Skip to main content

Recent outbreaks of rust diseases and the importance of basic biological research for controlling rusts

Abstract

Rust fungi are obligate plant parasites belonging to the order Pucciniales; they comprise about 7,800 species throughout the world. Some species seriously damage crops, vegetables, fruits and trees. Of these species, wheat stem rust (Puccinia graminis f. sp. tritici), Asian soybean rust (Phakopsora pachyrhizi) and myrtle rust (Puccinia psidii) have recently become major concerns worldwide, and this review, discusses recent rust disease outbreaks of Asian soybean rust and myrtle rust. Both rusts have very wide host ranges. Asian soybean rust has spread from its original region of distribution (eastern Asia) to many areas of soybean cultivation around the world. Myrtle rust is a new disease in areas where host plants were first introduced and has spread to other parts of the world including the areas where the host plants are indigenous. New diseases of economically important plants can occur by host shifts from wild host plants or host jumps from phylogenetically unrelated plant species. Recent advances in molecular phylogenetic studies have contributed to a revision of rust taxonomy. Molecular phylogenetic analyses, together with precise morphological observations and inoculation experiments, have identified taxonomic groups among populations that are morphologically very similar. Systematic, ecological and other basic biological studies of rust fungi in both cultivated and wild host plants are very important for developing methods to control rust diseases. Recent changes in the International Code of Botanical Nomenclature will surely affect the systematics of rust fungi.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Agrios GN (2005) Plant pathology. Elsevier Academic Press, San Diego

    Google Scholar 

  2. Aime MC (2006) Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47:112–122

    CAS  Google Scholar 

  3. Akamatsu H, Yamanaka N, Yamaoka Y, Soares RM, Morel W, Ivancovich AJG, Bogado AN, Kato M, Yorinori JT, Suenaga K (2013) Pathogenic diversity of soybean rust in Argentina, Brazil and Paraguay. J Gen Plant Pathol 79:28–40

    Google Scholar 

  4. Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Lin Soc 161:105–121

    Google Scholar 

  5. Anikster Y, Bushnell WR, Eilam T, Manisterski J, Roelfs AP (1997) Puccinia recondita causing leaf rust on cultivated wheats, wild wheats, and rye. Can J Bot 75:2082–2096

    Google Scholar 

  6. Arthur JC (1905) Terminology of the spore-structures in the Uredinales. Bot Gaz 39:219–222

    Google Scholar 

  7. Arthur JC (1934) Manual of the rusts in United States and Canada. Purdue Research Foundation, Lafayette, Indiana, USA. Reprinted with a supplement by G. B. Cummins (1962) Hafner, New York, 438, p 24

  8. Asian Vegetable Research and Development Center (AVRDC) (1985) Progress report 1983. AVRDC Publication, Shanhua

    Google Scholar 

  9. Berkeley MJ (1874) Notices of North American fungi. Grevillea 3:49–64

    Google Scholar 

  10. Berkeley MJ, Curtis MA (1860) Characters of new fungi, collected in the North Pacific exploring expedition by Charles Wright. Proc Am Acad Arts Sci 4:111–130

    Google Scholar 

  11. Bolton MD, Kolmer JA, Garvin DF (2008) Wheat leaf rust caused by Puccinia triticina. Mol Plant Pathol 9:563–575

    PubMed  Google Scholar 

  12. Bonde MR, Peterson GL, Dowler WM (1988) A comparison of isozymes of Phakopsora pachyrhizi from the Eastern Hemisphere and the New World. Phytopathology 78:1491–1494

    CAS  Google Scholar 

  13. Bonde MR, Nester SE, Moore WF, Allen TW (2009) Comparative susceptibility of kudzu accessions from the southeastern United States to infection by Phakopsora pachyrhizi. Plant Dis 93:593–598

    Google Scholar 

  14. Bromfield KR (1984) Soybean rust, Monograph 11. American Phytopathological Society, St. Paul

    Google Scholar 

  15. Burdon JJ, Marshall DR (1981) Evaluation of Australian native species of Glycine for resistance to soybean rust. Plant Dis 65:44–45

