Plant Pathology & Quarantine 7(1): 1–14 (2017) www.ppqjournal.org Copyright © 2017 Article ISSN 2229-2217 PPQ Online Edition Doi 10.5943/ppq/7/1/1 Uromyces trifolii, a new addition to rust fungi of Himachal Pradesh, India, with a checklist of Uromyces in India Gautam AK1* and Avasthi S2 1 2 School of Agriculture, Faculty of Science, Abhilashi University, Mandi (H.P.) 175028, India Department of Botany, Abhilashi Institute of Life Sciences, Mandi (H.P.) 175008, India Gautam AK, Avasthi S 2017  Uromyces trifolii, a new addition to rust fungi of Himachal Pradesh, India with a checklist of Uromyces in India. Plant Pathology & Quarantine 7(1), 1–14, Doi 10.5943/ppq/7/1/1 Abstract Uromyces is a genus of rust fungi that infects both monocots and dicots throughout the world. The genus is particularly common on plant families like Asteraceae, Euphorbiaceae, Fabaceae, Liliaceae, Poaceae, and Loranthaceae. A rust infection was observed on leaves and stem of Trifolium repens from Himachal Pradesh, India. The symptoms appeared as dark brown to blackish brown pustules. Morphological and microscopic analyses of diseased samples identified it as Uromyces trifolii, which is new to Himachal Pradesh. Taxonomic descriptions and illustrations of the specimen are given. A checklist to assess diversity and distribution of the genus Uromyces in India is provided. Key words – checklist – Himachal Pradesh – new record – rust fungi – Trifolium repens Introduction Uromyces (Link) Unger, a genus of rust fungi was proposed by Unger (1833). There are more than 1562 taxonomic names within this genus worldwide (IndexFungorum 2016). According to Cummins & Hiratsuka (2003) it is the second largest genus of rust fungi next to Puccinia and contains more than 600 reported species. It is mainly characterized by 1-celled teliospores which differentiate it from Puccinia, which has 2-celled teliospores. Uromyces infects both monocots and dicots throughout the world, infecting plant families like Asteraceae, Euphorbiaceae, Fabaceae, Liliaceae, and Poaceae, but Loranthaceae is a major one (Vidal-Russell & Nickrent 2008). The genus has a wide diversity and host range in India also. Himachal Pradesh, the northern hilly state of India is situated in the western part of Himalaya. It is a mountainous state with elevations ranging from about 350–7,000 m above sea level. Climatic conditions vary from hot and sub-humid tropical in the southern tracts to cold, alpine and glacial in the northern and eastern mountain ranges. The changeable geographical and climatic conditions of the state are favourable for biodiversity including growth and development of plant pathogens. One of the most important characteristics of plant rusts is their exceptionally high degree of host specificity. The vast biodiversity and climatic conditions of the state lead to a wide rust diversity, distribution and host range of this fungal group. Submitted 17 February 2016, Accepted 4 November 2016, Published 24 January 2017 Corresponding Author: A. K. Gautam – e-mail – a2gautam2006@gmail.com 1 A rust infection was observed on leaves and stems of Trifolium repen L. (Fabaceae) during our routine phytopathological survey from district