________________________________Ciências Agrárias AN UPDATED LIST OF PLANT FUNGI FROM CEARÁ STATE (BRAZIL) II. RUSTS Francisco das Chagas Oliveira Freire1 Reinhard Berndt2 RESUMO – O presente trabalho apresenta uma lista atualizada das espécies de ferrugens (Basidiomicota, Uredinales), identificadas sobre plantas do estado do Ceará, atingindo, até o momento, um total de 113 espécies fúngicas associadas a 129 plantas hospedeiras. O gênero com o maior número de espécies foi Puccinia, com 46 espécies, seguido por Uromyces, com 21 espécies. Os gêneros Achrotelium, Chaconia, Dasyspora, Esalque, Hemileia, Kimuromyces, Maravalia, Melampsora, Phragmidium, Porotenus, Physopella, Prospodium, Pucciniosira, Sphaerophragmium, Sphenospora e Ypsilospora estão representados por uma espécie cada. Maravalia allophyli, Phakopsora merremiae, Prospodium bicristatum, Puccinia tianguensis, Uredo calatheae, Uredo stryphnodendri e Uromyces cearensis são incluídas como novas espécies. Dentre as espécies catalogadas, Coleosporium solidaginis, Phakopsora euvitis, Puccinia horiana e Uromyces transversalis foram introduzidas recentemente no Ceará através de material vegetativo infectado proveniente da região Sudeste. Palavras-chave: Ferrugens. Novas espécies. Levantamento. 1 INTRODUCTION This unique group of fungi parasitizes a wide range of host plants, including ferns, conifers and angiosperms, and have been classified in the Order Uredinales of the Class Basidiomycetes. The name rust fungi stems from the frequent orange to red-orange colour of the rust sori (sporulating structures). Their relationships with their hosts, on which they are completely dependent and with which they 1 Eng. Agrônomo, Ph.D., Plant Pathologist, Embrapa Agroindústria Tropical, Fortaleza, Ceará, Brasil, 60.511-110, [email protected] 2 Biólogo, Ph.D., Micologist, ETH Zurich, Institute of integrative Biology (IBZ), Switzerland Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 Ciências Agrárias have coevolved, are highly specialized. Although in their natural habitat they behave as obligate biotrophic parasites (CUMMINGS & HIRATSUKA, 2003). The only comprehensive study of rust fungi in Ceará State was provided by Almeida (1988). As part of a project to identify fungi associated with plants from Ceará State (Brazil), in progress since 1997, we present in this work the second list which encompasses rust fungi. 2 MATERIALS AND METHODS Specimens have been collected from all types of vegetation in different counties of Ceará state and examined using light (LM) and scanning electron microscopy (SEM). All determinations were based on a careful morphological study of the available spore stages and assigned to species using standard literature (CUMMINGS & HIRATSUKA, 2003). When necessary, for comparative purposes, specimens were borrowed from the following herbaria: Mycological Herbarium of the Centro de Ciências Agrárias da Universidade Federal do Ceará, Brazil (CCAM), Berlin (B) and Upsala (UPS). Holotypes were deposited in Herbarium of Brasilia University (UB). Additional specimens have been retained in the senior author,s personal herbarium (HFF), in Fortaleza city, State of Ceará (Brazil). 3 RESULTS AND DISCUSSION All rust species so far confirmed on plants from Ceará State are listed in Table 1. A total of 113 species and 129 host plants are included. One hundred and nine rust species belong to holomorph genera, while only Aecidium and Uredo are considered anamorphic. Puccinia is the most common genus encompassing a total of 46 species, followed by Uromyces with 21 species. Achrotelium, Chaconia, Dasyspora, Esalque, Hemileia, Kimuromyces, Maravalia, Melampsora, Phragmidium, Porotenus, Physopella, Prospodium, Pucciniosira, Sphaerophragmium, Sphenophora and Ypsilospora are represented by only one species each. 54 Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 Ciências Agrárias Species indicated by asterisks are new record for Ceará State or for Brazil. All others species, otherwise stated, were already reported by Almeida (1988). The species Maravalia allophyli, Phakopsora merremiae, Prospodium bicristatum, Puccinia tianguensis, Uredo calatheae, Uredo stryphnodendri and Uromyces cearensis represent new species and have been published elsewhere (BERNDT, 2002; BERNDT & FREIRE, 2004; BERNDT et al., 2007; 2008). Puccinia fuireniphila is proposed as a new name for Puccinia fuirenicola (BERNDT & FREIRE, 2004). Phakopsora phyllanthi and Phakopsora vernoniae are newly reported for Brazil and the New World, whilst Puccinia melaena is new for Brazil and Tocoyena guianensis (Rubiaceae) is new host genus for this fungus species. Arachis pintoi is also a new host for Puccinia arachidis in this State. Although rust infections are not generally fatal to plants, they may severely limit growth and fruiting ability. Among the species listed many are important pathogen of cultivated plants. The following diseases caused by rut fungi are considered to be economically important to