    Google Scholar 

  16. Burdon JJ, Speer SS (1984) A set of differential Glycine hosts for the identification of races of Phakopsora pachyrhizi Syd. Euphytica 33:891–896

    Google Scholar 

  17. 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. Aust Plant Pathol 39:463–466

    Google Scholar 

  18. Chatasiri S, Ono Y (2008) Phylogeny and taxonomy of the Asian grapevine leaf rust fungus, Phakopsora euvitis, and its allies (Uredinales). Mycoscience 49:66–74

    CAS  Google Scholar 

  19. Coelho L, Alfenas AC, Ferreira FA (2001) Physiologic variability of Puccinia psidii: the rust of Eucalyptus (in Portuguese with English summary). Summa Phytopathol 27:95–300

    Google Scholar 

  20. Cook RTA (2001) First report in England of changes in the susceptibility of Puccinia horiana, the cause of chrysanthemum white rust, to triazole and strobilurin fungicides. Plant Pathol 50:792

    Google Scholar 

  21. Coutinho TA, Wingfield MJ, Alfenas AC, Crous PW (1998) Eucalyptus rust: a disease with the potential for serious international implications. Plant Dis 82:819–825

    Google Scholar 

  22. Cummins GB (1971) The rust fungi of cereals, grasses and bamboos. Springer-Verlag, New York

    Google Scholar 

  23. Cummins GB, Hiratsuka Y (2003) Illustrated genera of rust fungi. APS Press, St. Paul

    Google Scholar 

  24. de Castro HA, Krügner TL, Ideriha CHF, Cappello MSC, Marchi AB (1983) Cross inoculation of Eucalyptus, Psidium guajava and Syzygium jambos with Puccinia psidii (in Portuguese with English summary). Fitopatol Bras 8:491–497

    Google Scholar 

  25. FAOSTAT (2013) FAO statistical databases and data-sets. Food and Agriculture Organization of the United Nations, http://faostat3.fao.org/faostat-gateway/go/to/home/E

  26. Ferreira FA (1983) Ferrugem do eucalipto (in Portuguese with English summary). Rev Árvore 7:91–109

    Google Scholar 

  27. Figueiredo MB (2001) Life cycle and ecology of Puccinia psidii (in Portuguese with English summary). O Biologico 63:69–71

    Google Scholar 

  28. Frederick RD, Snyder CL, Peterson GL, Bonde MR (2002) Polymerase chain reaction assays for the detection and discrimination of the soybean rust pathogens Phakopsora pachyrhizi and P. meibomiae. Phytopathology 92:217–227

    CAS  PubMed  Google Scholar 

  29. Garcia A, Calvo ES, Kiihl RAS, Harada A, Hiromoto DM, Vieira LGE (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117:545–553

    CAS  PubMed  Google Scholar 

  30. Gäumann E (1959) Die Rostpilze Motteleuropas. Buchdruckerei Buechler & Co., Bern

    Google Scholar 

  31. Glen M, Alfenas AC, Zauza EAV, Wingfield MJ, Mohammed C (2007) Puccinia psidii: a threat to the Australian environment and economy: a review. Austral Plant Pathol 36:1–16

    Google Scholar 

  32. Goellner K, Loehrer M, Langenbach C, Conrath U, Koch E, Schaffrath U (2010) Phakopsora pachyrhizi, the causal agent of Asian soybean rust. Mol Plant Pathol 11:169–177

    CAS  PubMed  Google Scholar 

  33. Guimarães LMS, Titon M, Lau D, Rosse LN, Oliveira LSS, Rosado CCG, Christo GGO, Alfenas AC (2010) Eucalyptus pellita as a source of resistance to rust, ceratocystis wilt and leaf blight. Crop Breed Appl Biotech 10:124–131

    Google Scholar 

  34. Harada Y (1984) Pear and apple rusts in Japan, with special reference to their life cycles and host ranges. Rept Tottori Mycol Inst 22:108–119

    Google Scholar 

  35. Harada Y (2010) The significance of field observations and inoculation experiments in studying the life cycle of rust fungi: with emphasis on heteroecism and variation in spore form. In: Workshop FPP (ed) Instruction on fungal plant pathogen useful in fields: Taxonomy, identification and handling (in Japanese). Fungal Plant Pathogen Workshop, Tsukuba, pp 193–203

