Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2022-02-04
Page range: 1-48
Abstract views: 51
PDF downloaded: 3

Phylogenetic approach for identification and life cycles of Puccinia (Pucciniaceae) species on Poaceae from northeastern China

Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun, Jilin 130118, China. Tangshan Key Laboratory of Agricultural Pathogenic Fungi and Toxins, Department of Life Science, Tangshan Normal University, Tangshan 063000, PR China
Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Tai’an 271000, China.
Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun, Jilin 130118, China
Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun, Jilin 130118, China; University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
Rust fungus Species differentiation Taxonomy Fungi

Abstract

About 300 species of Puccinia on Poaceae have been reported globally. However, these species can be difficult to identify because of morphological similarities and difficulties of host plant identifications. The presence of many cryptic species is also suspected. Based on about 150 specimens on Poaceae and about 50 related specimens of spermogonial and aecial stages, all collected in northeastern China, a phylogenetic approach was conducted to clarify their identification and life cycles. In phylogenetic analyses 25 clades among specimens on Poaceae were detected. Each clade detected in phylogeny was interpreted as an independent species, although many clades were morphologically similar to each other. After comparative morphology with species previously reported, 17 species including three first records in China (P. cerienthes-agropyrina, P. coronati-agrostidis, P. coronati-hordei) were identified, and eight species (P. ampliaticoronata, P. digitaticoronata, P. eleganticoronata, P. elymi-albispora, P. oncospora, P. pileiformis, P. protuberanticoronata, P. ramificatacoronata) are described as new. In uredinial and telial stages, the host range of above 25 species was variable ranging from one host plant species to several host species, sometimes involving different grass genera. Thus, a phylogenetic approach is more suitable for species identifications of Puccinia on Poaceae rather than relying on rust morphology and host plant identification. Life cycle relations for 15 spermogonial and aecial species were also clarified by phylogenetic analyses. It is also suspected that grass rusts can be differentiated to species based on spermogonial and aecial stages on same or related host plants.

References

<p>Abbasi, M., Stephen, B., Goodwin, B. &amp; Scholler, M. (2005) Taxonomy, phylogeny, and distribution of <em>Puccinia graminis</em>, the black stem rust: new insights based on rDNA sequence data.<em> Mycoscience</em> 46: 241–247.&nbsp; https://doi.org/10.1007/s10267-005-0244-x</p>
<p>Aime, M.C. (2006) Toward resolving family-level relationships in rust fungi (<em>Uredinales</em>). <em>Mycoscience</em> 47: 112–122.&nbsp; https://doi.org/10.1007/s10267-006-0281-0</p>
<p>Aime, M.C., Bell, C.D. &amp; Wilson, A.W. (2018) Deconstructing the evolutionary complexity between rust fungi (<em>Pucciniales</em>) and their plant hosts. <em>Studies in Mycology</em> 89: 143–152.&nbsp; https://doi.org/10.1016/j.simyco.2018.02.002</p>
<p>Aime, M.C. &amp; McTaggart, A.R. (2021) A higher-lank classification for rust fungi, with notes on genera.<em> Fungal Systematics and Evolution</em> 7: 21–47.&nbsp; https://doi.org/10.3114/fuse.2021.07.02</p>
