Advertisement

Tree Genetics & Genomes

, 15:72 | Cite as

Independent QTL underlie resistance to the native pathogen Quambalaria pitereka and the exotic pathogen Austropuccinia psidii in Corymbia

  • Jakob B. Butler
  • Brad M. Potts
  • René E. Vaillancourt
  • David J. Lee
  • Geoff S. Pegg
  • Jules S. FreemanEmail author
Original Article
  • 86 Downloads
Part of the following topical collections:
  1. Disease Resistance

Abstract

Fungal diseases such as the exotic myrtle rust (Austropuccinia psidii), and the native Quambalaria shoot blight (QSB; caused by Quambalaria species including Q. pitereka), constitute a significant threat to both native forests and Corymbia plantations in Australia and overseas. We here use quantitative trait loci (QTL) analysis to understand the genetic architecture of resistance to these pathogens in C. torelliana and C. citriodora subsp. variegata. QTL analysis was undertaken using 360 genotypes from two F1 crosses of C. torelliana × C. citriodora subsp. variegata, phenotyped by controlled inoculation with the strain of A. psidii present in Australia and independent inoculations with two strains of Q. pitereka (QSB1 & QSB2). A total of 22 QTL were identified, six for rust and 16 for QSB. The QTL for resistance to A. psidii and Q. pitereka in these pedigrees were independent from one another since they were generally in different parts of the genome, with only one case of co-location (QTL peak location within ± 2 MB). The QTL for the different QSB strains all mapped to discrete locations. The QTL for QSB were generally of a greater effect size than those for A. psidii. Several co-locations with QTL for resistance to rust and other fungal pathogens found in another eucalypt, Eucalyptus globulus, were detected and the implications of this observation are discussed.

Keywords

QTL Corymbia Eucalypt Myrtle rust Quambalaria shoot blight Austropuccinia psidii 

Notes

Acknowledgements

The authors wish to thank Ben Gosney for his advice regarding methods to evaluate QTL co-location, Mervyn Shepherd for his contributions to the genetic mapping of the Corymbia cross and DAF staff John Oostenbrink and Tracey Menzies for field and nursery work associated with the study.

Funding information

This work was supported by the Australian Research Council (grant numbers DP140102552, DP110101621) and an Australian Government Research Training Program Scholarship.

Data archiving statement

New marker sequences are presented in the Online Resources. The Corymbia citriodora subsp. variegata genome assemblies will be published in the Comparative Genomics database (https://genomevolution.org/coge/) when the associated paper is prepared.

Supplementary material

11295_2019_1378_MOESM1_ESM.xlsx (271 kb)
ESM 1 (XLSX 270 kb)
11295_2019_1378_MOESM2_ESM.xlsx (50 kb)
ESM 2 (XLSX 50 kb)
11295_2019_1378_MOESM3_ESM.xlsx (50 kb)
ESM 3 (XLSX 50 kb)
11295_2019_1378_MOESM4_ESM.xlsx (14 kb)
ESM 4 (XLSX 14 kb)
11295_2019_1378_MOESM5_ESM.xlsx (14 kb)
ESM 5 (XLSX 14 kb)
11295_2019_1378_MOESM6_ESM.png (652 kb)
ESM 6 (PNG 651 kb)