    Google Scholar 

  36. Hartman GL, Miles MR, Frederick RD (2005) Breeding for resistance to soybean rust. Plant Dis 89:664–666

    Google Scholar 

  37. Hartwig EE (1986) Identification of a fourth major gene conferring resistance to soybean rust. Crop Sci 26:1135–1136

    Google Scholar 

  38. Hartwig EE, Bromfield KR (1983) Relationships among three genes conferring specific resistance to rust in soybeans. Crop Sci 23:237–239

    Google Scholar 

  39. Hawksworth DL (2011) A new dawn for the naming of fungi: impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. MycoKeys 1:7–20

    Google Scholar 

  40. Hayashi K, Murotani Y, Yasui K (1989) Begonia L. In: Tsukamoto Y (ed) The grand dictionary of horticulture (in Japanese), vol 4. Shogakukan, Tokyo, pp 321–336

    Google Scholar 

  41. Hennings P (1900) Fungi japonici I. Bot Jahr 28:259–280

    Google Scholar 

  42. Hennings P (1903) Einige neue japanische Uredineen IV. Hedwigia Beibl 42:107–108

    Google Scholar 

  43. Hennings P (1905) Fungi japonici V. Bot Jahrb 34:593–606

    Google Scholar 

  44. Hiratsuka N (1932) Notes on soybean rust (in Japanese). Trans Biol Soc Tottori 1:8–11

    Google Scholar 

  45. Hiratsuka N (1944) Melampsoracearum nipponicarum. (Contributions to the rust-flora of eastern Asia, V) (in Japanese). Mem Tottori Agric Coll 7:91–273

    Google Scholar 

  46. Hiratsuka N (1958) Revision of taxonomy of the Pucciniastreae, with special reference to species of the Japanese Archipelago. Mem Fac Agric, Tokyo Univ Edu 5:1–167

    Google Scholar 

  47. Hiratsuka N (1960) A provisional list of Uredinales of Japan proper and the Ryukyu Islands. Sci Bull Div Agric Home Econ Eng Univ Ryukyus 7:189–314

    Google Scholar 

  48. Hiratsuka Y (1973) The nuclear cycle and the terminology of spore states in Uredinales. Mycologia 65:432–443

    Google Scholar 

  49. Hiratsuka Y (1975) Recent controversies on the terminology of rust fungi. Rept Tottori Mycol Inst 12:99–104

    Google Scholar 

  50. Hiratsuka Y, Powell JM (1976) Pine stem rusts of Canada. Canadian Forestry Service, Forestry Technical Report 4, Northern Forest Research Centre, Edmonton, Alberta

  51. Hiratsuka Y, Sato S (1982) Morphology and taxonomy of rust fungi. In: Scott KJ, Chakravorty AK (eds) The rust fungi. Academic press, London, pp 1–36

    Google Scholar 

  52. Hiratsuka N, Sato S, Katsuya K, Kakishima M, Hiratsuka Y, Kaneko S, Ono Y, Sato T, Harada Y, Hiratsuka T, Nakayama K (1992) The rust flora of Japan. Tsukuba Shuppankai, Tsukuba

    Google Scholar 

  53. Holm L (1973) Some notes on rust terminology (Japan). Rept Tottori Mycol Inst 10:183–187

    Google Scholar 

  54. Ishii H (2006) Impact of fungicide resistance in plant pathogens on crop disease control and agricultural environment. JARQ 40:205–211

    CAS  Google Scholar 

  55. Ito S (1938) Mycological flora of Japan. Vol. 2. Basidiomycetes. 2. Uredinales—Melampsoraceae (in Japanese). Yokendo, Tokyo

  56. Ito S (1950) Mycological flora of Japan. Vol. 2. Basidiomycetes. 3. Uredinales—Pucciniaceae, Uredinales Imperfecti (in Japanese). Yokendo, Tokyo

  57. Ito K (1974) Pathology of forest trees III (in Japanese). Norin Shuppan Co. Ltd, Tokyo

    Google Scholar 

  58. Ivancovich A (2005) Soybean rust in Argentina. Plant Dis 89:667–668

    Google Scholar 

  59. Iwai H, Matsui K (1988) Kalankoe Adans. In: Tsukamoto Y (ed) The grand dictionary of horticulture, vol 1. Shogakukan, Tokyo, pp 536–540

