Abstract
A new rust fungus was found on Lygodium flexuosum at Doi Suthep-Pui National Park in Chiang Mai Province, Thailand. Puccinia lygodii was the only rust fungus currently known on Lygodium spp. (Lygodioideae, Schizaeaceae, Schizaeales) from southern North America through northern South America. The new fungus produced uredinia linearly between veins, causing yellowish streaks, on the abaxial frond surface. The sori were covered with a layer of thin-walled fungal cells beneath the host epidermis and surrounded by thin-walled paraphyses. The sori did not have a distinct central aperture with ostiolar cells but ruptured irregularly to release urediniospores. Urediniospores were obovoid, obovoid-ellipsoid, or pyriform. The wall was thin, colorless, and completely echinulate. Neither amphispores nor teliospores were observed. The sorus and spore morphology indicated the taxonomic affinity of the fungus to the fern rust genera Hyalopsora and Milesina. A molecular phylogenetic analysis using nuclear large subunit ribosomal DNA sequence revealed that the Lygodium rust fungus was grouped in a paraphyletic Milesina clade. From the putative host preference, morphology, and estimated phylogenetic relationships, it was concluded that the fungus was a new species of Milesina.
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References
Aime MC (2006) Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience 47:112–122. https://doi.org/10.1007/S10267-006-0281-0
Aime MC, Bell CD, Wilson AW (2018) Deconstructing the evolutionary complexity between rust fungi (Pucciniales) and their plant hosts. Stud Mycol 89:143–152. https://doi.org/10.1016/j.simyco.2018.02.002
Anonymous (1960) Index of plant diseases in the United States. U.S.D.A. Agric Handb 165:1–531
Arthur JC (1924) New species of Uredinales - XV. Bull Torrey Bot Club 51:51–59
Bubner B, Buchheit R, Friedrich F, Kummer V, Scholler M (2019) Species identification of European forest pathogens of the genus Milesina (Pucciniales) using urediniospore morphology and molecular barcoding including M. woodwardiana sp. nov. MycoKeys 48:1–40. https://doi.org/10.3897/mycokeys.48.30350
Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217. https://doi.org/10.11646/Phytotaxa.261.3.1
Christenhusz MJM, Chase MW (2014) Trends and concepts in fern classification. Ann Bot 113:571–594. https://doi.org/10.1093/aob/mct299
Christenhusz MJM, Fay MF, Chase MW (2017) Plants of the world. An illustrated encyclopedia of vascular plants. University of Chicago Press, Chicago. 816 pp.
de Vienne DM, Refregier G, Lopez-Villavicencio M, Tellier A, Hood ME, Giraud T (2013) Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol 198:347–385. https://doi.org/10.1111/nph.12150
Faull JH (1932) Taxonomy and geographical distribution of the genus Milesia. Contributions from the Arnold Arboretum of Harvard University 2: 1–138
Faull JH (1938) Taxonomy and geographical distribution of the genus Uredinopsis. Contributions from the Arnold Arboretum of Harvard University 11: 1–120
Faull JH (1947) Tropical fern hosts of rust fungi. J Arnold Arboret 28:309–319
Gardner S, Sidisunthorn P, Anusarnsunthorn V (2000) A field guide to forest trees of northern Thailand. Kobfai Publishing Project, Bangkok. 560 pp.
Hanks JG (1998) A monographic study or Lygodium Swartz (Pteridophyta: Lygodiaceae). Ph. D. dissertation, City University of New York. 742 pp.
Hart JA (1988) Rust fungi and host plant coevolution: do primitive hosts harbor primitive parasites? Cladistics 4:339–366. https://doi.org/10.1111/j.1096-0031.1988.tb00519.x
Hennen JF (1997) Uredo vetus sp. nov., the first record of a rust on Selaginella, and the use of the name Uredo. Mycologia 89:801–803. https://doi.org/10.2307/3761137
Hiratsuka N (1936) A monograph of the Pucciniastraceae. Mem Tottori Agric Coll 4:1–374
Kasuya T, Ono Y (2018) Herpobasidium filicinum (Eocronartiaceae, Platygloeales) occurs on Dennstaedtia wilfordii (Dennstaedtiaceae) in Japan. Mycoscience 59:443–448. https://doi.org/10.1016/j.myc.2018.03.001
Katoh K, Standly DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Khamyong N, Wangpakapattanawong P, Chairuangsri S, Inta A, Tiansawat P (2018) Tree species composition and height-diameter allometry of three forest types in northern Thailand. Chiang Mai Univ J Nat Sci 17: 289–306; Doi: https://doi.org/10.12982/CMUJNS.2018.0021
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/mst054
Kuprevich V, Transhel V (1957) Cryptogamic plants of the USSR, Vol. IV, Rust fungi. No. 1, Family Melampsoraceae. The Academy of Science U.S.S.R. Moscow. 518 pp.
Lindsay and Middleton (2012 onwards), Ferns of Thailand, Laos, and Cambodia. http://rbg-web2.rbge.org.uk/thaiferns/.
Mabberley DJ (1997) The plant book, 2nd edn. Cambridge University Press, Cambridge. 780 pp.
Madeira PT, Pemberton RW, Center TD (2008) A molecular phylogeny of the genus Lygodium (Schizaeaceae) with special reference to the biological control and host range testing of Lygodium microphyllum. Biol Contr 45:308–318.
