White pine blister rust: the nemesis of North American white pines

1. White pine blister rust:the nemesis of North American white pines A presentation by Kristen M. Baker

2. Blister rust cankers: sugar pine whitebark pine

3. Top kill in whitebark pine

4. Complex system involving 5 spore stages and two hosts Pinus and Ribes Introduced into North America around 1900 on infected eastern white pine stock; separate introductions on east and west coasts Native and Asia Cronartium ribicola:the causal agent

5. C. ribicola life cycle

6. Low genetic diversity in N.A. High diversity between subpopulations Indicative of frequent founder events and little gene flow Genetic center: Asia To infect white pines: 48 hours <68 F, 100% relative humidity A Few Pathogen Details

7. Ribes eradication Not successful except a few isolated incidents Use of Risk Zones for planting and management potential pitfalls: must also account for airflow patterns Pruning Can be successful; costly; may need repeated entries; probably would not work in whitebark Genetics: probably most successful method Sugar and western white pines Whitebark pine work in progress Attempts to control WPBR

8. Widespread mortality in western white pine

9. Pruning research in sugar pine before...

10. Pruning research in sugar pine ...after

11. Genus Pinus Hapoxylon subgroup Five-needled Eastern and western white pines, whitebark, sugar, limber, southwestern white, foxtail (and potentially the bristlecone pines) Whitebark is closely related to European stone pines, where rust is endemic The tree host: white pines

12. Some details on Pinus

13. Largely cut over prior to rust, so loss due to rust minimal, but regenerating difficult Only tree where Ribes control was mildly successful Most land managers won’t risk it in high risk zones Eastern white pine (P. strobus)

14. High elevations in the western US and Canada Keystone species; slow growth Mutualistic relationship with nutcracker Wildlife dependence on nuts Restoration treatments: a helping hand for a tree with a bleak future Whitebark pine (P. albicaulis)

15. Largely disappeared from the Inland Northwest, where it was once most valuable timber species Like eastern, avoided in plantings Changing species comp. and structure made forest more susceptible to fire, insects and other pathogens Western white pine (P. monticola)

16. CA and PNW Tree of largest stature in mixed-conifer forests Few native pests, none causing such widespread mortality Also avoided in some planted settings Sugar pine (P. lambertiana)

17. Major gene for resistance Found in sugar, western white, and southwestern white so far Thought to be gene-for-gene (because virulent race of pathogen neutralizes this gene) Gene-for-gene typically indicates a pathosystem in which the host and pathogen have evolved over long time periods- so what is going on in this system? Tree resistance

18. A quick review of gene-for-gene resistance

19. Lesion types: sugar pine

20. Sugar pine Slow rusting resistance - many components of resistance combined into a single phenotypic expression, exhibited as amount and type of infection with moderately strong inheritance and independently inherited expressions (low infection # and high infection abortion) Ontogenetic resistance - another phenotypic expression that develops as the tree ages; under genetic controls; offspring may be fully susceptible Additional types of tree resistance

21. Western white pine Slow canker growth - non race specific trait; produces abnormally small cankers; may reduce pruning necessity (due to success) Reduced needle lesion frequency - also non race specific trait; few individual infection sites per seedling; may only be juvenile trait (seen in cotyledons) Additional types of tree resistance, cont’d

