Mycological Progress

, Volume 17, Issue 11, pp 1251–1267 | Cite as

New insight into the species diversity and life cycles of rust fungi (Pucciniales) affecting bioenergy switchgrass (Panicum virgatum) in the Eastern and Central United States

  • Shawn C. Kenaley
  • Menchus Quan
  • M. Catherine Aime
  • Gary C. BergstromEmail author
Original Article


Research was undertaken to clarify the taxonomic identity of leaf rust (Pucciniales) fungi on bioenergy switchgrass in the Eastern and Central U.S. We integrated internal transcribed spacer 2 (ITS2) and partial 28S ribosomal RNA gene sequence data from collections taken from cultivated switchgrass and herbarium specimens, including purported aecial and telial states of Puccinia graminicola and Puccinia pammelii. Maximum likelihood and Bayesian analyses revealed four monophyletic clades: Puccinia emaculata sensu stricto (s.s.), P. pammelii, P. graminicola, and Puccinia novopanici. Results also indicated that P. emaculata s.s. was not affecting cultivated, bioenergy switchgrass. Aecidium pammelii and P. pammelii were distinct phylogenetically from P. emaculata s.s. and grouped within a well-supported clade, demonstrating aecial-telial host alternation for P. pammelii between Euphorbia corollata and switchgrass. Aecidium stillingiae on queen’s delight (Stillingia sylvatica)—a purported aecial state host for P. graminicola—shared identical sequences with the recently described species Puccinia pascua. The latter fungus, however, was recovered within a subclade of P. graminicola. Hence, queen’s delight likely is not an aecial host to P. graminicola s.s. Additional molecular studies are warranted to determine species boundaries within the P. graminicola complex. The majority of contemporary collections from cultivated switchgrass were recognized as P. novopanici. Collectively, bioenergy switchgrass is host to at least three phylogenetically distinct species, presenting a significant challenge to the future selection and breeding of switchgrass with improved rust resistance.


Aecidium stillingiae Perennial grass Phylogeny Puccinia novopanici Puccinia pammelii 


Funding information

This study was funded in part by the Cornell University Hatch Project NYC 153743 from the United States Department of Agriculture-National Institute for Food and Agriculture (USDA-NIFA). The findings, conclusions, and/or recommendations expressed in this publication are those of the authors and do not necessarily reflect the view of the USDA-NIFA.