Maier W, Begerow D, Weiß M, Oberwinkler F (2003) Phylogeny of the rust fungi: An approach using nuclear large subunit ribosomal DNA sequences. Can J Bot 81:12–23. https://doi.org/10.1139/b02-113.
Magnus P (1904) Ein weiterer Beitrag zur Kenntnis der Gattung Uredinopsis. Hedwigia 43:119–125
McTaggart AR, Geering AWD, Shivas RG (2014) Uredinopsis pteridis and Desmella aneimiae, the first rust fungi (Pucciniales) reported on ferns (Pteridophyta) in Australia. Aust Plant Dis Notes 9:149. https://doi.org/10.1007/s13314-014-0149-7
McTaggart AR, Shivas RG, van der Nest MA, Roux J, Wingfield BD, Wingfield MJ (2016) Host jumps shaped the diversity of extant rust fungi (Pucciniales). New Phytol 209:1149–1158. https://doi.org/10.1111/nph.13686
Nylander, J. A. A. (2004). MrModeltest 2.3. Program distributed by the author. Uppsala: Evolutionary Biology Centre, Uppsala University.
O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) the fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal. CABI, Wallingford, pp 225–233
Ono Y, Hennen JF (1983) Taxonomy of the chaconiaceous genera (Uredinales). Trans Mycol Soc Jpn 24:369–402
Padamsee M, McKenzie EHC (2014) A new species of rust fungus on the New Zealand endemic plant, Myosotidium, in isolated Chatham Islands. Phytotaxa. 174:223–230.
Ronquist F, Teslenko M. van der Mark P, Ayres DL, Darling A, Hohna, S, Larget B, Liu L, 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. https://doi.org/10.1093/sysbio/sys029
Rothfels CJ, Sundue MA, Kuo L-Y, Larsson A, Kato M, Schuettpelz E, Pryer KM (2012) A revised family-level classification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon 61:515–533. https://doi.org/10.1002/tax.613003
Roy BA (2001) Patterns of association between crucifers and their flower-mimic pathogens: host jumps are more common than coevolution or cospeciation. Evolution 55:41–53. https://doi.org/10.1554/0014-3820(2001)055[0041:POABCA]2.0.CO;2
Sawyer JO Jr, Chermsirivathana CA (1969) A flora of Doi Suthep, Doi Pui, Chiang Mai, North Thailand. Nat Hist Bull Siam Soc 23:99–132
Schuettpelz E, Pryer KM (2007) Fern phylogeny inferred from 400 leptosporangiate species and three plastid genes. Taxon 56:1037–1050. https://doi.org/10.2307/25065903
Shen H, Jin D, Shu J-P, Zhou X-L, Lei M, We R, Shang H, Wei H-J, Zhang R, Liu L, Gu Y-F, Zhang X-C, Yan Y-H (2018) Large-scale phylogenomic analysis resolves a backbone phylogeny of ferns. GigaScience 7:1–11. https://doi.org/10.1093/gigascience/gix116
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127011-0056-0
Sjamsuridzal W, Nishida H, Ogawa H, Kakishima M, Sugiyama J (1999) Phylogenetic positions of rust fungi parasitic on ferns: evidence from 18S rDNA sequence analysis. Mycoscience 40:21–27. https://doi.org/10.1007/BF02465669
Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG (2006) A classification for extant ferns. Taxon 55:705–731. https://doi.org/10.2307/25065646
Sydow H, Petrak F (1931) Mycromycetes philippinenses. Series secunda. Ann Mycol 29:145–279
Sydow H, Sydow P (1918) Mykologische Mitteilungen. Ann Mycol 16:240–248
Vasco A, Moran RC, Ambrose BA (2013) The evolution, morphology, and development of fern leaves. Front Plant Sci 4(345):345. https://doi.org/10.3389/fpls.2013.00345
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Zhuang J-Y (1983) A provisional list of Uredinales of Fujian Province, China. Acta Mycol Sin 2:146–158
Acknowledgments
This study was carried out under the permission from the National Research Council of Thailand for the international project entitled “Taxonomy and life cycle of rust fungi with special reference to grapevine and fern leaf rusts” (Project ID: 2018/043). We thank the Department of National Park, Wildlife and Plant Conservation, Ministry of Natural Resources and Environment, Thailand, for permitting to survey plant rusts and to sample rusted plant leaves at Doi Suthep-Pui National Park.
The Forest Herbarium (the Department of National Park, Wildlife and Plant Conservation) provided us with the opportunity to examine Lygodium specimens for search of possible rust infection.
Funding
This study was supported, in part, by a Grant-in-Aid (G-2018-1-019) from the Institute of Fermentation, Osaka (IFO) (YO), and a Grant-in-Aid for Scientific Research (A) No. 14255004 from the Ministry of Education, Science and Culture, Japan (YO).
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Ono, Y., Ohmachi, K., Unartngam, J. et al. Milesina thailandica, a second rust fungus on an early diverged leptosporangiate fern genus, Lygodium, found in Thailand. Mycol Progress 19, 147–154 (2020). https://doi.org/10.1007/s11557-019-01549-4
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DOI: https://doi.org/10.1007/s11557-019-01549-4