22. References Dahir, S.E. and J.E. Cummings Carlson. 2001. Incidence of white pine blister rsut in a high-hazard region of Wisconsin. Nor. J. App. For. 18:(3): 81-86. Ekramoddoullah, A.K.M. and Y. Tan. 1998. Differential accumulation of proteins in resistant and susceptible sugar pine (Pinus lambertiana) seedlings inoculated with the white pine blister rust fungus (Cronartium ribicola). Can. J. Plant Path. 20:(3): 308-318. Ekramoddoullah, A.K.M., Y. Tan, X. Yu, D.W. Taylor and S. Misra. 1999. Identification of a protein secreted by the blister rust fungus Cronartium ribicola in infected white pines and its cDNA cloning and characterization. Can. J. Bot. 77:(6): 800-808. Et-touil, K., L. Bernier, J. Beaulieu, J.A. Berube, A. Hopkin and R.C. Hamelin. 1999. Genetic structure of Cronartium ribicola populations in eastern Canada. Phytopathology 89:(10): 915-919. Gitzendanner, M.A., E.E. White, B.M. Foord, G.E. Dupper, P.D. Hodgskiss and B.B. Kinloch. 1996. Genetics of Cronartium ribicola: III. Mating system. Canadian Journal of Botany 74:(11): 1852-1859. Hamelin, R.C., M. Dusabenyagasani and K. Et-Touil. 1998. Fine-level genetic structure of white pine blister rust populations. Phytopathology 88:(11): 1187-1191. Hamelin, R.C., R.S. Hunt, B.W. Geils, G.D. Jensen, V. Jacobi and N. Lecours. 2000. Barrier to gene flow between eastern and western populations of Cronartium ribicola in North America. Phytopathology 90:(10): 1073-1078. Harkins, D.M., G.N. Johnson, P.A. Skaggs, A.D. Mix, G.E. Dupper, M.E. Devey, B.B. Kinloch and D.B. Neale. 1998. Saturation mapping of a major gene for resistance to white pine blister rust in sugar pine. Theor. App. Gen. 97:(8): 1355-1360. Hessburg, P.F., B.G. Smith, R.B. Salter, R.D. Ottmar and E. Alvarado. 2000. Recent changes (1930's-1990's) in spatial patterns of interior northwest forests, USA. For. Ecol. Man. 136:53-83. Hoff, R. and S. Hagle. 1990. Diseases of whitebark pine with special emphasis on white pine blister rust. Pp. 179-190. In: W.C. Schmidt & K.J. McDonald (ed.) Proceedings-Symposium on whitebark pine ecosystems: Ecology and management of a high-mountain resource, USDA For. Serv. Int. Res. Stn. Gen. Tech. Rep. INT-270 Hoff, R.J., R.T. Bingham and G.I. McDonald. 1980. Relative blister rust resistance of white pines. European J. For. Path. 10:307-316. Hoff, R.J. and G.I. McDonald. 1971. Resistance to Cronartium ribicola in Pinus monticola: short shoot fungicidal reaction. Can. J. Bot. 49:1235-1239. Hunt, R.S. 1998. Pruning western white pine in British Columbia to reduce white pine blister rust losses: 10-year results. W. J. App. For. 13:(2): 60-63. Hunt, R.S. 2000. White pine blister rust, root disease, and bears. Western Journal of Applied Forestry 15:(1): 38-39. Hunt, R.S. 2002. Relationship between early family-selection traits and natural blister rust cankering in western white pine families. Can. J. Plant Path. 24:200-204. Hunt, R.S. and G.D. Jensen. 2001. Frequency of resistant western white pine seedlings from parents of different phenotypes. West. J. Appl. For. 16:(4): 149-152.

23. References, cont’d Kinloch, B.B. and G.E. Dupper. 1996. Genetics of Cronartium ribicola. I. Axenic culture of haploid clones. Canadian Journal of Botany 74:(3): 456-460. Kinloch, B.B. and G.E. Dupper. 1999. Evidence of cytoplasmic inheritance of virulence in Cronartium ribicola to major gene resistance in sugar pine. Phytopathology 89:(3): 192-196. Kinloch, B.B., Jr. and G.E. Dupper. 2002. Genetic specificity in the white pine-blister rust pathosystem. Phytopathology 92:278-280. Kinloch, B.B., Jr. and J.L. Littlefield. 1977. White pine blister rust: hypersensitive resistance in sugar pine. Can. J. Bot. 55:1148-1155. Kinloch, B.B., R.D. Westfall, E.E. White, M.A. Gitzendanner, G.E. Dupper, B.M. Foord and P.D. Hodgskiss. 1998. Genetics of Cronartium ribicola: IV. Population structure in western North America. Canadian Journal of Botany 76:(1): 91-98. Kliejunas, J.T. 1985. Spread and intensification of white pine blister rust in the southern Sierra Nevada. Phytopathology 75:(11): 1367. Maloy, O.C. 1997. White pine blister rust control in North America: A case history. Ann. Rev. Phytopath. 35:87-109. McDonald, G.I. and R.J. Hoff. 1971. Resistance to Cronartium ribicola in Pinus monticola: Genetic control of needle-spots-only resistance factors. Can. J. For. Res. 1:(4): 197-202. Ostrofsky, W.D., T. Rumpf, D. Struble and R. Bradbury. 1988. Incidence of white pine blister rust in Maine after 70 years of a Ribes eradication program. Plant Dis. 72:(11): 967-970. Smith, J.P. and J.T. Hoffman. 2001. Site and stand characteristics related to white pine blister rust in high-elevation forests of southern Idaho and estern Wyoming. West. Nor. Am. Nat. 61:(4): 409-416. Smith, R.S., Jr. 1992. Spread and intensification of blister rust in the range of sugar pine. Pp. 112-118. In: B.B. Kinloch, Jr., M. Marosy & M.E. Huddleston (ed.) Sugar pine: Status, vaues, and roles in ecosystems, University of California Div. of Ag. and Nat. Res., University of California, Davis Pub. 3362. White, E.E., B.M. Foord and B.B. Kinloch. 1996. Genetics of Cronartium ribicola. II. Variation in the ribosomal gene cluster. Canadian Journal of Botany 74:(3): 461-468. Woo, K.S., L. Fins, G.I. McDonald and M.V. Wiese. 2001. Differences in needle morphology between blister rust resistant and susceptible western white pine stocks. Can. J. For. Res. 31:1880-1886. Yu, X., A.K.M. Ekramoddoullah, D.W. Taylor and N. Piggott. 2002. Cloning and characterization of a cDNA of cro rI from the white pine blister rust fungus Cronartium ribicola. Fungal Gen. Biol. 35:53-66. Zeglen, S. 2002. Whitebark pine and white pine blister rust in British Columbia, Canada. Can. J. For. Res. 32:1265-1274.