Mandi of Himachal Pradesh in 2015. A detailed taxonomic study and survey of the literature as well as comparative analyses revealed that the fungus is a new addition to the rust fungi in Himachal Pradesh (Mukherji & Juneja 1974, Sarbhoy 1975, 1980, Bilgrami 1991, Jamaluddin et al. 2004). The disease was studied further and is described in the present study. A checklist to assess diversity and distribution of the genus Uromyces in India is also provided. Materials and methods Naturally infected plant parts showing rust symptoms were collected from Chail Chowk area of district Mandi, Himachal Pradesh. Infected leaves and stems were placed in separate polythene bags and taken to the laboratory for further examination. Specimens are deposited in the Abhilashi University Mycological Herbarium (AUMH), School of Agriculture, Faculty of Science, Abhilashi University, Mandi, Himachal Pradesh, India. Morphological features of all specimens were noted, and measurements were made. Diseased spots were photographed with a Sony DSC-X80 camera. Mounts of spores and free-hand sections of sori were prepared in lactophenol and heated to boiling. The fungal structures were examined under a light microscope (Olympus). At least 25 measurements for each microscopic structure were taken. Taxonomic analyses were made by consulting relevant literature and illustrations are given in accordance with Cummins & Hiratsuka (2003). A checklist of the genus Uromyces was also prepared to assess diversity and distribution in India. An exhaustive bibliographic survey of the literature published in various national and international journals, monographs, books, book chapters and magazines on these rust fungi was carried out. Some species names as reported in the cited publications have been replaced with their currently accepted name according to the Species Fungorum website (Speciesfungorum 2016). Results Trifolium repens is a perennial, herbaceous, low growing flowering plant of family Fabaceae and is commonly known as white clover. It is considered as a folk medicine in India, used against intestinal helminthic worms. An experimental in vivo study validated that the aerial shoots of T. repens bear significant anticestodal properties (Yadav et al. 2004). On leaves and stem dark brown to blackish brown telial pustules were observed (Fig. 1). Taxonomy Uromyces trifolii (R. Hedw.) Lév., Annls Sci. Nat., Bot., sér. 3, 8: 371 (1847) (Figs. 1, 2) =Uromyces flectens Lagerh., Svensk bot. Tidskr. 3: 36 (1909). =Uromyces nerviphilus (Grognot) Hotson, Publ. Puget Sound Biol. Sta. Univ. Wash. 4: 368 (1925). Telia mostly hypophyllous, sometimes epiphyllous, rounded, scattered, subepidermal, erumpent, pulverulent, surrounded by the ruptured epidermis, dark brown to blackish brown, 0.08– 0.19 × 0.09–0.3 mm. Teliospores globose to subglobose or ellipsoid to obovoid, 21–30 × 15–24 μm (mean 26.0 × 19.6 μm), the apex rounded with minute hyaline papilla; wall 1–2 μm thick, brown to chestnut brown, smooth or with minute scattered warts; apex 3–4 μm thick, germ pore 1; pedicel hyaline, 4–8 μm wide and up to 24 μm long. Spermagonia, aecia and uredinia not found. Material examined − On Trifolium repens L., with III stage, India, Himachal Pradesh, Chail Chowk (Mandi), at 1400 m, 24 August 2015, coll. Ajay K. Gautam (AUMH 1030). 