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Forest environment mediated intraspecific resistance of Eucalyptus marginata to Phytophthora cinnamomi

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Abstract

The effect of forest environments on the expression of intraspecific resistance in Eucalyptus marginata to Phytophthora cinnamomi was determined in three Jarrah Forest bioregion provenances. Temperature was varied by inoculating in summer and winter. A nested design was used to partition variation between inoculation time, between genotypes within provenances and between provenances. Intraspecific variation in the response of E. marginata to P. cinnamomi in the forest environments occurred as resistant-susceptibility continua from a few resistant to a few highly susceptible trees. Rates of lesion extension and girdling were significantly less for the winter than the summer inoculation. The distributions of rates of lesion extension and girdling were positively skewed for the winter inoculation. Coppice completely girdled by P. cinnamomi was 4–7 % in the winter inoculation compared to 30–73 % in the summer inoculation. Regional variation in intraspecific resistance in E. marginata to P. cinnamomi may account for the Park Block provenance having least girdled coppice by the pathogen and the greatest proportion of trees with the slowest rates of lesion development, compared to the other two provenances. Resistance to P. cinnamomi in native flora of south-western Australia has probably evolved as a fortuitous side effect of ecological fitting of functional traits that evolved in response to different sets of biotic and abiotic conditions that occurred before the introduction of the pathogen. Sowing seed from resistant E. marginata into communities would be an option for reactive restoration of infested areas or proactive intervention in threatened healthy communities, to ensure their survival and the conservation of ecosystem genetic and functional diversity.

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References

  • Abbott I, Loneragan O (1986) Ecology of jarrah (Eucalyptus marginata) in the northern jarrah forest of Western Australia. Research Bulletin 1, Department Conservation and Land Management, Perth

  • Agosta SJ, Klemens JA (2008) Ecological fitting by phenotypically flexible genotypes: implications for species associations, community assembly and evolution. Ecol Lett 11:1123–1134

    PubMed  Google Scholar 

  • Barrett LG, Kniskern JM, Bodenhausen N, Zhang W, Bergelson J (2009) Continua of specificity and virulence in plant host-pathogen interactions: causes and consequences. New Phytol 183:513–529

    Article  PubMed  Google Scholar 

  • Bennett IJ, McComb JA, Tonkin CM (1993) Inoculation of Eucalyptus marginata Donn ex Sm. (jarrah) clones with Phytophthora cinnamomi Rands in vitro and under glasshouse conditions. For Ecol Manage 57:115–124

    Article  Google Scholar 

  • Boesewinkel HJ (1976) Storage of fungal cultures in water. Trans Brit Mycol Soc 66:183–185

    Article  Google Scholar 

  • Brown BN (1977) Aspects of interaction between environmental factors, Eucalyptus spp., and pythiaceous fungi, especially Phytophthora cinnamomi. PhD thesis, University of Auckland

  • Bryan WC (1965) Testing shortleaf pine seedlings for resistance to infection by Phytophthora cinnamomi. US Forest Service Research Note SE-50. Southeastern Forest Experiment Station, North Carolina

  • Bunny FJ, Crombie DS, Williams MR (1995) Growth of lesions of Phytophthora cinnamomi in stems and roots of jarrah (Eucalyptus marginata) in relation to rainfall and stand density in mediterranean forest of Western Australia. Can J For Res 25:961–969

    Article  Google Scholar 

  • Butcher TB, Stukely MJC, Chester GW (1984) Genetic variation in resistance of Pinus radiata to Phytophthora cinnamomi. For Ecol Manage 8:197–220

    Article  Google Scholar 

  • Byrne M (2004) Genetic variation captured in dieback resistant jarrah clones. Report to ALCOA Ltd. Department of Conservation and Environment, Kensington

  • Byrne M, Moran GF, Stukely M, Emebiri LC, Williams ER (1997) Identification of QTL for resistance to Phytophthora cinnamomi in Eucalyptus marginata. In proceedings of the 11th Biennial Conference of the Australasian Plant Pathology Society, Perth, p. 111