<p>Aime, M.C., McTaggart, A.R., Mondo, S.J. &amp; Duplessis, S. (2017) Phylogenetics and phylogenomics of rust fungi. <em>Advances in Genetics</em> 100: 267–307.&nbsp; https://doi.org/10.1016/bs.adgen.2017.09.011</p>
<p>Arthur, J.C. (1934) <em>Manual of the rusts in United States and Canada</em>. Purdue Research Foundation, USA.</p>
<p>Azbukina, Z.M. (2005) <em>Rust fungi, Cryptogamic plants, fungi and mosses of the Russian Far East, vol</em>. <em>5</em>. Dalnauka, Vladivostok, Russia.</p>
<p>Azbukina, Z.M. (2015) <em>Definitorium fungorum Rossiae, Ordo Pucciniales 1</em>. Dal’nauka, Vladivostok, Russia.</p>
<p>Berlin, A., Wallenhammar, A.C. &amp; Andersson, B. (2018) Population differentiation of <em>Puccinia coronata</em> between hosts –implications for the epidemiology of oat crown rust. <em>European Journal of Plant Pathology</em> 152: 901–907.&nbsp; https://doi.org/10.1007/s10658-018-01605-x</p>
<p>Bolton, M.D., Kolmer, J.A. &amp; Garvin, D.F. (2008) Wheat leaf rust caused by <em>Puccinia triticina</em>. <em>Molecular Plant Pathology</em> 9: 563–575.&nbsp; https://doi.org/10.1111/j.1364-3703.2008.00487.x</p>
<p>Bushnell, W.R. &amp; Roelfs, A.P. (Eds.) (1984) <em>The cereal rusts vol 1</em>. Academic Press, Orland, USA.</p>
<p>Chen, W., Wellings, C., Chen, X., Kang, Z. &amp; Liu, T. (2014) Wheat stripe (yellow) rust caused by <em>Puccinia striiformis</em> f. sp.<em> tritici</em>. <em>Molecular Plant Pathology</em> 15: 433–446.&nbsp; https://doi.org/10.1111/mpp.12116</p>
<p>Cunningham, G.H. (1931) <em>The rust fungi of New Zealand</em>. John McIndoe Printer, Dumedin, New Zealand.</p>
<p>Cummins, G.B. (1951) Uredinales of continental China collected by S. Y. Cheo II. <em>Mycologia</em> 43: 78–98.</p>
<p>Cummins, G.B. (1971) <em>The rust fungi of cereals, grasses and bamboos</em>. Springer-Verlag, New York, USA.</p>
<p>Cummins, G.B. &amp; Hiratsuka, Y. (2003) <em>Illustrated genera of rust fungi, 3<sup>rd</sup> ed</em>. American Phytopathological Society, St. Paul, Minnesota, USA.</p>
<p>Demers, J.E., Liu, M., Hambleton, S. &amp; Castlebury, L.A.&nbsp;(2017)&nbsp;Rust fungi on&nbsp;<em>Panicum</em>.&nbsp;<em>Mycologia</em>&nbsp;109: 1–17.&nbsp; https://doi.org/10.1080/00275514.2016.1262656</p>
<p>Dixon, L.J., Castlebury, L.A., Aime, M.C., Glynn, N.C. &amp; Comstock, J.C. (2010) Phylogenetic relationships of sugarcane rust fungi. <em>Mycological Progress</em> 9: 459–468.&nbsp; https://doi.org/10.1007/s11557-009-0649-6</p>
<p>Edler, D., Klein, J., Antonelli, A. &amp; Silvestro, D. (2021) raxmlGUI 2.0: a graphical interface and toolkit for phylogenetic analyses using RAxML. <em>Methods in Ecology and Evolution</em> 12: 373–377.&nbsp; https://doi.org/10.1101/800912</p>
<p>Gardes, M. &amp; Bruns, T.D. (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. <em>Molecular Ecology</em> 2: 113–118.&nbsp; https://dx.doi.org/10.1111/j.1365-294X.1993.tb00005.x</p>
<p>Gäumann, E. (1959) <em>Die Rostpilze</em> <em>Mitteleuropas</em>. Buchdruckerei Bucheler Co, Bern, Germany.</p>
<p>Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. <em>Nucleic Acids Symposium</em> Series 41: 95–98.</p>
<p>Harada, Y. (1984) Materials for the rust flora of Japan IV. <em>Transactions of Mycological Society of Japan</em> 25: 287–294.</p>
<p>Harada, Y. &amp; Hasegawa, H. (1975) Aecial states of two <em>Phragmites</em> rust fungi, <em>Puccinia</em> <em>moriokaensis </em>S. Ito and <em>P</em>. <em>okatamaensis</em> S. Ito. <em>Transactions of Mycological Society of Japan</em> 16: 42–50.</p>