References

  1. Alves AA, Rosado CCG, Faria DA, da Silva Guimaraes LM, Lau D, Brommonschenkel SH, Grattapaglia D, Alfenas AC (2012) Genetic mapping provides evidence for the role of additive and non-additive QTLs in the response of inter-specific hybrids of Eucalyptus to Puccinia psidii rust infection. Euphytica 183:27–38Google Scholar
  2. Anagnostakis SL (1987) Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79:23–37Google Scholar
  3. Asante KS, Brophy JJ, Doran JC, Goldsack RJ, Hibbert DB, Larmour JS (2001) A comparative study of the seedling leaf oils of the spotted gums: species of the Corymbia (Myrtaceae), section Politaria. Aust J Bot 49:55–66Google Scholar
  4. Balmelli G, Simeto S, Marroni V, Altier N, Diez JJ (2014) Genetic variation for resistance to Mycosphaerella leaf disease and Eucalyptus rust on Eucalyptus globulus in Uruguay. Australas Plant Pathol 43:97–107Google Scholar
  5. Barbour RC, Crawford AC, Henson M, Lee DJ, Potts BM, Shepherd M (2008) The risk of pollen-mediated gene flow from exotic Corymbia plantations into native Corymbia populations in Australia. For Ecol Manag 256:1–19Google Scholar
  6. Beenken L (2017) Austropuccinia: a new genus name for the myrtle rust Puccinia psidii placed within the redefined family Sphaerophragmiaceae (Pucciniales). Phytotaxa 297:53–61Google Scholar
  7. Berthon K, Esperon-Rodriguez M, Beaumont LJ, Carnegie AJ, Leishman MR (2018) Assessment and prioritisation of plant species at risk from myrtle rust (Austropuccinia psidii) under current and future climates in Australia. Biol Conserv 218:154–162Google Scholar
  8. Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW (1994) A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6:927–933PubMedPubMedCentralGoogle Scholar
  9. Brawner JT, Lee DJ, Hardner CM, Dieters MJ (2011) Relationships between early growth and Quambalaria shoot blight tolerance in Corymbia citriodora progeny trials established in Queensland, Australia. Tree Genet Genomes 7:759–772Google Scholar
  10. Brooker MIH (2000) A new classification of the genus Eucalyptus L'Hér. (Myrtaceae). Aust Syst Bot 13:79–148Google Scholar
  11. Burdon JJ, Thrall PH, Ericson L (2006) The current and future dynamics of disease in plant communities. Annu Rev Phytopathol 44:19–39PubMedGoogle Scholar
  12. Burgess TI, Wingfield MJ (2016) Pathogens on the move: a 100-year global experiment with planted eucalypts. Bioscience 67:14–25Google Scholar
  13. Butler JB, Freeman JS, Vaillancourt RE, Potts BM, Glen M, Lee DJ, Pegg GS (2016) Evidence for different QTL underlying the immune and hypersensitive responses of Eucalyptus globulus to the rust pathogen Puccinia psidii. Tree Genet Genomes 12:1–13Google Scholar
  14. Butler JB, Vaillancourt RE, Potts BM, Lee DJ, King GJ, Baten A, Shepherd M, Freeman JS (2017) Comparative genomics of Eucalyptus and Corymbia reveals low rates of genome structural rearrangement. BMC Genomics 18:397PubMedPubMedCentralGoogle Scholar
  15. Carnegie AJ (2007) Forest health condition in New South Wales, Australia, 1996–2005. II. Fungal damage recorded in eucalypt plantations during forest health surveys and their management. Australas Plant Pathol 36:225–239Google Scholar
  16. Carnegie AJ, Lidbetter JR, Walker J, Horwood MA, Tesoriero L, Glen M, Priest MJ (2010) Uredo rangelii, a taxon in the guava rust complex, newly recorded on Myrtaceae in Australia. Australas Plant Pathol 39:463–466Google Scholar
  17. Carnegie AJ, Pegg GS (2018) Lessons from the incursion of myrtle rust in Australia. Annu Rev Phytopathol 56:457–478PubMedGoogle Scholar