  1. Aime MC (2006) Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47:112–122. CrossRefGoogle Scholar
  2. Aime MC, Bell C, Wilson AW (2018) Deconstructing the evolutionary complexity of rust fungi (Pucciniales) and their hosts. Stud Mycol 89:143–152. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr AC-19:716–723. CrossRefGoogle Scholar
  4. Alaei H, De Backer M, Nuytinck J, Maes M, Höfte M, Heungens K (2009) Phylogenetic relationships of Puccinia horiana and other rust pathogens of Chrysanthemum × morifolium based on rDNA ITS sequence analysis. Mycol Res 113:668–683. CrossRefPubMedGoogle Scholar
  5. Anonymous (1970) Index of plant diseases in the United States. United States Department of Agriculture, Agricultural handbook no. 165. U.S. Government Printing Office, Washington, D.C. 531Google Scholar
  6. Arias Aguirre A, Studer B, Frei U, Lübberstedt T (2012) Prospects for hybrid breeding in bioenergy grasses. Bioenergy Res 5:10–19. CrossRefGoogle Scholar
  7. Arthur JC (1902) Cultures of Uredineae in 1900 and 1901. J Mycol 8:51–56. CrossRefGoogle Scholar
  8. Arthur JC (1903) Cultures of Uredineae in 1902. Bot Gaz 35:10–23. CrossRefGoogle Scholar
  9. Arthur JC (1905) Cultures of Uredineae in 1904. J Mycol 11:50–67. CrossRefGoogle Scholar
  10. Arthur JC (1906) Cultures of Uredineae in 1905. J Mycol 12:11–27. CrossRefGoogle Scholar
  11. Arthur JC (1907) Cultures of Uredineae in 1906. J Mycol 13:189–205. CrossRefGoogle Scholar
  12. Arthur JC (1908) Cultures of Uredineae in 1907. J Mycol 14:7–26. CrossRefGoogle Scholar
  13. Arthur JC (1909) Cultures of Uredineae in 1908. Mycologia 1:225–256. CrossRefGoogle Scholar
  14. Arthur JC (1910) Cultures of Uredineae in 1909. Mycologia 2:213–240. CrossRefGoogle Scholar
  15. Arthur JC (1915) Cultures of Uredineae in 1912, 1913 and 1914. Mycologia 7:61–89. CrossRefGoogle Scholar
  16. Arthur JC (1917) Cultures of Uredineae in 1916 and 1917. Mycologia 9:294–312. CrossRefGoogle Scholar
  17. Arthur JC (1934) Manual of the rusts in United States and Canada. Purdue Research Foundation, Lafayette, IN. The Science Press Printing Co., Lancaster, PA. 438Google Scholar
  18. Barnes CW, Szabo LJ (2007) Detection and identification of four common rust pathogens of cereals and grasses using real-time polymerase chain reaction. Phytopathology 97:717–727. CrossRefPubMedGoogle Scholar
  19. Bennett C, Aime MC, Newcombe G (2011) Molecular and pathogenic variation within Melampsora on Salix in western North America reveals numerous cryptic species. Mycologia 103:1004–1018. CrossRefPubMedGoogle Scholar
  20. Burrill TJ (1884) New species of Uredineae (collection made by a. B. Seymour). Bot Gaz 9:187–191. CrossRefGoogle Scholar
  21. Casler MD, Vogel KP (2014) Selection for biomass yield in upland, lowland, and hybrid switchgrass. Crop Sci 54:626–636. CrossRefGoogle Scholar
  22. Casler MD, Stendal CA, Kapich L, Vogel KP (2007) Genetic diversity, plant adaptation regions, and gene pools for switchgrass. Crop Sci 47:2261–2273. CrossRefGoogle Scholar
  23. Casler MD, Tobias CM, Kaeppler SM, Buell CR, Wang Z-Y, Cao P, Schmutz J, Ronald P (2011) The switchgrass genome: tools and strategies. Plant Genome 4:273–282. CrossRefGoogle Scholar
  24. Casler MD, Vogel KP, Harrison M (2015) Switchgrass germplasm resources. Crop Sci 55:2463–2478. CrossRefGoogle Scholar
  25. Cornelius DR, Johnston CO (1941) Differences in plant type and reaction to rust among several collections of Panicum virgatum L. J Am Soc Agron 33:115–124. CrossRefGoogle Scholar
  26. Cortese LM, Bonos SA (2013) Bioenergy traits of ten switchgrass populations grown in the northeastern/mid-Atlantic USA. Bioenergy Res 6:580–590. CrossRefGoogle Scholar