<p>Hiratsuka, N. (1960) A provisional list of <em>Uredinales</em> of Japan proper and the Ryukyu Islands. <em>The</em> <em>Science</em> <em>Bulletin</em> <em>of</em> <em>the</em> <em>Division</em> <em>of</em> <em>Agriculture,</em> <em>Home</em> <em>Economics</em> <em>and Engineering,</em> <em>University</em> <em>of</em> <em>Ryukyus</em> 7: 189–314.</p>
<p>Hiratsuka, N. &amp; Chen, Z.C. (1991) A list of Uredinales collected from Taiwan. <em>Transactions of Mycological Society of Japan</em> 32: 3–22.</p>
<p>Hiratsuka, N. &amp; Kaneko, S. (1983) A provisional list of <em>Puccinia</em> species on the grasses in Japan. <em>Report of Tottori Mycological Institute </em>(<em>Japan</em>) 21: 61–75.</p>
<p>Hiratsuka, N., Sato, S., Katsuya, K., Kakishima, M., Hiratsuka, Y., Kaneko, S., Ono, Y., Sato, T., Harada, Y., Hiratsuka, T. &amp; Nakayama, K. (1992) <em>The rust flora of Japan</em>. Tsukuba-shuppankai, Tsukuba, Japan.</p>
<p>Hiratsuka, T. (1958) The species of rust fungi parasitic on the grasses collected in the southern Kyusyu and the Ryukyu Islands, Japan. <em>Scientific Bulletin of the Agriculture, Home Economics and Engeineering Division, University of the Ryukyus</em> 5: 23–106.</p>
<p>Hiratsuka, Y. &amp; Sato, S. (1982) Morphology and taxonomy of rust fungi. <em>In</em>: Scott, K.J. &amp; Chakravorty, A.K. (Eds.) <em>The rust fungi</em>. Academic Press, London, UK, pp. 1–36.</p>
<p>Hrabětová, M., Kolařík, M. &amp; Marková, J. (2015) Phylogeny and taxonomy of grass rusts with aecia on <em>Ranunculus</em> and <em>Ficaria</em>. <em>Mycological Progress</em> 14: 12.&nbsp; https://doi.org/10.1007/s11557-015-1033-3</p>
<p>Huelsenbeck, J.P. &amp; Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. <em>Bioinformatics</em> 17: 754–755.</p>
<p>Hylander, N., Jørstad, I. &amp; Nannfeldt, J.A. (1953) Enumeratio Uredinearum Scandinavicarum. <em>Opera Botany</em> 1: 1–102.</p>
<p>Ito, S. (1909) On the Uredinales parasitic on the Japanese <em>Gramineae</em>. <em>Journal of College of Agriculture, Tohoku Imperial University </em>(<em>Sapporo</em>) 3: 180–265.</p>
<p>Ito, S. (1950) <em>Mycological flora of Japan, vol</em>. <em>2, no</em>. <em>3</em>. Yokendo, Tokyo, Japan.</p>
<p>Ji, J.X., Li, Z., Wan, Q., Li, Y. &amp; Kakishima, M. (2017) Life cycle of <em>Aecidium klugkistianum</em> on <em>Ligstrum</em> and its new combination, <em>Puccinia klugkistiana</em>. <em>Mycoscience</em> 58: 307–311.&nbsp; https://doi.org/10.1016/j.myc.2017.01.004</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2019a) Two new species of<em> Pucciniastrum </em>producing dimorphic sori and spores from northeast of China. <em>Mycological Progress</em> 18: 529–540.&nbsp; https://doi.org/10.1007/s11557-018-1460-z</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2019b) Life cycle of <em>Nothoravenelia japonic</em>a and its phylogenetic position in <em>Pucciniales</em>, with special reference to the genus <em>Phakopsora</em>. <em>Mycological Progress</em> 18: 855–864.&nbsp; https://doi.org/10.1007/s11557-019-01496-0</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2019c) Notes on rust fungi in China 7. <em>Aecidium caulophylli</em> life cycle inferred from phylogenetic evidence and renamed as <em>Puccinia caulophylli</em> <em>comb. nov.</em> <em>Mycotaxon </em>134: 719–730.&nbsp; https://doi.org/10.5248/134.719</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2020a) Notes on rust fungi in China 8. <em>Pucciniastrum tiliae </em>life cycle and new host plants inferred from phylogenetic evidence. <em>Mycotaxon</em> 135: 491–500.