  18. Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L, Kanzaki H, Okuyama Y, Morel J-B, Fournier E, Tharreau D, Terauchi R, Kroj T (2013) The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 25:1463–1481PubMedPubMedCentralGoogle Scholar
  19. Cesari S (2017) Multiple strategies for pathogen perception by plant immune receptors. New Phytol 219:17–24PubMedGoogle Scholar
  20. Christie N, Tobias PA, Naidoo S, Külheim C (2016) The Eucalyptus grandis NBS-LRR gene family: physical clustering and expression hotspots. Front Plant Sci 6:1238PubMedPubMedCentralGoogle Scholar
  21. Chu HY, Wegel E, Osbourn A (2011) From hormones to secondary metabolism: the emergence of metabolic gene clusters in plants. Plant J 66:66–79PubMedGoogle Scholar
  22. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedPubMedCentralGoogle Scholar
  23. Coutinho T, Wingfield M, Alfenas A, Crous P (1998) Eucalyptus rust: a disease with the potential for serious international implications. Plant Dis 82:819–825PubMedGoogle Scholar
  24. Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511PubMedGoogle Scholar
  25. Cui L-G, Shan J-X, Shi M, Gao J-P, Lin H-X (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80:1108–1117Google Scholar
  26. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedGoogle Scholar
  27. Dickinson GR, Lee DJ, Huth JR (2004) Early plantation growth and tolerance to ramularia shoot blight of provenances of three spotted gum taxa on a range of sites in Queensland. Aust For 67:122–130Google Scholar
  28. Dickinson GR, Wallace HM, Lee DJ (2010) Controlled pollination methods for creating Corymbia hybrids. Silvae Genetica 59:233–241Google Scholar
  29. Dillon SK, Brawner JT, Meder R, Lee DJ, Southerton SG (2012) Association genetics in Corymbia citriodora subsp. variegata identifies single nucleotide polymorphisms affecting wood growth and cellulosic pulp yield. New Phytol 195:596–608PubMedGoogle Scholar
  30. Dowkiw A, Voisin E, Bastien C (2010) Potential of Eurasian poplar rust to overcome a major quantitative resistance factor. Plant Pathol 59:523–534Google Scholar
  31. Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477PubMedPubMedCentralGoogle Scholar
  32. Ennos RA (2015) Resilience of forests to pathogens: an evolutionary ecology perspective. Forestry: An International Journal of Forest Research 88:41–52Google Scholar
  33. Ferreira F (1983) Eucalyptus rust. Revista Arvore 7:91–109Google Scholar
  34. Field B, Osbourn AE (2008) Metabolic diversification - independent assembly of operon-like gene clusters in different plants. Science 320:543–547PubMedGoogle Scholar
  35. Flor H (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:e69Google Scholar
  36. Freeman JS, Potts BM, Vaillancourt RE (2008) Few Mendelian genes underlie the quantitative response of a forest tree, Eucalyptus globulus, to a natural fungal epidemic. Genetics 178:563–571PubMedPubMedCentralGoogle Scholar
  37. Freeman JS, Hamilton MG, Lee DJ, Pegg GS, Brawner JT, Tilyard PA, Potts BM (2018) Comparison of host susceptibility to native and exotic pathogens provides evidence for pathogen imposed selection in forest trees. New Phytol 221(4):2261–2272PubMedGoogle Scholar
  38. Giblin F, Carnegie A (2014) Puccinia psidii (Myrtle rust) - Australian host list. http://www.anpc.asn.au/myrtle-rust. Accessed 10 May 2018
  39. Glen M, Alfenas A, Zauza E, Wingfield M, Mohammed C (2007) Puccinia psidii: a threat to the Australian environment and economy—a review. Australas Plant Pathol 36:1–16Google Scholar
  40. Gosney BJ, Potts BM, O'Reilly-Wapstra JM, Vaillancourt RE, Fitzgerald H, Davies NW, Freeman JS (2016) Genetic control of cuticular wax compounds in Eucalyptus globulus. New Phytol 209:202–215PubMedGoogle Scholar