    Google Scholar 

  60. Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch T Jr (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92:923–926

    Google Scholar 

  61. Kakishima M, Yamamoto T, Tagami M (1985) Rust diseases of ornamental plants (I) Rust of begonia caused by Puccinastrum boehmeriae. Ann Phytopath Soc Japan 51:623–626

    Google Scholar 

  62. Kaneko S (2000) Cronartium orientale, sp. nov., segregation of the pine gall rust in eastern Asia from Cronartium quercuum. Mycoscience 41:115–122

    Google Scholar 

  63. Kaneko S, Hiratsuka N (1984) Newly-found rusts of birches and fir. (in Japanese). J Jpn For Soc 66:280–284

    Google Scholar 

  64. Kato M, Yorinori JT (2008) A study on a race composition of Phakopsora pachyrhizi in Brazil: a difficulty of race identification. In: Kudo H, Suenaga K, Soares RM, Toledo A (eds) Facing the challenge of soybean rust in South America, JIRCAS Working Report No. 58. JIRCAS, Tsukuba, pp 94–98

    Google Scholar 

  65. Kato M, Yorinori JT, Paiva WM, Yamaoka Y, Almeida AMR (2007) Epidemiological studies of soybean rust in South America: host susceptibility and pathogenic races. In: Suenaga K, Kudo H, Oshio S (eds) Comprehensive studies on the development of sustainable soybean production technology in South America, JIRCAS Working Report No. 51. JIRCAS, Tsukuba, pp 35–46

    Google Scholar 

  66. Katsumoto K (2010) List of fungi recorded in Japan (in Japanese). Kanto Branch of the Mycological Society of Japan, Chiba

    Google Scholar 

  67. Katsuya K, Kakishima M, Sato S (1978) Axenic culture of two rust fungi, Puccinia coronata f. sp. avenae and P. recondita f. sp. tritici. Ann Phytopath Soc Japan 44:606–611

    Google Scholar 

  68. 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 75:428–431

    Google Scholar 

  69. Killgore E, Heu R, Gardner DE (1994) First report of soybean rust in Hawaii. Plant Dis 78:1216

    Google Scholar 

  70. Kirk PM, Cannon PF, Minter DW, Stalpers JA (2008) Ainsworth and Bisby’s dictionary of the Fungi. CAB International, Wallingford

    Google Scholar 

  71. Kitani K, Inoue Y (1960) Studies on the soybean rust and its control measure. Part 1. Studies on the soybean rust (in Japanese with English summary). Shikoku Agric Exp Stn (Zentsuji, Japan) Bull 5:319–342

    Google Scholar 

  72. Kitani K, Inoue Y, Natsume T (1960) Studies on the soybean rust and its control measure. Part 2. Studies on the control measure on the soybean rust (in Japanese with English summary). Shikoku Agric Exp Stn (Zentsuji, Japan) Bull 5:343–358

    Google Scholar 

  73. Kondo H (1975) Studies on eastern gall rust of pines (Cronartium quercuum (Berk.) Miyabe ex Shirai), with special reference to the life cycle, the infection period to pines, and pathogenic variability to alternate hosts of the causal fungus (in Japanese with English summary). Bull Ibaraki Pref For Exp Stat 8:1–107

    Google Scholar 

  74. Kuhlman EG, Kaneko S (1991) Comparisons of basidiospores and urediniospores of formae speciales of Cronartium quercuum. Mycologia 83:440–445

    Google Scholar 

  75. Kuprevich VF, Tranzshel VG (1957) Rust fungi. 1. Family Melampsoraceae, Moscow-Leningrad (English translation, 1970, Israel Program for Scientific Translations, Jerusalem)

  76. Large EC (1940) The advance of the fungi. Jonathan Cape, London

    Google Scholar 

  77. Laundon GF (1967) Terminology in the rust fungi. Trans Br Mycol Soc 50:189–194

    Google Scholar 

  78. Lemos NG, Braccini AL, Abdelnoor RV, de Oliveira MCN, Suenaga K, Yamanaka N (2011) Characterization of genes Rpp2, Rpp4, and Rpp5 for resistance to soybean rust. Euphytica 182:53–64