  • Cahill D, Legge N, Grant B, Weste G (1989) Cellular and histological changes induced by Phytophthora cinnamomi in a group of plant species ranging from fully susceptible to fully resistant. Phytopathology 79:417–424

    Article  Google Scholar 

  • Cahill DM, Bennett IJ, McComb JA (1992) Resistance of micropropagated Eucalyptus marginata to Phytophthora cinnamomi. Plant Dis 76:630–632

    Article  Google Scholar 

  • Cahill DM, Bennett IJ, McComb JA (1993) Mechanisms of resistance to Phytophthora cinnamomi in clonal, micropropagated Eucalyptus marginata. Plant Pathol 42:865–872

    Article  Google Scholar 

  • Chapin FS, Autumn K, Pugnaire F (1993) Evolution of suites of traits in response to environmental stress. Am Nat 142:S78–S92

    Article  Google Scholar 

  • Davison EM, Shearer BL (1989) Phytophthora spp. in indigenous forests in Australia. N Z J For Sc 19:277–289

    Google Scholar 

  • Davison EM, Tay FCS (1989) Phenology of Eucalyptus marginata on sites infested with Phytophthora cinnamomi. Aust J Bot 37:193–206

    Article  Google Scholar 

  • Del Río JA, Báidez AG, Botía JM, Ortuño A (2003) Enhancement of phenolic compounds in olive plants (Olea europaea L.) and their influence on resistance against Phytophthora sp. Food Chem 83:75–78

    Article  Google Scholar 

  • Dell B, Havel JJ, Malajczuk N (1989) The jarrah forest. A complex mediterranean ecosystem. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Díaz S, Lavorel S, de Bello F, Quétier F, Grigulis K, Robson TM (2007) Incorporating plant functional diversity effects in ecosystem service assessments. PNAS 104:20684–20689

    Article  PubMed Central  PubMed  Google Scholar 

  • Dobrowolski MP, Tommerup IC, Shearer BL, O’Brien PA (2003) Three clonal lineages of Phytophthora cinnamomi in Australia revealed by microsatellites. Phytopathology 93:695–704

    Article  CAS  PubMed  Google Scholar 

  • Douhan GW, Fuller E, McKee B, Pond E (2011) Genetic diversity analysis of avocado (Persea americana Miller) rootstocks selected under greenhouse conditions for tolerance to phytophthora root rot caused by Phytophthora cinnamomi. Euphytica 182:209–217

    Article  Google Scholar 

  • Draper AD, Mircetich SM, Scott DH (1971) Vaccinium clones resistant to Phytophthora cinnamomi. HortSci 6:167–169

    Google Scholar 

  • Elliott M, Chastagner GA, DeBauw A, Dermott G, Sniezko RA (2012) A first look at genetic variation in resistance to the root pathogen Phytophthora cinnamomi using a range-wide collection of Pacific madrone (Arbutus menziesii). United States Department of Agriculture Forest Service Pacific Southwest Research Station Gen Tech Rep PSW-GTR-240:290-294

  • Gabor BK, Guillemet FB, Coffey MD (1990) Comparison of field resistance to Phytophthora cinnamomi in twelve avocado rootstock. HortSci 25:1655–1656

    Google Scholar 

  • Grant BR, Byrt PN (1984) Root temperature effects on the growth of Phytophthora cinnamomi in the roots of Eucalyptus marginata and E. calophylla. Phytopathology 74:179–184

    Article  Google Scholar 

  • Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910

    Article  Google Scholar 

  • Hanley ME, Lamont BB (2001) Herbivory, serotiny and seedling defence in Western Australian Proteaceae. Oecologica 126:409–417

    Article  Google Scholar 

  • Hanley ME, Lamont BB (2002) Relationships between physical and chemical attributes of congeneric seedlings: how important is seedling defence? Func Ecol 16:216–222