  27. Crouch JA, Beirn LA, Cortese LM, Bonos SA, Clarke BB (2009) Anthracnose disease of switchgrass caused by the novel fungal species Colletotrichum navitas. Mycol Res 113:1411–1421. CrossRefPubMedGoogle Scholar
  28. Cummins GB (1971) The rust fungi of cereals, grasses and bamboos, 2nd edn. Springer, New York, p 570CrossRefGoogle Scholar
  29. Cummins GB, Hiratsuka Y (2003) Illustrated genera of rust fungi, 3rd edn. The American Phytopathological Society, APS Press, St. Paul, Minnesota, U.S.A. 225Google Scholar
  30. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Das MK, Fuentes RG, Taliaferro CM (2004) Genetic variability and trait relationships in switchgrass. Crop Sci 44:443–448. CrossRefGoogle Scholar
  32. Davis SC, Anderson-Teixeira KJ, DeLucia EH (2009) Life-cycle analysis and the ecology of biofuels. Trends Plant Sci 14:140–146. CrossRefPubMedGoogle Scholar
  33. Demers JE, Liu M, Hambleton S, Castlebury LA (2017) Rust fungi of Panicum. Mycologia 109:1–17. CrossRefPubMedGoogle Scholar
  34. van der Merwe M, Ericson L, Walker J, Thrall PH, Burdon JJ (2007) Evolutionary relationships among species of Puccinia and Uromyces (Pucciniaceae, Uredinales) inferred from partial protein coding gene phylogenies. Mycol Res 111:163–175. CrossRefPubMedGoogle Scholar
  35. van der Merwe MM, Walker J, Ericson L, Burdon JJ (2008) Coevolution with higher taxonomic host groups within the Puccinia/Uromyces rust lineage obscured by host jumps. Mycol Res 112:1387–1408. CrossRefPubMedGoogle Scholar
  36. Dietel P (1895) New North American Uredineae. Erythea 3:57–82Google Scholar
  37. Dietel P (1928) Unterklasse Hemibasidii (Ustilaginales and Uredinales). Reihe Uredinales. In: Engler A (ed) Die natürlichen Pflanzenfamilien, vol 6, pp 24–98Google Scholar
  38. Farr DF, Rossman AY (2018) Fungal databases, systematic mycology and microbiology laboratory, ARS, USDA. Accessed 06 April 2018
  39. Frazier T, Shen Z, Zhao B, Bush E (2013) First report of Puccinia emaculata infection on switchgrass in Virginia. Plant Dis 97:424. CrossRefGoogle Scholar
  40. Gardes M, Brun TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to identification of mycorrhizae and rusts. Mol Ecol 2:113–118. CrossRefPubMedGoogle Scholar
  41. Gilley M, Tomaso-Peterson M, Orquera GK, Marek SM (2013) First report of rust caused by Puccinia emaculata on switchgrass in Mississippi. J Miss Acad Sci 58:197–200Google Scholar
  42. Gravert C, Munkvold G (2002) Fungi and diseases associated with cultivated switchgrass in Iowa. J Iowa Acad Sci 109:30–34Google Scholar
  43. Gravert CE, Tiffany LH, Munkvold GP (2000) Outbreak of smut caused by Tilletia maclaganii on cultivated switchgrass in Iowa. Plant Dis 84:596. CrossRefGoogle Scholar
  44. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Gustafson DM, Boe A, Jin Y (2003) Genetic variation for Puccinia emaculata infection in switchgrass. Crop Sci 43:755–759. CrossRefGoogle Scholar
  46. Helaers R, Milinkovitch MC (2010) MetaPIGA v2.0: maximum likelihood large phylogeny estimation using the metapopulation genetic algorithm and other stochastic heuristics. BMC Bioinformatics 11:379. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Hirsch RL, TeBeest DO, Bluhm BH, West CP (2010) First report of rust caused by Puccinia emaculata on switchgrass in Arkansas. Plant Dis 94:381. CrossRefGoogle Scholar
  48. Jackson HS (1917) The Uredinales of Delaware. Proc Indiana Acad Sci 27:311–385Google Scholar
  49. Kenaley SC, Smart LB, Hudler GW (2014) Genetic evidence for three discrete taxa of Melampsora (Pucciniales) affecting willows (Salix spp.) in New York State. Fungal Biol 118:704–720. CrossRefPubMedGoogle Scholar
  50. Kenaley SC, Hudler GW, Bergstrom GC (2016) Detection and phylogenetic relationships of Puccinia emaculata and Uromyces graminicola (Pucciniales) on switchgrass in New York State using rDNA sequence information. Fungal Biol 120:791–806. CrossRefPubMedGoogle Scholar