    CAS  Google Scholar 

  79. Levy C (2005) Epidemiology and chemical control of soybean rust in Southern Africa. Plant Dis 89:669–674

    CAS  Google Scholar 

  80. Li S, Smith JR, Ray JD, Frederick RD (2012) Identification of a new soybean rust resistance gene in PI 567102B. Theor Appl Genet 125:133–142

    CAS  PubMed  Google Scholar 

  81. Lin SY (1966) Studies on the physiologic races of soybean rust fungus, Phakopsora pachyrhizi Syd. (in Chinese with English summary). J Taiwan Agric Res 15:24–28

    Google Scholar 

  82. Maclean DJ (1982) Axenic culture and metabolism of rust fungi. In: Scott KJ, Chakravorty AK (eds) The rust fungi. Academic Press, London, pp 37–120

    Google Scholar 

  83. Mamani EMC, Bueno NW, Faria DA, Guimarães LMS, 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 Genom 6:953–962

    Google Scholar 

  84. Maphosa M, Talwana H, Tukamuhabwa P (2012) Enhancing soybean rust resistance through Rpp2, Rpp3 and Rpp4 pair wise gene pyramiding. Afr J Agric Res 7:4271–4277

    Google Scholar 

  85. McAlpine D (1906) The rusts of Australia. Brian, Melbourne

    Google Scholar 

  86. McLean RJ, Byth DE (1976) Resistance of soybean to rust in Australia. Austral Plant Pathol Soc Newsl 5:34–36

    Google Scholar 

  87. McNeill J, Barrie FR, Burdet HM, Demoulin V, Hawksworth DL, Marhold K, Nicolson DH, Prado J, Silva PC, Skog JE, Wiersema JH, Turland NJ (2006) International Code of Botanical Nomenclature (Vienna Code) adopted by the 17th International Botanical Congress Vienna, Austria, July 2005. A. R. G. Gantner Verlag KG, Ruggell

  88. Ministry of Agriculture, Forestry and Fisheries (MAFF) (2013) The 87th Statistical yearbook of Ministry of Agriculture, Forestry and Fisheries (2011–2012). http://www.maff.go.jp/e/tokei/kikaku/nenji_e/87nenji/index.html

  89. 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:e35434

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Nakamura H, Kaneko S, Spaine P (1998) Differences in molecular characteristics between Cronartium quercuum from Japan and fusiform rust from USA. In: Jalkanen R, Crane P, Walla JA, Aalto T (eds) Proc First IUFRO, Rusts of Forest Trees Working Party Conf, Finnish Forest Research Institute, Research Papers, Saariselka, pp 235–241

  91. Okada G (2011) Unified nomenclature for anamorphic fungi or fungi with a pleomorphic life cycle adopted at the 18th International Botanical Congress (IBC2011, Melbourne). Jpn J Mycol 52:82–97

    Google Scholar 

  92. Ono Y (2000) Taxonomy of the Phakospora ampelopsidis species complex on vitaceous hosts in Asia including a new species P. euvitis. Mycologia 92:154–173

    Google Scholar 

  93. Ono Y (2008) Why life-cycle studies?: implications in the taxonomy of rust fungi (Uredinales) (in Japanese with English summary). Nippon Kingakukai Kaiho 49:1–28

    Google Scholar 

  94. Ono Y, Buritica P, Hennen JF (1992) Delimitation of Phakopsora, Physopella and Cerotelium and their species on Leguminosae. Mycol Res 96:825–850

    Google Scholar 

  95. Ono Y, Chatasiri S, Pota S, Yamaoka Y (2012) Phakopsora montana, another grapevine leaf rust pathogen in Japan. J Gen Plant Pathol 78:338–347

    CAS  Google Scholar 

  96. Paul C, Hartman GL (2009) Sources of soybean rust resistance challenged with single-spored isolates of Phakopsora pachyrhizi. Crop Sci 49:1781–1785