    Article  Google Scholar 

  • Harris JA, Kasaby FY, Smith IW (1985) Variations in mortality in families of Eucalyptus regnans caused by Phytophthora cinnamomi, up to 5 years after planting. Aust For Res 15:57–65

    Google Scholar 

  • Havel JJ (1975) Site-vegetation mapping in the northern jarrah forest (Darling Range). 1. Definition of site-vegetation types. Bulletin 86, Forests Department, Perth

  • Havel JJ (1979) Identification of vulnerable communities and prediction of disease spread. In: Old KM (ed) Phytophthora and Forest Management in Australia. CSIRO, Melbourne, pp 64–72

    Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319

    Article  CAS  PubMed  Google Scholar 

  • Hinesley LE, Parker KC, Benson DM (2000) Evaluation of seedling of Fraser, Momi, and Siberian fir for resistance to Phytophthora cinnamomi. HortSci 35:87–88

    Google Scholar 

  • Hüberli D, Tommerup IC, Calver MC, Colqhhoun IJ, Hardy GESJ (2002) Temperature and inoculation method influence disease phenotypes and mortality of Eucalyptus marginata clonal lines inoculated with Phytophthora cinnamomi. Australas Plant Pathol 31:107–118

    Article  Google Scholar 

  • Jeffrey SJ, Carter JO, Moodie KB, Beswick AR (2001) Using spatial interpolation to construct a comprehensive archive of Australian climate data. Environ Model Softw 16:309–330

    Article  Google Scholar 

  • Kamoun S (2001) Nonhost resistance to Phytophthora: novel prospects for classical problem. Curr Opin Plant Biol 4:295–300

    Article  CAS  PubMed  Google Scholar 

  • Kirby KN (1993) Advanced data analysis with SYSTAT. Van Nostrad Reinhold, New York

    Google Scholar 

  • Krebs SL, Wilson MD (2002) Resistance to Phytophthora root rot in contemporary Rhododendron cultivars. HortSci 37:790–792

    Google Scholar 

  • Maddox GD, Cappuccino N (1986) Genetic determination of plant susceptibility to an herbivorous insect depends on environment context. Evolution 40:863–866

    Article  Google Scholar 

  • Marks GC, Smith IW, Kasaby FY (1981) Trunk infection of Eucalyptus species by Phytophthora cinnamomi. Aust For Res 11:257–267

    Google Scholar 

  • McCredie TA, Dixon KW, Sivasithamparam K (1985) Variability in the resistance of Banksia L.f. species to Phytophthora cinnamomi Rands. Aust J Bot 33:629–637

    Article  Google Scholar 

  • McDougall KL, Hardy GESJ, Hobbs RJ (2007) Comparison of colonisation by Phytophthora cinnamomi in detached stem tissue of Eucalyptus marginata in relation to site disease status. Australas Plant Pathol 36:498–500

    Article  Google Scholar 

  • McKey D (1979) The distribution of secondary compounds within plants. In: Rosenthal GA, Janzen DH (eds) Herbivores. Their interaction with secondary plant metabolites. Academic Press, New York, pp 55–133

    Google Scholar 

  • Meyer EM, Ranney TG, Eaker TA, Ivors K (2009) Differential resistance of Gordoniea trees to Phytophthora cinnamomi. HortSci 44:1484–1486

    Google Scholar 

  • Miranda-Fontaíña ME, Fernández-López J, Vettraino AM, Vannini A (2007) Resistance of Castanea clones to Phytophthora cinnamomi: testing and genetic control. Silvae Genet 56:11–21

    Google Scholar 

  • Moran MD (2003) Arguments for rejecting the sequential Bonferroni in ecological studies. Oikos 100:403–405

    Article  Google Scholar 

  • Mouttet R, Kaplan I, Bearez P, Amiens-Desneux E, Desneux N (2013) Spatiotemporal patterns of induced resistance and susceptibility linking diverse plant parasites. Oecologica 173:1379–1386