  41. Gosney BJ (2017) Community genetics of eucalypts: provenance effects on canopy communities, potential drivers and underlying QTL. PhD thesis, University of TasmaniaGoogle Scholar
  42. Healey A, Shepherd M, Baten A, King GJ, Lee DJ, Furtado A, Vaillancourt RE, Butler JB, Freeman JS, Potts BM, Grattapaglia D, Junior OBDS, Barry KW, Schmutz J, Simmons B, Henry RJ (2017) Sequencing the branches of the eucalypt tree: comparison between Eucalyptus and Corymbia genomes. In conference: Plant & Animal Genome Conference XXV, San Diego, United States of AmericaGoogle Scholar
  43. Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319PubMedGoogle Scholar
  44. Hill KD, Johnson LA (1995) Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6:185–504Google Scholar
  45. Hobert O (2008) Gene regulation by transcription factors and microRNAs. Science 319:1785–1786PubMedGoogle Scholar
  46. Höglund S, Rönnberg-Wästljung AC, Lagercrantz U, Larsson S (2012) A rare major plant QTL determines non-responsiveness to a gall-forming insect in willow. Tree Genet Genomes 8:1051–1060Google Scholar
  47. Hörger AC, Ilyas M, Stephan W, Tellier A, van der Hoorn RAL, Rose LE (2012) Balancing selection at the tomato RCR3 guardee gene family maintains variation in strength of pathogen defense. PLoS Genet 8:e1002813PubMedPubMedCentralGoogle Scholar
  48. Hsieh J-F, Chuah A, Patel HR, Sandhu KS, Foley WJ, Külheim C (2017) Transcriptome profiling of Melaleuca quinquenervia challenged by myrtle rust reveals differences in defense responses among resistant individuals. Phytopathology 108:495–509Google Scholar
  49. Hudson CJ, Freeman JS, Jones RC, Potts BM, Wong MM, Weller JL, Hecht VF, Poethig RS, Vaillancourt RE (2014) Genetic control of heterochrony in Eucalyptus globulus. G3 4:1235–1245PubMedGoogle Scholar
  50. Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Front Immunol 4:297PubMedPubMedCentralGoogle Scholar
  51. Jansen C, Von Wettstein D, Schäfer W, Kogel K-H, Felk A, Maier FJ (2005) Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci U S A 102:16892–16897PubMedPubMedCentralGoogle Scholar
  52. Johnson IG, Carnegie AJ, Henson M (2009) Growth, form and Quambalaria shoot blight tolerance of spotted gum in North-Eastern New South Wales, Australia. Silvae Genetica 58:180–191Google Scholar
  53. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329Google Scholar
  54. Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C (2005) Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection. New Phytol 167:113–127PubMedGoogle Scholar
  55. Junghans D, Alfenas A, Brommonschenkel S, Oda S, Mello E, Grattapaglia D (2003a) Resistance to rust (Puccinia psidii winter) in Eucalyptus: mode of inheritance and mapping of a major gene with RAPD markers. Theor Appl Genet 108:175–180PubMedGoogle Scholar
  56. Junghans DT, Alfenas AC, Maffia LA (2003b) Escala de notas para quantificação da ferrugem em Eucalyptus. Fitopatol Bras 28:184–188Google Scholar
  57. Kanzaki H, Saitoh H, Ito A, Fujisawa S, Kamoun S, Katou S, Yoshioka H, Terauchi R (2003) Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol Plant Pathol 4:383–391PubMedGoogle Scholar
  58. Karnosky DF (1979) Dutch elm disease: a review of the history, environmental implications, control, and research needs. Environ Conserv 6:311–322Google Scholar
  59. Kawanishi T, Uematsu S, Kakishima M, Kagiwada S, Hamamoto H, Horie H, Namba S (2009) First report of rust disease on ohia and the causal fungus, Puccinia psidii, in Japan. J Gen Plant Pathol 75:428–431Google Scholar
  60. Kim YJ, Lin N-C, Martin GB (2002) Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109:589–598PubMedGoogle Scholar