2 Fig 1  Rust infection on Trifolium repens caused by Uromyces trifolii. Fig 2  Uromyces trifolii: Teliospores. Scale bar = 20 µm. Diversity and distribution Species of Uromyces infect both monocots and dicots throughout the world. Ninety-seven species of Uromyces have been identified and reported from India on 180 plant host species that belongs to 85 genera and 32 families. Thirty species have been found associated with family Fabaceae followed by Poaceae (23), Asteraceae (6), Lamiaceae and Caprifoliaceae (3 each) and Polygonaceae, Cyperaceae, Euphorbiaceae, Asparagaceae, Acanthaceae and Oleaceae (2 each). 3 The remaining host plant families are associated with a single species of Uromyces (Table 1). Of 97 Uromyces species reported from India, only 15 species are reported from Himachal Pradesh. Uromyces species have also been found in nineteen other states of India (Table 1). Discussion Based on morphological characteristics the rust on Trifolium repens was identified as Uromyces trifolii. This rust has been previously reported on T. resupinatum (reversed clover) and T. pratense (red clover) from Haryana and Uttrakhand, respectively (Sydow & Butler 1907a, b, Padwick & Khan 1944, Hooda & Saini 1990, Sokhi et al. 1985). The genus Uromyces is mainly characterized by 1-celled teliospores. The Fabaceae (legume, pea, or bean family) and Poaceae (grass family) are particularly susceptible to infection of Uromyces spp. In India, 30 species of Uromyces have been reported on legumes and 23 species on grasses. Nearly 180 plant species that belong to 85 genera and 32 families are infected with Uromyces spp. Table 1 Uromyces species recorded in India. Taxa Hosts Distribution* References U. pavgei Goswami Achyranthes aspera & Nagachan U. lycoctoni Aconitum leave (Kalchbr.) Fuckel U. aconiti Fuckel Aconitum lycoctonum AS Goswami & Nagachan 1979 J&K Arthur 1934, Cummins 1943 J&K U. acori T.S. Ramakr. & Rangaswamy U. sporogoni subsp. asiaticus (T.S. Ramakr. & Rangaswami) Parmelee & Savile U. agropyri Barclay U. sphaeropleus Cooke U. aloes (Cooke) Magnus U. apludae Syd. & E.J. Butler U. amphilophisinsculptae T.S. Ramakr., Sriniv. & Sundaram U. andropogonisannulati Syd., P. Syd. & E.J. Butler Acorus calamus TN Arthur 1934, Arthur & Cummins 1936 Ramakrisnan & Rangaswamy 1948 Acorus calamus TN Ramakrisnan & Sundaram 1955a Agropyron sp. HP Barclay 1891 Allium cepa MS Cooke 1876 Aloe spicata, Aloe vera Alpuda aristata TN, MS Ajrekar & Tonapy 1923 MS, PB Sydow & Butler 1907a Amphilophus insculpta TN Ramakrisnan 1952 Andropogon annulatus BR, UP, UK, AP, MS, MP Sydow & Butler 1907a, b Andropogon pertussis UP, TN Ramakrisnan 1951a 4 Table 1 (continued) Taxa U. clignyi Pat & Har. U. schoenanthi Syd. & P. Syd. U. andropogonis Tracy U. commelinae Cooke U. anotidismonospermatis T.S. Ramakr. & Sund. U. inayati Syd. & P. Syd. U. clivalis Mitter U. lapponicus Lagerh. U. hydrabadensis Bhagnarayana, Ramachar & Niranjan Rao U. vestergreni P. Syd. & Syd. U. bidentis Lagerh. U. satarensis P.B. Chavan & Bakare U. blainvilleae Berk. U. leptodermus Syd. & P. Syd. Hosts Distribution* References Andropogon pumilus, Bothriochloa sp., Dichanthium annulatum, Ermopogon faveolatus, Heteropogon contortus, Themeda triandra, Andropogon schoenanthus Andropogon sp. TN, MS, AP, KR Ramakrisnan. 