&nbsp; https://doi.org/10.5248/135.491</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2020b) Notes on rust fungi in China 9. <em>Puccinia miscanthi </em>life cycle and morphology confirmed by inoculation. <em>Mycotaxon</em> 135: 525–534.&nbsp; https://doi.org/10.5248/135.525</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2020c) Life cycle and taxonomy of <em>Chrysomyxa</em> <em>succinea</em> in China and phylogenetic positions of <em>Caeoma</em> species on <em>Rhododendron</em>. <em>Forest Pathology</em> 2020;50: e12585.&nbsp; https://doi.org/10.1111/efp.12585</p>
<p>Ji, J.X., Li, Z., Li, Y. &amp; Kakishima, M. (2020d) Life cycle and taxonomy of <em>Melampsora</em> <em>abietis</em>-<em>populi</em> in China and its phylogenetic position in <em>Melampsora</em> on <em>Populus</em>.<em> Mycological Progress</em> 19: 1281–1291.&nbsp; https://doi.org/10.1007/s11557-020-01624-1</p>
<p>Jia, L.X. &amp; Li, Z.Y. (2011) A report of rust disease on glossy privet. <em>Northern Horticulture</em> 2011 (09): 174–176.</p>
<p>Jin, Y., Szabo, L.J. &amp; Carson, M. (2010) Century-old mystery of <em>Puccinia striiformis </em>life history solved with the identification of <em>Berberis</em> as an alternate host. <em>Phytopathology</em> 100: 432–435.&nbsp; https://doi.org/10.1094/PHYTO-100-5-0432</p>
<p>Jørstad, I. (1950) The graminicolous rust fungi of Norway. <em>Skrifter Norske Vidensk Akademie I </em>1950: 1–92.</p>
<p>Kakishima, M. &amp; Sato, S. (1988) Rust diseases of ornamental plants (II) Rusts of olomon’s seal and lily of valley caused by <em>Puccinia sessilis</em>.<em> Annals of</em> <em>the Phytopathological Society of Japan</em> 54: 60–63.</p>
<p>Kenaley, S.C., Hudler, G.W. &amp; Bergstrom, G.C. (2016) Detection and phylogenetic relationships of <em>Puccinia emaculata </em>and <em>Uromyces graminicola </em>(<em>Pucciniales</em>) on switchgrass in New York State using rDNA sequence information. <em>Fungal Biology</em> 120: 791–806.&nbsp; https://doi.org/10.1016/j.funbio.2016.01.016</p>
<p>Kim, C.J. (1963) A provisional list of <em>Uredinales</em> of Korea. <em>Korean</em> <em>Journal</em> <em>of Microbiology</em> 1: 51–64.</p>
<p>Leppik, E.E. (1965) Some viewpoints on the phylogeny of rust fungi. V. Evolution of biological specialization. <em>Mycologia</em> 57: 6–22.</p>
<p>Leppik, E.E. (1967) Some viewpoints on the phylogeny of rust fungi. VI. Biogenic radiation. <em>Mycologia</em> 59: 568–579.</p>
<p>Lee, S.H., Seo, S.T., Lee, S.K., Lee, C.K. &amp; Shin, H.D. (2019) First report of rust caused by aecial stage of <em>Puccinia klugkistiana </em>on <em>Ligustrum japonicum </em>in Korea. <em>Plant Disease</em> 103: 160.&nbsp; https://doi.org/10.1094/PDIS-07-18-1233-PDN</p>
<p>Li, Z., Li, Y., Wang, X. &amp; Wang, D.L. (2009) First report of the aecial stage of a rust disease caused by<em> Puccinia elymi</em> on <em>Thalictrum squarrosum</em> in China. <em>Plant Pathology</em> 58: 798.&nbsp; https://doi.org/10.1111/j.1365-3059.2009.02029.x</p>
<p>Liu, M. &amp; Hambleton, S. (2010) Taxonomic study of stripe rust, <em>Puccinia striiformis</em> sensu lato, based on molecular and morphological evidence. <em>Fungal Biology </em>114: 881–899.</p>
<p>Liu, M. &amp; Hambleton, S. (2013) Laying the formation for a taxonomic review of <em>Puccinia coronata</em> s.l. in a phylogenetic context. <em>Mycological Progress</em> 12: 63–89.&nbsp; https://doi.org/10.1007/s11557-012-0814-1</p>