  61. Kinloch BB, Dupper GE (2002) Genetic specificity in the white pine-blister rust pathosystem. Phytopathology 92:278–280PubMedGoogle Scholar
  62. Kinloch BB (2003) White pine blister rust in North America: past and prognosis. Phytopathology 93:1044–1047PubMedGoogle Scholar
  63. Kubisiak TL, Roberds JH, Spaine PC, Doudrick RL (2003) Microsatellite DNA suggests regional structure in the fusiform rust fungus Cronartium quercuum f. sp fusiforme. Heredity 92:41Google Scholar
  64. Kushalappa AC, Yogendra KN, Karre S (2016) Plant innate immune response: qualitative and quantitative resistance. Crit Rev Plant Sci 35:38–55Google Scholar
  65. Lander E, Kruglyak L (1995) Genetic dissection of complex traits: guidelines for interpreting and reporting linkage results. Nat Genet 11:241–247PubMedGoogle Scholar
  66. Lanfear R, Ho SYW, Jonathan Davies T, Moles AT, Aarssen L, Swenson NG, Warman L, Zanne AE, Allen AP (2013) Taller plants have lower rates of molecular evolution. Nat Commun 4:1879PubMedGoogle Scholar
  67. Lawson SA, McDonald JM, Pegg GS (2008) Forest health surveillance methodology in hardwood plantations in Queensland, Australia. Aust For 71:177–181Google Scholar
  68. Lee DJ (2007) Achievements in forest tree genetic improvement in Australia and New Zealand 2: development of Corymbia species and hybrids for plantations in eastern Australia. Aust For 70:11–16Google Scholar
  69. Lee DJ, Huth JR, Brawner JT, Dickinson GR (2009) Comparative performance of Corymbia hybrids and parental species in subtropical Queensland and implications for breeding and deployment. Silvae Genetica 58:205–212Google Scholar
  70. Lind M, Källman T, Chen J, Ma X-F, Bousquet J, Morgante M, Zaina G, Karlsson B, Elfstrand M, Lascoux M, Stenlid J (2014) A Picea abies linkage map based on SNP markers identifies QTLs for four aspects of resistance to Heterobasidion parviporum infection. PLoS One 9:e101049PubMedPubMedCentralGoogle Scholar
  71. Lyons E, Freeling M (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J 53:661–673PubMedGoogle Scholar
  72. Makinson RO (2018) Myrtle rust reviewed: the impacts of the invasive pathogen Austropuccinia psidii on the Australian environment. Plant Biosecurity Cooperative Research Centre, CanberraGoogle Scholar
  73. Mamani EM, Bueno NW, Faria DA, Guimarães LM, Lau D, Alfenas AC, Grattapaglia D (2010) Positioning of the major locus for Puccinia psidii rust resistance (Ppr1) on the Eucalyptus reference map and its validation across unrelated pedigrees. Tree Genet Genomes 6:953–962Google Scholar
  74. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61PubMedGoogle Scholar
  75. McTaggart AR, Shuey LS, Granados GM, Ed P, Fraser S, Barnes I, Naidoo S, Wingfield MJ, Roux J (2018) Evidence that Austropuccinia psidii may complete its sexual life cycle on Myrtaceae. Plant Pathol 67:729–734Google Scholar
  76. Minchinton E, Smith D, Hamley K, Donald C (2014) Myrtle rust in Australia. Acta Hortic 1055:89–90Google Scholar
  77. Moerschbacher BM, Noll U, Ocampo CA, Flott BE, Gotthardt U, Wüslefeld A, Reisener H-J (1990) Hypersensitive lignification response as the mechanism of non-host resistance of wheat against oat crown rust. Physiol Plant 78:609–615Google Scholar
  78. Morin L, Aveyard R, Lidbetter JR, Wilson PG (2012) Investigating the host-range of the rust fungus Puccinia psidii sensu lato across tribes of the family Myrtaceae present in Australia. PLoS One 7:e35434PubMedPubMedCentralGoogle Scholar
  79. Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan ARK, Hussey SG, Pinard D, Merwe KVD, Singh P, Jaarsveld IV, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye C-Y, Li T, Sterck L, Vanneste K, Murat F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Peer YVD, Rokhsar DS, Schmut J (2014) The genome of Eucalyptus grandis. Nature 510:356–362Google Scholar