1953, Ramachar 1978, Hosagouder 1985 MS, KA, KL Sydow & Butler 1938 Kud, (J&K) Pachkheda 1985 Aneilema giganteum, Commelina benghalensis, C. obliqua, C. forskalii, C. tuberosa, C. kurzii, C. tricolor, C. attenuate, Cyanotis cristata, C. obtuse, C. axillaris, C. fasciculata, Murdannia divergens, M. versicolor, Zygomenes cucullata, Anotis monosperma KL, TN, MS, RJ, KA, UK Joshi 1958, Jain 1966, Patil 1966, Patil & Thirumalachar 1968, Rolla & Addala 1963, Sydow & Butler 1938 TN Ramakrisnan & Sundaram 1955a Apluda aristata, A. varia UK Sydow & Butler 1907a Argyrolobium flaccidum Astragalus maddenianus UK J&K Sydow & Mitter 1933 Cummins et al. 1943 Atylosa scarabaeoides AP Bhagyanarayana 1987 Bauhinia tomentosa, B. accuminata Bidens pilosa, Bidens sp. KA, TN, MS Magdum 1967, Sydow & Butler 1938 Ramakrisnan & Sundaram 1955a, Sydow & Butler 1938 Blainvillea latifolia MS Chavan & Bakare 1973a, b Blainvillea rhomboidea, B. acmella Brachiaria reptans, B. distachya, B. ramose, Panicum javanicum, P. prostratum, P. antidotale, P. maximum AP, MS Patil & Thirumalachar 1981, Sydow & Butler 1907a Mitter & Tandon 1932, Pandotra 1966, Ramakrisnan 1952, Sundaram 1964, Sydow & Butler 1938, Sydow & Butler 1938 TN, KL, KA BR, MS, AP, TN, WB, UP, 5 Table 1 (continued) Taxa Hosts Distribution* References U. ambiens Cooke Buxus sempervirens UK, HP U. loculiformis T.S. Ramakr. & K. Ramakr. U. ciceris-arietini (Grognot.) Jacz. & G. Boyer Chlorophytum attenuatum TN Cicer arietinum, Lathyrus aphaca, L. odoratus, Trogonella corniculata, T. polyrata, Vicia biennis, V. ervillia, V. faba, V. gracilis, V. hirsuta,V. narbonensis, V. sativa, V. tetrasperma Citrus reticulata, Dendrophthoe falcata, Loranthus sp., Crotalaria juncea, C.rustica, C. retusa, C. medicagenia BR, MS, MP, UP, DL, HP Agarwal 1959, Asthana 1957, Bhahadur & Singh 1967, Butler & Mcrae 1930, Jain 1966, Payak 1949, Payak 1962, Vasudeva 1950 TN, MS, Chavan 1975, Ponappa 1961 AP, UK, KR, UP, MS, KL, BR U. nilagiricus T.S. Ramakr. & K. Ramakr. U. decorates Syd. Barclay 1891, Cooke 1874, Sydow 1913 Ramakrisnan & Ramakrisnan 1948 Uromyces Dalbergia latifolia achrous Syd. & P. Syd. U. ascorus Syd. Dalbergia latifolia U. capitatus Syd. & Desmodium tiliaefolia P. Syd. Dicanthium annulatum U. appendiculatus Dolichos lablab, haseolus (Pers.) Link sp., P. mungo, P. vulgaris, P. aconitfolius, Vigna unguiculata, V. vexillata, Vigna sinensis KL Behera & Mukherji 1974, Chaudhari & Singh 1974, Hosagouder 1985, Khan 1994, Ramakrisnan & Sundaram 1955a, Patil 1966, Payak 1949, Prakash. 