    Article  Google Scholar 

  • Myers N (2001) Mediterranean-climate regions: glowing hotspots of diversity. J Medit Ecol 2157–163

  • Mysore KS, Ryu C-M (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97–104

    Article  CAS  PubMed  Google Scholar 

  • O’Brien EK (2007) Local adaption and genetic variation in south-western Australian forest trees: implications for restoration. PhD, University of Western Australia

  • O’Brien EK, Mazanec RA, Krauss SL (2007) Provenance variation of ecologically important taits of forest trees: implications for restoration. J Appl Ecol 44:583–593

    Article  Google Scholar 

  • O’Reilly-Wapstra JM, Potts BM, McArthur C, Davies NW (2005) Effects of nutrient variability on the genetic-based resistance of Eucalyptus globulus to a mammalian herbivore and on plant defensive chemistry. Oecologia 142:597–605

    Article  PubMed  Google Scholar 

  • Ockels FS, Eyles A, McPherson BA, Wood DL, Bonello P (2007) Phenolic chemistry of coast live oak response to Phytophthora ramorum infection. J Chem Ecol 33:1721–1732

    Article  CAS  PubMed  Google Scholar 

  • Osier TL, Lindroth RL (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148:293–303

    Article  PubMed  Google Scholar 

  • Podger FD (1972) Phytophthora cinnamomi, a cause of lethal disease in indigenous plant communities in Western Australia. Phytopathology 62:972–981

    Article  Google Scholar 

  • Ranathunge K, Thomas RH, Fang X, Peterson CA, Gijzen M, Bernards MA (2008) Soybean root suberin and partial resistance to root rot caused by Phytophthora sojae. Phytopathology 98:1179–1189

    Article  PubMed  Google Scholar 

  • Rausher MD (2001) Co-evolution and plant resistance to natural enemies. Nature 411:857–864

    Article  CAS  PubMed  Google Scholar 

  • Ritchie AL, Krauss SL (2012) A genetic assessment of ecological restoration success in Banksia attenuata. Restoration Ecol 20:441–449

    Article  Google Scholar 

  • Robin C (1992) Trunk inoculations of Phytophthora cinnamomi in red oaks. Eur J For Path 22:157–165

    Article  Google Scholar 

  • Schoettle AW, Klutsch JG, Sniezko RA (2012) Integrated regeneration, genetic resistance, and timing of intervention for the long-term sustainability of ecosystems challenged by non-native pests – a novel proactive approach. United States Department of Agriculture Forest Service Pacific Southwest Research Station Gen Tech Rep PSW-GTR-240:112-123

  • Shea SR, Gillen KJ, Leppard WI (1980) Seasonal variation in population levels of Phytophthora cinnamomi Rands in soil in diseased, freely drained Eucalyptus marginata Sm sites in the northern jarrah forest of south-western Australia. Prot Ecol 2:135–156

    Google Scholar 

  • Shearer BL, Crane CE (2012) Phytophthora cinnamomi visible necrotic lesion-colonisation relationships in native flora. Australas Plant Pathol 41:633–644

    Article  Google Scholar 

  • Shearer BL, Smith IW (2000) Diseases of eucalypts caused by soilborne species of Phytophthora and Pythium. In: Keane PJ, Kile GA, Podger FD, Brown BN (eds) Diseases and pathogens of eucalypts. CSIRO Publishing, Melbourne, pp 259–291

    Google Scholar 

  • Shearer BL, Tippett JT (1989) Jarrah dieback: the dynamics and management of Phytophthora cinnamomi in the jarrah (Eucalyptus marginata) forest of south-western Australia. Research Bulletin 3, Department Conservation and Land Management, Perth

  • Shearer BL, Michaelsen BJ, Warren HJ (1987a) Comparative behaviour of Phytophthora species in the secondary phloem of stems and excised roots of Banksia grandis and Eucalyptus marginata. Aust J Bot 35:103–110