  80. Newcombe G, Bradshaw HD Jr (1996) Quantitative trait loci conferring resistance in hybrid poplar to Septoriapopulicola, the cause of leaf spot. Can J For Res 26:1943–1950Google Scholar
  81. Oh E, Hansen EM, Sniezko RA (2006) Port-Orford-cedar resistant to Phytophthora lateralis. For Pathol 36:385–394Google Scholar
  82. Paap T, Burgess TI, McComb JA, Shearer BL, St J, Hardy GE (2008) Quambalaria species, including Q. coyrecup sp. nov., implicated in canker and shoot blight diseases causing decline of Corymbia species in the southwest of Western Australia. Mycol Res 112:57–69PubMedGoogle Scholar
  83. Parra-O C, Bayly MJ, Drinnan A, Udovicic F, Ladiges P (2009) Phylogeny, major clades and infrageneric classification of Corymbia (Myrtaceae), based on nuclear ribosomal DNA and morphology. Aust Syst Bot 22:384–399Google Scholar
  84. Patharkar OR, Gassmann W, Walker JC (2017) Leaf shedding as an anti-bacterial defense in Arabidopsis cauline leaves. PLoS Genet 13:e1007132PubMedPubMedCentralGoogle Scholar
  85. Pegg GS, O'Dwyer C, Carnegie AJ, Burgess TI, Wingfield MJ, Drenth A (2008) Quambalaria species associated with plantation and native eucalypts in Australia. Plant Pathol 57:702–714Google Scholar
  86. Pegg GS, Webb R, Carnegie A, Wingfield M, Drenth A (2009) Infection and disease development of Quambalaria spp. on Corymbia and Eucalyptus species. Plant Pathol 58:642–654Google Scholar
  87. Pegg GS, Carnegie AJ, Wingfield MJ, Drenth A (2011) Variable resistance to Quambalaria pitereka in spotted gum reveal opportunities for disease screening. Australas Plant Pathol 40:76–86Google Scholar
  88. Pegg GS, Perry S, Carnegie A, Ireland K, Giblin F (2012) Understanding myrtle rust epidemiology and host specificity to determine disease impact in Australia. Cooperative research Centre for National Plant Biosecurity. Bruce, AustraliaGoogle Scholar
  89. Pegg GS, Brawner JT, Lee DJ (2014a) Screening Corymbia populations for resistance to Puccinia psidii. Plant Pathol 63:425–436Google Scholar
  90. Pegg GS, Giblin F, McTaggart A, Guymer G, Taylor H, Ireland K, Shivas R, Perry S (2014b) Puccinia psidii in Queensland, Australia: disease symptoms, distribution and impact. Plant Pathol 63:1005–1021Google Scholar
  91. Pegg GS, Taylor T, Entwistle P, Guymer G, Giblin F, Carnegie A (2017) Impact of Austropuccinia psidii (myrtle rust) on Myrtaceae-rich wet sclerophyll forests in south east Queensland. PLoS One 12:e0188058PubMedPubMedCentralGoogle Scholar
  92. Pegg GS, Lee DJ, Carnegie AJ (2018) Predicting impact of Austropuccinia psidii on populations of broad leaved Melaleuca species in Australia. Australas Plant Pathol 47:421–430Google Scholar
  93. Core Team R (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  94. Rae AM, Street NR, Robinson KM, Harris N, Taylor G (2009) Five QTL hotspots for yield in short rotation coppice bioenergy poplar: the poplar biomass loci. BMC Plant Biol 9:23PubMedPubMedCentralGoogle Scholar
  95. Rizzo DM, Garbelotto M (2003) Sudden oak death: endangering California and Oregon forest ecosystems. Front Ecol Environ 1:197–204Google Scholar
  96. Robin C, Amira M-H, Gion J-M, Kremer A, Desprez-Loustau M-L (2012) Quantitative trait loci for resistance to two fungal pathogens in Quercus robur. Pacific Southwest Research Station. Forest Service, U.S. Department of Agriculture, AlbanyGoogle Scholar
  97. Rockwood D, Rudie A, Ralph S, Zhu J, Winandy J (2008) Energy product options for Eucalyptus species grown as short rotation woody crops. Int J Mol Sci 9:1361–1378PubMedPubMedCentralGoogle Scholar