    Google Scholar 

  97. Powers HRJ, Kaneko S, Kuhlman EG, La Y-J, Yi C-K (1991) Susceptibility of Asian and American oaks and pines to Cronartium quercuum. In: Hiratsuka Y, Samoil JK, Blenis PV, Crane PE, Laishley BL (eds) Rusts of pine. Proceedings of the IUFRO Rusts of Pine Working Party Conference, Information Report NOR-X-317, Forestry Canada, Northern Forestry Centre, Edmonton, Alberta, pp 313–318

  98. Rayachhetry MB, Van TK, Center TD, Elliott ML (2001) Host range of Puccinia psidii, a potential biological control agent of Melaleuca quinquenervia in Florida. Biol Cont 22:38–45

    Google Scholar 

  99. Roelfs AP (1982) Effects of barberry eradication on stem rust in the United States. Plant Dis 66:177–181

    Google Scholar 

  100. Roelfs AP (1985) Wheat and rye stem rust. In: Roelfs AP, Bushnell WR (eds) The cereal rusts, vol II Diseases, distribution, epidemiology, and control. Academic Press, Orlando, pp 3–37

    Google Scholar 

  101. Roux J, Greyling I, Coutinho TA, Verleur M, Wingfield MJ (2013) The myrtle rust pathogen, Puccinia psidii, discovered in Africa. IMA Fungus 4:155–159

    PubMed Central  PubMed  Google Scholar 

  102. Rupe J, Sconyers L (2008) Soybean rust. Plant Health Instr. doi:10.1094/PHI-I-2008-0401-01

    Google Scholar 

  103. Saho H (1968) Studies on the needle rust of the five-needled pines (in Japanese). Bull Tokyo Univ For 64:59–148

    Google Scholar 

  104. Saksirirat W, Hoppe HH (1990) Verticillium psalliotae, an effective mycoparasite of the soybean rust fungus Phakopsora pachyrhizi Syd. J Plant Dis Prot 97:622–633

    Google Scholar 

  105. Sato S (1984) Current topics of research on the rust fungi (in Japanese). Plant Protect 38:288–293

    Google Scholar 

  106. Sato T, Sato S (1982) Infective ability of soybean rust to several leguminous plants. Soybean Rust Newsl 5:22–26

    Google Scholar 

  107. Savile DBO (1984) Taxonomy of the cereal rust fungi. In: Bushnell WR, Roelfs AP (eds) The cereal rusts, vol 1. Academic Press, Orlando, pp 79–112

    Google Scholar 

  108. Scherm H, Christiano RSC, Esker PD, Del Ponte EM, Godoy CV (2009) Quantitative review of fungicide efficacy trials for managing soybean rust in Brazil. Crop Protect 28:774–782

    CAS  Google Scholar 

  109. Schneider RW, Hollier CA, Whitam HK, Palm ME, McKemy JM, Hernández JR, Levy L, DeVries-Paterson R (2005) First report of soybean rust caused by Phakopsora pachyrhizi in the continental United States. Plant Dis 89:774

    Google Scholar 

  110. Seixas CDS, Godoy CV (2007) Vazio sanitário: panorama nacional e medidas de monitoramento Simpósio brasileiro de ferrugem asiática da soja (in Portuguese). Anais do simpósio brasileiro de ferrugem asiática da soja, Embrapa Soja, pp 23–33

    Google Scholar 

  111. Shirai M (1899) On the genetic connection between Peridermium giganteum (Mayr) Tubeuf and Cronartium quercuum (Cooke) Miyabe. Bot Mag (Tokyo) 13:74–79

    Google Scholar 

  112. Silva PHM, Miranda AC, Moraes MLT, Furtado EL, Stape JL, Alvares CA, Sentelhas PC, Mori ES, Sebbenn AM (2013) Selecting for rust (Puccinia psidii) resistance in Eucalyptus grandis in São Paulo State, Brazil. For Ecol Manag 303:91–97

    Google Scholar 

  113. Sinclair JB, Hartman GL (1999) Soybean rust. In: Hartman GL, Sinclair JB, Rupe JC (eds) Compendium of soybean diseases. APS Press, St. Paul, pp 25–26