<p>Liu, M., McCabe, E., Chapados, J.T., Carey, J., Wilson, S.K., Tropiano, R., Redhead, S.A., Lévesque, C.A. &amp; Hambleton, S. (2015) Detection and identification of selected cereal rust pathogens by TaqMan real-time PCR. <em>Canadian Journal of Plant Pathology</em> 37: 92–105.&nbsp; https://doi.org/10.1080/07060661.2014.999123&nbsp;</p>
<p>Ma, X., Liu, Y., Li, Q., Tian, X., Du, Z., Kang, Z. &amp; Zhao, J. (2020) Identification of<em> Berberis</em> spp. as alternate hosts for <em>Puccinia achnatheri</em>-<em>sibirici</em> under controlled conditions and morphologic observations of sexual stage development of the rust fungus. <em>Frontiers in Microbiology</em> 11: 1278.&nbsp; https://doi.org/10.3389/fmicb.2020.01278</p>
<p>Maier, W., Wingfield, B.D., Mennicken, M. &amp; Wingfield, M.J. (2007) Polyphyly and two emerging lineages in the rust genera<em> Puccinia</em> and <em>Uromyces</em>. <em>Mycological Research</em> 111: 176–185.&nbsp; https://doi.org//10.1016/j.mycres.2006.11.005</p>
<p>McTaggart, A.R., Shivas, R.G., Van der Nest, M.A., Roux, J., Wingfield, B.D. &amp; Wingfield, M.J. (2016) Host jumps shaped the diversity of extant rust fungi (<em>Pucciniales</em>).<em> New Phytologist</em> 209:1149–1158.&nbsp; https://doi.org/10.1111/nph.13686</p>
<p>Miura, M. (1928) <em>Flora of Manchuria and east Mongolia </em>Ⅲ. <em>Cryptogams, Fungi</em>. Minamimanshutetsudo, Dalian, China.</p>
<p>O’Donnell, K. (1993) <em>Fusarium</em> and its near relatives. <em>In</em>: Reynolds, D.R. &amp; Taylor, J.W. (Eds.) <em>The fungal holomorph</em>: <em>mitotic, meiotic and pleomorphic speciation in fungal systematics</em>. CAB International, Wallingford, UK, pp. 225–233.</p>
<p>Ono, Y. (2008) Why life-cycle studies?: Implications in the taxonomy of rust fungi (Uredinales). <em>Nippon Kingakukai Kaiho</em> 49: 1–28.&nbsp; https://doi.org/10.18962/jjom.jjom.H19-01</p>
<p>Ono, Y. &amp; Azbukina, Z.M. (1997) Heteroecious life cycle of two graminicolous <em>Puccinia </em>(<em>Urediniales</em>).<em> Mycoscience </em>38: 281–286.&nbsp; https://doi.org/10.1007/BF02464085</p>
<p>Padamsee, M. &amp; McKenzie, E.H.C. (2017) The intriguing and convoluted life of a heteroecious rust fungus in New Zealand. <em>Plant Pathology </em>66: 1248–1257.&nbsp; https://doi.org/10.1111/ppa.12672</p>
<p>Petersen, R.H. (1974) The rust fungus life cycle. <em>Botanical Review</em> 40: 453–513.</p>
<p>Posada, D. &amp; Crandall, K.A. (1998) MODELTEST: testing the model of DNA substitution. <em>Bioinformatics</em> 14: 817–818.</p>
<p>Rambaut, A. (2014) FigTree v1.4.2, A graphical viewer of phylogenetic trees. [http://tree.bio.ed.ac.uk/software/figtree/]</p>
<p>Roelfs, A.P. &amp; Bushnell, W.R. (Eds.) (1985) <em>The cereal rust vol</em>. <em>2</em>. Academic Press, Orland, USA.</p>
<p>Roy, B.A., Vogler, D.R., Bruns, T.D. &amp; Szaro, T.M. (1998) Cryptic species in the <em>Puccinia</em> <em>monoica</em> complex. <em>Mycologia</em> 90: 846–853.&nbsp; https://doi.org/10.1080/00275514.1998.12026978</p>
<p>Sato, T. &amp; Sato, S. (1982) Aeciospore surface structure of the Uredinales. <em>Transactions of Mycological Society of Japan</em> 23: 51–63.</p>
<p>Sato, T. &amp; Sato, S. (1985) Morphology of aecia of the rust fungi. <em>Transactions of British Mycological Society</em> 85: 223–238.</p>
<p>Savile, D.B.O. (1984) Taxonomy of the cereal rust fungi. <em>In</em>: Bushnell, W.R. &amp; Roelfs, A.P. (Eds.) <em>The Cereal Rusts, vol</em>. <em>1</em>. Academic Press, Orlando, USA, pp. 79–112.</p>