  98. Rosado CCG, da Silva Guimarães LM, Faria DA, de Resende MDV, Cruz CD, Grattapaglia D, Alfenas AC (2016) QTL mapping for resistance to Ceratocystis wilt in Eucalyptus. Tree Genet Genomes 12:72Google Scholar
  99. Roux J, Mthalane Z, De Beer Z, Eisenberg B, Wingfield M (2006) Quambalaria leaf and shoot blight on Eucalyptus nitens in South Africa. Australas Plant Pathol 35:427–433Google Scholar
  100. Roux J, Greyling I, Coutinho TA, Verleur M, Wingfield MJ (2013) The myrtle rust pathogen, Puccinia psidii, discovered in Africa. IMA Fungus 4:155–159PubMedPubMedCentralGoogle Scholar
  101. Samils B, Rönnberg-Wästljung A-C, Stenlid J (2011) QTL mapping of resistance to leaf rust in Salix. Tree Genet Genomes 7:1219–1235Google Scholar
  102. 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:e0184381PubMedPubMedCentralGoogle Scholar
  103. Santos MR, da Silva Guimarães LM, de Resende MDV, Rosse LN, Zamprogno KC, Alfenas AC (2014) Eucalypts rust (Puccinia psidii) resistance in Eucalyptus pellita. Crop Breed Appl Biotechnol 14:244–250Google Scholar
  104. Schoettle AW, Sniezko RA, Kegley A, Burns KS (2013) White pine blister rust resistance in limber pine: evidence for a major gene. Phytopathology 104:163–173Google Scholar
  105. Shepherd M, Baten A, Junior OBDS, Lee DJ, Butler JB, Freeman J, Vaillancourt R, Potts B, Grattapaglia D, King G (2015) Towards a Corymbia reference genome: comparative efficiencies of Illumina, PacBio and hybrid de novo assemblies of a complex heterozygous genome. In conference: Vettori C, Vendramin GG, Paffetti D, Travaglini D (eds) Proceedings of the IUFRO Tree Biotechnology 2015 Conference: "forests: the importance to the planet and society", Florence, ItalyGoogle Scholar
  106. Shepherd M, Barry KW, Baten A, Butler JB, Freeman JS, Furtado A, Grattapaglia D, Healey A, Henry RJ, King GJ, Lee D, Potts BM, Schmutz J, da Silva Junior OB, Simmons B, Vaillancourt R (2016) Spotting the difference: comparing the genome of Corymbia with its larger cousin Eucalyptus grandis, XXIV edn. In conference: Plant & Animal Genome Conference, San DiegoGoogle Scholar
  107. Simpson JA (2000) Quambalaria, a new genus of eucalypt pathogens. Aust Mycol 19:57–62Google Scholar
  108. Slee A, Brooker M, Duffy S, West J (2006) EUCLID eucalypts of Australia. 3rd edn. Centre for Plant Biodiversity Research - CSIRO Publishing CanberraGoogle Scholar
  109. Smith A, Potts B, Ratkowsky D, Pinkard E, Mohammed C (2017) Association of Eucalyptus globulus leaf anatomy with susceptibility to Teratosphaeria leaf disease. For Pathol 48:e12395Google Scholar
  110. Stone C, Simpson JA, Eldridge RH (1998) Insect and fungal damage to young eucalypt trial plantings in northern New South Wales. Aust For 61:7–20Google Scholar
  111. Thumma BR, Pegg GS, Warburton P, Brawner J, Macdonell P, Yang X, Southerton S (2013) Molecular tagging of rust resistance genes in eucalypts. CSIRO Plant Industry, CanberraGoogle Scholar
  112. Tobias PA, Park RF, Külheim C, Guest DI (2015) Wild-sourced Chamelaucium uncinatum have no resistance to Puccinia psidii (myrtle rust). Aust Plant Dis Notes 10:15Google Scholar
  113. Tobias PA, Guest DI, Külheim C, Hsieh JF, Park RF (2016) A curious case of resistance to a new encounter pathogen: myrtle rust in Australia. Mol Plant Pathol 17:783–788PubMedPubMedCentralGoogle Scholar
  114. Tobias PA, Guest D, Külheim C, Park RF (2017) De novo transcriptome study identifies candidate genes involved in resistance to Austropuccinia psidii (myrtle rust) in Syzygium luehmannnii (Riberry). Phytopathology 108:627–640Google Scholar
  115. Uchida J, Zhong S, Killgore E (2006) First report of a rust disease on ohia caused by Puccinia psidii in Hawaii. Plant Dis 90:524–524PubMedGoogle Scholar