    Google Scholar 

  114. Sinclair WA, Lyon HH (2005) Diseases of trees and shrubs, 2nd edn. Cornell University Press, Ithaca

    Google Scholar 

  115. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P, Wanyera R, Herrera-Foessel SA, Ward RW (2008) Will stem rust destroy the world’s wheat crop? Adv Agro 98:271–309

    CAS  Google Scholar 

  116. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Bhavani S, Njau P, Herrera-Foessel S, Singh PK, Singh S, Govindan V (2011) The emergence of Ug99 races of the stem rust fungus is a threat to world wheat production. Annu Rev Phytopathol 49:465–481

    CAS  PubMed  Google Scholar 

  117. Tainter FH, Baker FA (eds) (1996) Principles of forest pathology. John Wiley, New York

    Google Scholar 

  118. Tommerup IC, Alfenas AC, Old KM (2003) Guava rust in Brazil: a threat to eucalyptus and other Myrtaceae. New Zealand J For Sci 33:420–428

    Google Scholar 

  119. Tschanz AT (1989) Rust. In: Sinclair JB, Backman PA (eds) Compendium of soybean diseases. APS Press, St. Paul, pp 24–27

    Google Scholar 

  120. Twizeyimana M, Hartman GL (2012) Pathogenic variation of Phakopsora pachyrhizi isolates on soybean in the United States from 2006 to 2009. Plant Dis 96:75–81

    Google Scholar 

  121. Twizeyimana M, Ojiambo PS, Sonder K, Ikotun T, Hartman GL, Bandyopadhyay R (2009) Pathogenic variation of Phakopsora pachyrhizi infecting soybean in Nigeria. Phytopathology 99:353–361

    CAS  PubMed  Google Scholar 

  122. 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

    Google Scholar 

  123. Umemoto S, Murata A, Nagai Y (1989) Dispersal of Japanese pear rust fungus, Gymnosporangium asiaticum Miyabe ex Yamada (in Japanese with English summary). Ann Phytopath Soc Japan 55:250–253

    Google Scholar 

  124. Uppalapati SR, Ishiga Y, Doraiswamy V, Bedair M, Mittal S, Chen J, Nakashima J, Tang Y, Tadege M, Ratet P, Chen R, Schultheiss H, Mysore KS (2012) Loss of abaxial leaf epicuticular wax in Medicago truncatula irg1/palm1 mutants results in reduced spore differentiation of anthracnose and nonhost rust pathogens. Plant Cell 24:353–370

    CAS  PubMed Central  PubMed  Google Scholar 

  125. Ward NA, Robertson CL, Chanda AK, Schneider RW (2012) Effects of Simplicillium lanosoniveum on Phakopsora pachyrhizi, the soybean rust pathogen, and its use as a biological control agent. Phytopathology 102:749–760

    CAS  PubMed  Google Scholar 

  126. Williams PG (1984) Obligate parasitism and axenic culture. In: Bushnell WR, Roelfs AP (eds) The cereal rusts, vol I Origins, specificity, structure, and physiology. Academic Press, Orlando, pp 399–425

    Google Scholar 

  127. Williams PG, Scott KJ, Kuhl JL (1966) Vegetative growth of Puccinia graminis f. sp. tritici in vitro. Phytopathology 56:1418–1419

    Google Scholar 

  128. Wilson M, Henderson DM (1966) British rust fungi. Cambridge University Press, London

    Google Scholar 

  129. Winter G (1884) Repertorium Rabenhorstii fungi europaei et extraeuraopaei (in German). Cent XXXI et XXXII Hedwigia 23:164–175

    Google Scholar 

  130. Xavier AA, von Sanfuentes E, Junghans DT, Alfenas AC (2007) Resistência de Eucalyptus globulus e Eucalyptus nitens à ferrugem (Puccinia psidii) (Resistance of Eucalyptus globulus and E. nitens to rust) (in Portuguese with English summary). R Árvore, Viçosa-MG 31:731–735

    Google Scholar 

  131. Yamanaka N, Yamaoka Y, Kato M, Lemos NG, Passianotto ALL, dos Santos JVM, Benitez ER, Abdelnoor RV, Soares RM, Suenaga K (2010) Development of classification criteria for resistance to soybean rust and differences in virulence among Japanese and Brazilian rust populations. Trop Plant Pathol 35:153–162

