDA Forest Service provided support for R.A. Sniezko and associated resistance programs in white pines and Port-Orford-cedar. We thank Jim Hamlin for his suggestions on an earlier version. We also thank the two anonymous reviewers for their constructive comments of an earlier version of this paper that improved the final version.

Funding

The USDA Forest Service provide funding for RAS.

Author information

Authors and Affiliations

Authors

Contributions

RAS had the idea for the article, RAS and JJL reviewed the literature, RAS developed the first draft and JJL provide edits and added content. Both authors have read and approved the final manuscript.

Corresponding author

Correspondence to Richard A. Sniezko.

Ethics declarations

Conflict of interest

No conflicts of interest.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sniezko, R.A., Liu, JJ. Prospects for developing durable resistance in populations of forest trees. New Forests 54, 751–767 (2023). https://doi.org/10.1007/s11056-021-09898-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11056-021-09898-3

Keywords

Navigation