  116. Van Der Biezen EA, Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23:454–456PubMedGoogle Scholar
  117. Van der Colff D, Dreyer LL, Valentine A, Roets F (2017) Differences in physiological responses to infection by Ceratocystis tsitsikammensis, a native ophiostomatoid pathogen, between a native forest and an exotic forestry tree in South Africa. Fungal Ecol 27:107–115Google Scholar
  118. Van der Hoorn RAL, De Wit PJGM, Joosten MHAJ (2002) Balancing selection favors guarding resistance proteins. Trends Plant Sci 7:67–71PubMedGoogle Scholar
  119. Van der Hoorn RAL, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017PubMedPubMedCentralGoogle Scholar
  120. van Ooijen J (2009) MapQTL 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Wageningen, Kyazma BVGoogle Scholar
  121. van Ooijen JW (1999) LOD significance thresholds for QTL analysis in experimental populations of diploid species. Heredity 83:613–624PubMedGoogle Scholar
  122. Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedPubMedCentralGoogle Scholar
  123. Wallace HM, Trueman SJ (1995) Dispersal of Eucalyptus torelliana seeds by the resin-collecting stingless bee, Trigona carbonaria. Oecologia 104:12–16PubMedGoogle Scholar
  124. Wallace HM, Howell MG, Lee DJ (2008) Standard yet unusual mechanisms of long-distance dispersal: seed dispersal of Corymbia torelliana by bees. Divers Distrib 14:87–94Google Scholar
  125. Westaway JO (2016) The pathogen Myrtle rust (‘Puccinia psidii’) in the Northern Territory: first detection, new host and potential impacts. Northern Territory Natur 27:13Google Scholar
  126. Whalen MC, Stall RE, Staskawicz BJ (1988) Characterization of a gene from a tomato pathogen determining hypersensitive resistance in non-host species and genetic analysis of this resistance in bean. Proc Natl Acad Sci 85:6743–6747PubMedGoogle Scholar
  127. Wiesner-Hanks T, Nelson R (2016) Multiple disease resistance in plants. Annu Rev Phytopathol 54:229–252PubMedGoogle Scholar
  128. Wingfield MJ, Crous PW, Swart WJ (1993) Sporothrix eucalypti (sp. nov.), a shoot and leaf pathogen of Eucalyptus in South Africa. Mycopathologia 123:159–164Google Scholar
  129. Xavier AA, Alfenas AC, Matsuoka K, Hodges CS (2001) Infection of resistant and susceptible Eucalyptus grandis genotypes by urediniospores of Puccinia psidii. Australas Plant Pathol 30:277–281Google Scholar
  130. Zauza EAV, Alfenas AC, Old K, Couto MMF, Graça RN, Maffia LA (2010) Myrtaceae species resistance to rust caused by Puccinia psidii. Australas Plant Pathol 39:406–411Google Scholar
  131. Zhai J, Jeong D-H, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553PubMedPubMedCentralGoogle Scholar
  132. Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16PubMedGoogle Scholar
  133. Zhao J-P, Jiang X-L, Zhang B-Y, Su X-H (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7:e44968PubMedPubMedCentralGoogle Scholar
  134. Zhou X, De Beer ZW, Xie Y, Pegg GS, Wingfield MJ (2007) DNA-based identification of Quambalaria pitereka causing severe leaf blight of Corymbia citriodora in China. Fungal Divers 25:245–254Google Scholar
  135. Zhuang J-Y, Wei S-X (2011) Additional materials for the rust flora of Hainan Province, China. Mycosystema 30:853–860Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Natural SciencesUniversity of TasmaniaHobartAustralia
  2. 2.ARC Training Centre for Forest ValueUniversity of TasmaniaHobartAustralia
  3. 3.Forest Industries Research CentreUniversity of the Sunshine CoastMaroochydore DCAustralia
  4. 4.Department of Agriculture and FisheriesEcosciences PrecinctBrisbaneAustralia
  5. 5.ScionRotoruaNew Zealand

Personalised recommendations