  51. Kiniry JR, Johnson M-VV, Bruckerhoff SB, Kaiser JU, Cordsiemon RL, Harmel RD (2012) Clash of the titans: comparing productivity via radiation use efficiency for two grass giants of the biofuel field. Bioenergy Res 5:41–48. CrossRefGoogle Scholar
  52. Kropp BR, Albee S, Flint KM, Zambino P, Szabo L, Thomson SV (1995) Early detection of systemic rust infections of dyers woad (Isatis tinctoria) using the polymerase chain reaction. Weed Sci 43:467–472. CrossRefGoogle Scholar
  53. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliams H, Gibson TJ, Higgins DG (2007) Clustal V and Clustal X version 2.0. Bioinformatics 23:2947–2948. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lenne JM (1990) World list of fungal diseases of tropical pasture species. Phytopathological Papers No. 31. CAB International, Oxon, UK. 162Google Scholar
  55. Lipka AE, Lu F, Cherney JH, Buckler ES, Casler MD, Costich DE (2014) Accelerating the switchgrass (Panicum virgatum L.) breeding cycle using genomic selection approaches. PLoS One 9:e112227. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Liu M, Hambleton S (2010) Taxonomic study of stripe rust, Puccinia striiformis sensu lato, based on molecular and morphological evidence. Fungal Biol 114:881–899. CrossRefPubMedGoogle Scholar
  57. Liu M, Hambleton S (2013) Laying the foundation for a taxonomic review of Puccinia coronata s.l. in a phylogenetic context. Mycol Prog 12:63–89. CrossRefGoogle Scholar
  58. Lowry DB, Behrman KD, Grabowski P, Morris GP, Kiniry JR, Juenger TE (2014) Adaptations between ecotypes and along environmental gradients in Panicum virgatum. Am Nat 183:682–692. CrossRefPubMedGoogle Scholar
  59. Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis. Version 3.04. Accessed 06 April 2018
  60. Maier W, Begerow D, Weiß M, Oberwinkler F (2003) Phylogeny of the rust fungi: an approach using large subunit ribosomal DNA sequences. Can J Bot 81:12–23. CrossRefGoogle Scholar
  61. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379. CrossRefPubMedGoogle Scholar
  62. McLaughlin SB, Adams Kszos L (2005) Development of switchgrass (Panicum virgatum) as a bioenergy feedstock in the United States. Biomass Bioenergy 28:515–535. CrossRefGoogle Scholar
  63. Minnis AM, McTaggart A, Rossman A, Aime MC (2012) Taxonomy of mayapple rust: the genus Allodus resurrected. Mycologia 104:942–950. CrossRefPubMedGoogle Scholar
  64. Orquera-Tornakian GK, Garrido P, Kronmiller B, Hunger R, Tyler BM, Garzon CD, Marek SM (2017) Identification and characterization of simple sequence repeats (SSRs) for population studies of Puccinia novopanici. J Microbiol Methods 139:113–122. CrossRefPubMedGoogle Scholar
  65. Parish ES, Hilliard MR, Baskaran LM, Dale VH, Griffiths NA, Mulholland PJ, Sorokine A, Thomas, Downing ME, Middleton RS (2012) Multimetric spatial optimization of switchgrass plantings across a watershed. Biofuel Bioprod Bior 6:58–72CrossRefGoogle Scholar
  66. Ramachar P, Cummins G (1963) The species of Uromyces on the tribe Paniceae. Mycopathol Mycol Appl 19:49–61. CrossRefPubMedGoogle Scholar
  67. Ramachar P, Cummins G (1965) The species of Puccinia on the tribe Paniceae. Mycopathol Mycol Appl 25:7–60. CrossRefGoogle Scholar
  68. Rambaut A, Drummond J (2009) Tracer v1.5. (Distributed by the first author, Department of Biology, University of York, UK) Accessed 8 April 2018
  69. Ronquist F, Teslenko M, van der Mark MP, Ayres DL, Darling A, Höhna S, Larget B, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Roy BA, Vogler DR, Bruns TD, Szaro TM (1998) Cryptic species in the Puccinia monoica complex. Mycologia 90:846–853. CrossRefGoogle Scholar