    Article  Google Scholar 

  • Shearer BL, Shea SR, Deegan PM (1987b) Temperature-growth relationships of Phytophthora cinnamomi in the secondary phloem of roots of Banksia grandis and Eucalyptus marginata. Phytopathology 77:661–665

    Article  Google Scholar 

  • Shearer BL, Michaelsen BJ, Somerford PJ (1988) Effects of isolate and time of inoculation on invasion of secondary phloem of Eucalyptus spp. and Banksia grandis by Phytophthora spp. Plant Dis 72:121–126

    Article  Google Scholar 

  • Shearer BL, Crane CE, Cochrane A (2004) Quantification of the susceptibility of the native flora of the South-West Botanical Province, Western Australia, to Phytophthora cinnamomi. Aust J Bot 52:435–443

    Article  Google Scholar 

  • Shearer BL, Crane CE, Barrett S, Cochrane A (2007a) Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Aust J Bot 55:225–238

    Article  Google Scholar 

  • Shearer BL, Crane CE, Barrett S, Cochrane A (2007b) Assessment of threatened flora susceptibility to Phytophthora cinnamomi by analysis of disease progress curves in shadehouse and natural environments. Australas Plant Pathol 36:609–620

    Article  Google Scholar 

  • Shearer BL, Crane CE, Cochrane JA (2010) Variation in susceptibility to Phytophthora cinnamomi infection within the genus Lambertia. Aust J Bot 58:575–585

    Article  Google Scholar 

  • Shearer BL, Crane CE, Dunne CP (2012) Variation in vegetation cover between shrubland, woodland and forest biomes invaded by Phytophthora cinnamomi. Australas Plant Pathol 41:413–424

    Article  Google Scholar 

  • Shearer BL, Crane CE, Cochrane JA (2013a) Variation in susceptibility of Banksia (including Dryandra) to Phytophthora cinnamomi. Australas Plant Pathol 42:351–361

    Article  Google Scholar 

  • Shearer BL, Crane CE, Cochrane JA, Dunne CP (2013b) Variation in susceptibility of threatened flora to Phytophthora cinnamomi. Australas Plant Pathol 42:491–502

    Article  CAS  Google Scholar 

  • Smith IW, Marks GC (1986) Effect of moisture stress in Eucalyptus sieberi on growth of lesions caused by Phytophthora cinnamomi. Aust For Res 16:273–279

    Google Scholar 

  • Stukely MJC, Crane CE (1994) Genetically based resistance of Eucalyptus marginata to Phytophthora cinnamomi. Phytopathology 84:650–656

    Article  Google Scholar 

  • Tippett JT, Shea SR, Hill TC, Shearer BL (1983) Development of lesions caused by Phytophthora cinnamomi in the secondary phloem of Eucalyptus marginata. Aust J Bot 31:197–210

    Article  Google Scholar 

  • Tippett JT, Crombie DS, Hill TC (1987) Effect of phloem water relations on the growth of Phytophthora cinnamomi in Eucalyptus marginata. Phytopathology 77:246–250

    Article  Google Scholar 

  • Wink M (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochem 64:3–19

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful for the help of M Dillon and D Devlin with setting up the sites, R Fairman in harvesting inoculated coppice, H Warren for databasing and C Crane, J McComb and M Shearer for checking the manuscript.

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  1. Science Division, Department of Parks and Wildlife, Delivery Centre, Locked Bag 104, Bentley, WA, 6983, Australia

    B. L. Shearer, B. J. Michaelsen, P. J. Somerford & M. Williams

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  1. B. L. Shearer
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  2. B. J. Michaelsen
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  3. P. J. Somerford
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  4. M. Williams
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Correspondence to B. L. Shearer.

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Shearer, B.L., Michaelsen, B.J., Somerford, P.J. et al. Forest environment mediated intraspecific resistance of Eucalyptus marginata to Phytophthora cinnamomi . Australasian Plant Pathol. 43, 245–255 (2014). https://doi.org/10.1007/s13313-013-0263-6

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