<p>Soreng, R.J., Peterson, P.M., Romaschenko, K., Davidse, G., Zuloaga, F.O., Judziewicz, E.J., Filgueiras, T.S., Davis, J.I. &amp; Morrone, O. (2015) A worldwide phylogenetic classification of the <em>Poaceae</em> (<em>Gramineae</em>). <em>Journal of Systematics and Evolution</em> 53: 117–137.&nbsp; https://doi.org/10.1111/jse.12150</p>
<p>Swofford, D.L. (2019) <em>PAUP</em>*: <em>Phylogenetic analysis using parsimony and other methods, Version 4</em>.<em>0a165</em>. Sinauer Associates, Sunderland, USA.</p>
<p>Szabo, L. (2006) Deciphering species complexes: <em>Puccinia andropogonis</em> and <em>Puccinia</em> <em>coronata</em>, examples of differing modes of speciation.<em> Mycoscience</em> 47: 130–136.</p>
<p>Tai, F.L. (1979) <em>Sylloge fungorum Sinicorum</em>. Science Press, Beijing, China.</p>
<p>Taylor, J.W., Jacobson, D.J., Kroken, S., Kasuga, T., Geiser, D.M., Hibbett, D.S. &amp; Fischer, M.C. (2000) Phylogenetic species recognition and species concepts in fungi. <em>Fungal Genetics and Biology</em> 31: 21–32.</p>
<p>Termorshuizen, A.J. &amp; Swertz, C.A. (2011) <em>Dutch rust fungi</em>. Aad Termorsguizen, Netherland.</p>
<p>Van der Merwe, M.M., Walker, J., Ericson, L. &amp; Burdon, J.J. (2008) Coevolution with higher taxonomic host groups within the <em>Puccinia</em>/<em>Uromyces</em> rust lineage obscured by host jumps. <em>Mycological Research</em> 112: 1387–1408.&nbsp; https://doi.org/10.1016/j.mycres.2008.06.027</p>
<p>Virtudazo, E.V., Nakamura, H. &amp; Kakishima, M. (2001) Phylogenetic analysis of sugarcane rusts based on sequences of ITS, 5.8S rDNA and D1/D2 regions of LSU rDNA. <em>Journal of General Plant Pathology</em> 67: 28–36.&nbsp; https://doi.org/10.1007/PL00012983</p>
<p>Wang, Y.C. (1951) <em>Index</em> <em>Uredinearum</em> <em>Sinensium</em>. Academia Sinica, Beijing, China.</p>
<p>Wang, Y.C. (1965) New species of graminicolous rust fungi from China. <em>Acta Phytotaxa</em> 10: 291–299.</p>
<p>Wang, Y.C. &amp; Wei, S.X. (1983) <em>Taxonomic</em> <em>studies</em> <em>on</em> <em>graminicolous</em> <em>rust</em> <em>fungi</em> <em>of</em> <em>China</em>. Science Press, Beijing, China.</p>
<p>White, T.J., Bruns, T., Lee, S. &amp; Taylor, J. (1990) Amplification and direct sequence of fungal ribosomal RNA genes for phylogenetics. <em>In: </em>Innis, M.A., Gelfand, D.H., Sninsky, J.J. &amp; White, T.J. (Eds.) <em>PCR protocols</em>: <em>a guide to methods and applications</em>. Academic Press, San Diego, USA, pp. 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1</p>
<p>Wilson, M. &amp; Henderson, D.M. (1966) <em>The British rust fungi</em>. Cambridge University Press, Cambridge, UK.</p>
<p>Zambino, P.J. &amp; Szabo, L.J. (1993) Phylogenetic relationships of selected cereal and grass rusts based on rDNA sequence analysis. <em>Mycologia</em> 85: 401–414.&nbsp; https://doi.org/10.1080/00275514.1993.12026292</p>
<p>Zhao, P., Kakishima, M., Wang, Q. &amp; Cai, L. (2017) Resolving the <em>Melampsora epitea</em> complex. <em>Mycologia</em> 109: 391–407.&nbsp; http://dx.doi.org/10.1080/00275514.2017.1326791</p>
<p>Zhao, P., Wang, Q.H., Tian, C.M. &amp; Kakishima, M. (2015) Integrating a numerical taxonomic method and molecular phylogeny for species delimitation of<em> Melampsor</em>a species (<em>Melampsoraceae</em>, <em>Pucciniales</em>) on willows in China. <em>PLoS ONE</em> 10: e0144883.&nbsp; https://doi.org/10.1371/journal.pone.0144883</p>
<p>Zhuang, J.Y., Wei, S.X. &amp; Wang, Y.C. (1998) <em>Flora fungorum Sinicorum, vol</em>.<em>10, Uredinales </em>(<em>1</em>). Science Press, Beijing, China.</p>