    Google Scholar 

  132. Yamanaka N, Lemos NG, Akamatsu H, Yamaoka Y, Silva DCG, Passianotto ALL, Abdelnoor RV, Soares RM, Suenaga K (2011) Soybean breeding materials useful for resistance to soybean rust in Brazil. JARQ 45:385–395

    CAS  Google Scholar 

  133. Yamanaka N, Lemos NG, Uno M, Akamatsu H, Yamaoka Y, Abdelnoor RV, Braccini AL, Suenaga K (2013) Resistance to Asian soybean rust in soybean lines with the pyramided three Rpp genes. Crop Breed Appl Biotech 13:75–82

    Google Scholar 

  134. Yamaoka Y (2002) Axenic culture of rust fungi (in Japanese). Riken Symposium 2002, Yet-to-be cultured microorganisms and culture collections, Riken, pp 14–17

  135. Yamaoka Y, Iida H, Kakishima M (1994) Rust of Kalanchoe caused by Puccinia benkei. Ann Phytopath Soc Japan 60:563–568

    Google Scholar 

  136. Yamaoka Y, Fujii R, Iida H, Kakishima M, Onda T (1997) Pathogenicity of Puccinia benkei causing rust of Kalanchoe against plants belonging to Kalancoideae and Sedoideae, Crassulaceae (in Japanese with English summary). Ann Phytopathol Soc Jpn 63:51–56

    Google Scholar 

  137. Yamaoka Y, Fujiwara Y, Kakishima M, Katsuya K, Yamada K, Hagiwara H (2002) Pathogenic races of Phakopsora pachyrhizi on soybean and wild host plants collected in Japan. J Gen Plant Pathol 68:52–56

    Google Scholar 

  138. Yamaoka Y, Yamanaka N, Akamatsu H, Suenaga K (2014) Pathogenic races of soybean rust Phakopsora pachyrhizi collected in Tsukuba and vicinity in Ibaraki, Japan. J Gen Plant Pathol 80:184–188

  139. Yeh CC (1983) Physiological races of Phakopsora pachyrhizi in Taiwan. J Agric Res China 32:69–74

    Google Scholar 

  140. Yorinori JT (2008) Soybean germplasms with resistance and tolerance to Asian rust and screening methods. In: Kudo H, Suenaga K, Soares RM, Toledo A (eds) Facing the challenge of soybean rust in South America, JIRCAS Working Report No. 58. JIRCAS, Tsukuba, pp 70–87

    Google Scholar 

  141. Yorinori JT, Paiva WM, Frederick RD, Costamilan LM, Bertagnolli PF, Hartman GE, Godoy CV, Nunes J Jr (2005) Epidemics of soybean rust (Phakopsora pachyrhizi) in Brazil and Paraguay from 2001 to 2003. Plant Dis 89:675–677

    Google Scholar 

  142. Zambino PJ, Szabo LJ (1993) Phylogenetic relationships of selected cereal and grass rusts based on rDNA sequence analysis. Mycologia 85:401–414

    CAS  Google Scholar 

  143. Zauza EAV, Alfenas AC, Old KM, Couto MMF, Graça RN, Maffia LA (2010) Myrtaceae species resistance to rust caused by Puccinia psidii. Austral Plant Path 39:406–411

    Google Scholar 

  144. Zhuang J-Y, Wei S-X (2011) Additional materials for the rust flora of Hainan Province, China. Mycosystema 30:853–860

    Google Scholar 

  145. Zinno Y, Hayashi H (1977) Rust cankers on seedlings of Sophora japonica in Ibaraki Prefecture (in Japanese). For Pest 26:171–174

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Yuichi Yamaoka.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yamaoka, Y. Recent outbreaks of rust diseases and the importance of basic biological research for controlling rusts. J Gen Plant Pathol 80, 375–388 (2014). https://doi.org/10.1007/s10327-014-0529-z

Download citation

Keywords

  • Myrtle rust
  • Phakopsora
  • Puccinia
  • Pucciniales
  • Soybean rust
  • Systematics