  71. Sanford GR, Oates LG, Jasrotia P, Thelen KD, Robertson GP, Jackson RD (2016) Comparative productivity of alternative cellulosic bioenergy cropping systems in the North Central USA. Agric Ecosyst Environ 216:344–355. CrossRefGoogle Scholar
  72. Schmer MR, Vogel KP, Mitchell RB, Perrin RK (2008) Net energy of cellulosic ethanol from switchgrass. Proc Natl Acad Sci U S A 105:464–469. CrossRefPubMedPubMedCentralGoogle Scholar
  73. Serba DD, Uppalapati SR, Mukherjee S, Krom N, Tang Y, Mysore KS, Saha MC (2015) Transcriptome profiling of rust resistance in switchgrass using RNA-seq analysis. Plant Genome 8. CrossRefGoogle Scholar
  74. Stewart A, Cromey M (2011) Identifying disease threats and management practices for bio-energy crops. Curr Opin Environ Sustain 3:75–80. CrossRefGoogle Scholar
  75. Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Annu Rev Phytopathol 43:83–116. CrossRefPubMedGoogle Scholar
  76. Stuart W (1901) Some additions to the flora of Indiana. Proc Indiana Acad Sci 11:282–284Google Scholar
  77. Swofford DL 2003 Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer 758 Associates, Sunderland, Massachusetts, U.S.A.Google Scholar
  78. Sykes VR, Allen FL, Mielenz JR, Stewart CN, Windham MT, Hamilton CY, Rodriguez M, Yee KL (2016) Reduction of ethanol yield from switchgrass infected with rust caused by Puccinia emaculata. Bioenergy Res 9:239–247. CrossRefGoogle Scholar
  79. Szabo LJ (2006) Deciphering species complexes: Puccinia andropogonis and Puccinia coronata, examples of differing modes of speciation. Mycoscience 47:130–136. CrossRefGoogle Scholar
  80. Tiffany LH, Shearer JF, Knaphus G (1990) Plant parasitic fungi of four tallgrass prairies of northern Iowa: distribution and prevalence. J Iowa Acad Sci 97:157–166Google Scholar
  81. Tracy SM, Earle FS (1899) New fungi from Mississippi. Bull Torrey Bot Club 26:493–495. CrossRefGoogle Scholar
  82. Uppalapati SR, Serba DD, Ishiga Y, Szabo LJ, Mittal S, Bhandari HS, Bouton JH, Mysore KS, Saha MC (2013) Characterization of the rust fungus, Puccinia emaculata, and evaluation of genetic variability for rust resistance in switchgrass populations. Bioenergy Res 6:458–468. CrossRefGoogle Scholar
  83. USDA-NRCS (2018) The PLANTS Database. National Plant Data Team, Greensboro, NC Accessed on 06 April 2018Google Scholar
  84. Vialle AN, Feau N, Frey P, Bernier L, Hamelin RC (2013) Phylogenetic species recognition reveals host-specific lineages among poplar rust fungi. Mol Phylogenet Evol 66:628–644. CrossRefPubMedGoogle Scholar
  85. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246CrossRefGoogle Scholar
  86. Wingfield BD, Ericson L, Szaro T, Burdon JJ (2004) Phylogenetic patterns in the Uredinales. Australas Plant Pathol 33:327–335. CrossRefGoogle Scholar
  87. Yun HY, Minnis AM, Kim YH, Castlebury L, Aime MC (2011) The rust genus Frommeëlla revisited: a later synonym of Phragmidium after all. Mycologia 103:1451–1463. CrossRefPubMedGoogle Scholar
  88. Zale J, Freshour L, Agarwal S, Sorochan J, Ownley BH, Gwinn KD, Castlebury LA (2008) First report of rust on switchgrass (Panicum virgatum) caused by Puccinia emaculata in Tennessee. Plant Dis 92:1710. CrossRefGoogle Scholar
  89. Zambino PJ, Szabo LJ (1993) Phylogenetic relationships of selected cereal and grass rusts based on rDNA sequence analysis. Mycologia 85:401–414. CrossRefGoogle Scholar
  90. Zhu Q, Bennetzen JL, Smith SM (2013) Isolation and diversity analysis of resistance gene homologues from switchgrass. G3-Genes Genom Genet 3:1031–1042. CrossRefGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Integrative Plant Science, Plant Pathology and Plant-Microbe Biology SectionCornell UniversityIthacaUSA
  2. 2.Department of Botany and Plant PathologyPurdue UniversityWest LafayetteUSA

Personalised recommendations