1979 Hosagouder 1985 KL UK Hosagouder 1985 Sydow 1913, Sydow 1937 MP TN, BR, MS, HP, KA, KA, RJ, AP, MP, GJ U. eragrostidis Tracy U. prominens (DC.) Lév. Eragrostis cynosuroides, Eleusine coracana Euphorbia hypericifolia, E. hispida, E. dracunculoides Euphorbia pilosa BR, UP J&K Mishra & Nema 1976 Butler & Mcrae 1930, Jain 1966, Joshi 1958, Nema & Mishra 1965, Patil 1966, Prasad & Sinha 1962, Ramakrisnan & Sundaram 1955a, b, Sydow & Butler 1907a, b Dublish & Singh 1977, Sydow & Butler 1907a Butlere & Bisby 1931, Chavan & Bakare 1977, Cummins 1943, Sydow & Butler 1938 Cummins 1943 Euphorbia thymifolia GJ Ajrekar 1912 Fritillaria roylei J&K Arthur & Cummins 1936 U. haussknechtii Tranz. U. euphorbiae Cooke & Peck U. fritillariae Thum. UP, MS, 6 Table 1 (continued) Taxa U. geranii (DC.) G.H. Otth & Wartm. U. sojae (P. Henn.) Syd. & P. Syd. U. hedysariobscuri (DC.) Carestia & Picc. U. macintirianus Barclay U. heterogenus Cooke U. muscari (Duby) Graves U. orientalis Syd. Hosts Distribution* References Geranium wallichianum, G. aconitifolium J&K, BR Cummins 1943, Sydow & Butler 1907a, Yadav 1963 Glycine max TN Ramakrisnan 1951b Hedysarum cachemirianum J&K Arthur 1934, Arthur & Cummins 1936 Hemigraphis latebrosa HP, BR Sydow & Butler 1938 Hibiscus esculentus MS Uppal 1935 Hyacinthus orientalis TN Agarwal 1985 Indigofera linifolia, I. cordifolia, I. glandulosa, I. hirta Indigofera tinctoria, I. linifolia BR, MP, MS Sydow & Butler 1907a, b, Thite & Patil 1975 AP, MS U. gemmatus Berk. & M.A. Curtis U. hobsonii Vize Jacquemontia paniculata MS Chavan & Bakare 1977, Joshi & Reddy 1958, Joshi & Reddy 1959, Manoharachery 1975, Saksena1955, Vasudeva 1960 Patil & Thirumalachar 1981 Jasminum grandiflorum, J. malbaricum, J. scandens, J. auriculatum AP, J&K, HP, UK, KA, MS, MP, BR, RJ U. comedens P. Syd. & Syd. U. pisi (DC.) G.H. Otth U. fabae (Pers.) de Bary Jasminum sp. AS Butler & Mcrae 1930, Jain 1966, Joshi 1958, Mishra 1976, Parndekar 1964, Patil 1966, Ramakrisnan & Sundaram 1955b, Rao 1989, Sydow & Butler 1907a, b, Yadav & Thirumalachar 1955 Vasudeva 1960 Lathyrus sativus BR Saksena 1956 Lathyrus sphaericus, L. sativus, L. odoratus, Lens esculenta, Pisum sativum, P. arvense,Vigna radiata, Ocimum sp., Vicia faba, V. biennis, V. hirsuta, V. tetrasperma, V. narborensis, V. gracilis, HP, UP, BR, UK., MS, KA, TN, MP Lespedeza bicolor J&K Butler & Mcrae 1930, Jain 1966, Kapooria & Sinha 1966, Kulshreshtha 1998, Mishra 1969, Mishra & Khare 1969, Mitter & Tandon 1932, Patel 1973, Pavgi & Upadhyay 1966, Sydow & Butler 1938, Sydow & Butler 1907a, b, Ramakrisnan & Sundaram 1955a, b Sydow & Butler 1907a U. indigoferae Dietel & Holw. U. lespedezaeprocumbentis (Schwein.) Lagerh. 7 Table 1 (continued) Taxa Hosts Distribution* References U. rugulosus Pat. U. lespedezaesericae S. Ahmad Lespedeza eriocarpa Lespedeza stenocarpa UK UK Saksena 1956 Sachin et al.1980 U. behenis (DC.) Unger U. striatus Sch. Lychnis indica J&K Sydow & Butler 1907a Medicago sativa, M. denticulata Mucuna pruriens, M. deeringiana, M. rajada, M. cochinchinensis J&K, MS, HR, PB, BR, WB, BR, MS, KL, AP Ocimum sp. AP Joshi 1958, Pandotra & Sastry 1969, Sydow & Butler 1938 Butler & Mcrae 1930, Chavan & Patil 1972, Prakash & Singh 1976, Rabenhorst 1878, Sydow & Butler 1907a, b Bhagyanarayana & Ravinder 1994 Orthosiphon glabratus TN Panicum antidotale Panicum miliare, P. repens Poa annua MP MS, BR, TN, CG, KA, AP HR Polygonum aviculare, P. cogatum, P. paronychioides J&K, HP, J&K Cummins 1943,Sydow & Butler 1907b, Sydow 1938 Pontederia cordata AS Agarwal & Sarbhoy 1986 Pseudarthria viscida MS Rhynchosia minima Rottboellia speciosa MS UP, HP, J&K Chavan 1975, Patil & Thirumalachar 1981 Arthur 1934, Patel et al. 1949 Sydow & Butler 1938 Rumex dentatus, R. vescarius, R. dentatus HR, MS, J&K Scilla indica, S. hyacinthine Scirpus affinis Scirpus maritimus Sesbania aegyptiaca RJ, MS U. mucunae Rabenh. U. ramacharii Ravinder & Bhagyan. U. orthosiphonis T.S. Ramakr & Shriniv. U. superfluens Syd. U. linearis Berk. & Broome U. dactylidis var. poae (Rabenh.) Grove U. polygoniavicularis var. polygoni-avicularis (Pers.) P. Karst. U. pontederiae W.R. Gerard U. pseudoarthriae Cooke U. dolicholi Arthur U. rottboelliae Arthur U. rumicis (Schumach.) G. Winter U. scillarum (Grev.) G. Wint. U. indicus Pat. U. scirpi Burrill U. poonensis W.D. More & Moni PB MS Ramakrisnan & Srinivasan 1950 Butler & Mcrae 1930, Sydow & Butler 1907b Saini & Chand 1984 Behera & Mukherji 1974, Patel et al. 1949, Pandotra & Sastry 1969 Chakrabarty 1983, Prasad et al. 1962 Butler & Bisby 1960 Arthur & Cummins 1936 More & Moniz 1964 8 Table 1 (continued) Taxa Hosts Distribution* References Butler & Mcrae 1930, Sydow & Butler 1938, Dublish & Singh 1977, Mishra et al. 1976, Narasimhan & Thirumalachar 1964 Annonymus 1954, Barclay 1890, Dietel 1890 U. setariae-italicae Yoshino Setaria italica, S. verticillata,V. glauca, Eriochola trypheron, Cordia rothii MS, AP, Bihar, Kerela, UK, UP, MP, WB U. sommerfeltii Hyl., Jorst. & Nannf. U. tenuicutis MacAlpine Solidago virgaurea HP Sporobolus diander AS, UP, MS U. wellingtonica T.S. Ramakr. & K. Ramakr. U. mussooriensis Syd. & P. Syd. U. strobilanthus Barclay U. triandrae T.S. Ramakr. & Shriniv. U. trifolii (R. Hedw.) Lév. Sporobolus indicus TN Stipa sibirica Uttk. Sydow & Butler 1938 Strobilanthes dalhausianus Themeda triandra HP, UP, UK, MP TN Trifolium pratense, T. repens, T. resupinatum HR, J&K, PB U. minor J. Schrot. U. anthyllidis (Grev.) J. Schroet. U. tripogonicola Payak & Thirum U. trichoneurae Doidge U. trogonellae Pass. U. valerianae (Schumach.) Lév. U. valerianaewallichii Arthur & Cummins U. viciae-fabae (Pers.) J. Schroet. U. phaseoli G. Winter U. vignae Barclay U. vossiae Barclay U. pianhyensis Henn. Trifolium resupinatum Trigonella foenumgraecum Tripogon jacquemontii, T. lisboa Tripogon lisboae MS Mitter & Tandon 1938, Mishra 1969, Sydow & Butler 1938 Ramakrisnan & Srinivasan 1950 Hooda & Saini 1990, Padwick & Khan 1944, Sokhi et al. 1985, Sydow & Butler 1907b, Annonymous 1950 Joshi 1958, Payak 1962, Sydow & Butler 1907 Patil & Date 1980b MS, Kaul 1962, Patil 1966 Trogonella emodi UK. Sydow & Mitter 1933 Valeriana wallichii J&K Pandotra & Sastry 1969 Valeriana wallichii, V. leschenaultia HP, UK Arthur & Cummins 1936, Butler & Bisby 1931 Vicia sativa, V. hirsuta, Lathyrus aphaca Vigna capensis UP Butler & Bisby 1931, Dube et al. 1979a, Shrivastava 1979 Chavan & Bakare 1974 Vigna vexillata Vossia speciosa Wedelia urticaefolia HP HP TN, KL MS, RJ, HP MS Butler & Bisby 1931, Dube et al. 1979b, Goswami & Singh 1973, Patil & Date 1980a, Ramakrisnan & Ramakrisnan 1948 Barclay A 1891 Barclay 1890 Hosagouder 1985, Padwick & Merh 1943 9 Table 1 (continued) Taxa U. wedeliaebiflorae Boedijn U. coronatus Miyabe & Nishida U. ignobilis (Syd. & P. Syd.) 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