farmers of Ceará State: corn leaf rust (Puccinia polysora), coffee leaf rust (Hemileia vastatrix), sugarcane rust (Puccinia melanocephala), bean rust (Uromyces appendiculatus), cowpea rust (Uromyces vignae), peanut rust (Puccinia arachidis) and sunflower rust (Puccinia helianthi). The species Coleosporium solidaginis, Phakopsora euvitis, Puccinia horiana and Uromyces transversalis were recently introduced into Ceará State through infected seedlings from southeast region (FREIRE et al., 2004). Due to the frequent introduction of contaminated or infected plant parts into Ceará State a strict eradication and control campaign must be implemented aiming to protect the fruit and the ornamental industries. However, all efforts by the Federal Plant Health Inspection may fail if the trade and sell of these materials continue without curtailment. Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 55 Ciências Agrárias Table1 – Rust species on plants from Ceará State (Brazil). (Continues) Species Aecidium cordiae Henn. & Magn. A. erigerontis Kern. & Whetzel* Achrotelium lucumae (Arth. & R. Johnston) Cummins Cerotelium fici (Butl.) Arth. Chaconia brasiliensis Ono & Henn.* Coleosporium ipomoeae (Schw.) Burr.* C. solidaginis (Schyw.) Thuem.* C. plumierae Pat. C. vernoniae Berk. & Cut. Crossopsora byrsonimatis (Henn.) R.S. Peterson C. notata (Arth. & J.R. Johnston) Arth. Dasyspora gregaria (Kuntze) Henn.* Esalque holwayi (H.S. Jacks.) J.F. Hennen, Figueiredo & A.A. Carvalho Hemileia vastatrix Berk. & Br. Kimuromyces cerradensis Dianese, Santos, Medeiros & Furlaneto* Maravalia allophyli R. Berndt & F. Freire* Melampsora euphorbiae (Schub.) Cast.* Phakopsora crotonis (Burr.) Arth. P. jatrophicola Cummins Ex Cummins P. gossypii (Lagh.) Hirat. P. cf. argentinensis (Speg.) Arth.* P. lenticularis (Mains) Buriticá & J.F.Hennen * P. melaena H. Syd.* P. merremiae R. Berndt & F. Freire* P. phyllanthi Dietel* P. euvitis Ono* 56 Hosts Cordia sp. Conyza sp. Lucuma grandiflora A. DC. Ficus carica L. Stryphnodendron coriaceum Ipomoea sp. Solidago canadensis L. Plumeria alba L. Elephantopus sp. Byrsonima sp. Byrsonima crassifolia H.B.K. Xylopia sp. Caesalpinia ferrea Mart. ex Tul. Coffea arabica L. Astronium fraxinifolium Schott Allophylus sp. Euphobia heterophylla L. Croton sp. Jatropha pohliana Muel. Arg. Gossypium hirsutum L. Croton sp. Lasiacis sp. Tocoyena guianensis Merremia aegypta Mart. Phyllanthus acidus Skeels. Vitis vinifera L. Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 Ciências Agrárias Table1 – Rust species on plants from Ceará State (Brazil). Species P. vernoniae Joerstad* Phragmidium sp. Physopella compressa (Mains) Cummins & Ramachar Porotenus sp.* Prospodium aff. anomalum* P. tecomicola (Speg.) Jacks. Holw. P. bicristatum R. Berndt & F. Freire* Puccinia abrepta Kern P. arachidis Speg. P. arechavaletae Speg. P. aristidae Tracy var. chaetariae Cummins & Hussain P. canaliculata (Schw.) Lagh.* P. cenchri Diet. & Holw. P.chaseana Arth. & Fromme P. cnici-oleracei Pers. ex Desm. P. conoclini Seym. ex Burr. P. cucumeris Henn. P. cynodontis Lacroix ex Desm. P. cyperi Arth. P. distinguenda (Syd.) Jacks. & Holw. (continuation) Hosts Vernonia sp. Rosa sp. Axonopus compressus Beauv. , Paspalum conjugatum Berg. Memora sp. Pleonotomus sp. Tabebuia serratifolia (Vahl) Nicholson Mansoa sp. Cyperus sp. Arachis hypogaea L.; Arachis pintoi Krapov. & W.C. Gregory Cardiospermum sp., Paulinia pinnata L., Serjania sp. Aristida setifolia H.B.K. Cyperus surinamensis Rottb. Cenchrus echinatus L. Anthephora hermaphrodita (L.) Kuntze Acanthospermum brasilum Schrank, Emilia sonchifolia DC., Spilanthes acmella Murr. Eupatorium ballotaefolium H.B.K. Cucumis anguria L. Cynodon dactilon (L.) Pers. Cyperus sp., Kyllinga odorata Vahl Ipomoea batatas Poir., I. crassicaulis Robinson , I. fistulosa Mart. ex Choisy Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 57 Ciências Agrárias Table1 – Rust species on plants from Ceará State (Brazil). (continuation) Species P. dolosa Arth. & Fromme var. circumdata (Mains) Ramachar & Cummins Hosts Panicum maximum Jacq. P. fuireniphila R. Berndt & F. Freire* comb. nov. P. helianthi Schw. P. heterospora Berk. & Curt. Fuirena umbellata Rottb. P. horiana Henn.* P. huberi Henn. P. hydrocotyles Cke. P. inaequata Jacks. & Holw.* P. insueta Winter* P. invaginata Arth. & Johnst.* P. lantanae Farl. P. lateritia Berk. & Curt. P. lithospermi Ell. & Kell. P. malvacearum Mont.* P. melanocephala Syd. & P. Syd.** P. melampodii Dietel & Holw.* P. mogiphanis Arth. P. neorotundata Cummins* P. oahuensis Ell. & Ev. P. obliqua Berk. & Curt. P. oxalidis (Lév.) Dietel & Ellis P. pappophori Cumm. P. pelargoni-zonalis Doidge* P. psidii Winter 58 Helianthus annuus L. Herissantia tiubae (K. Schum) Brizichy, Pseudabutilon spicatum R.E.Fr., Sida spinosa L., Wissadula amplissima (L.) R.E. Fries Chrysanthemum morifolium Ramt. Panicum microspermum Fourn. Hydrocotyle sp. Vernonia sp. Malpighiaceae Gouania sp. Lantana camara L. Diodia sp. Evolvulus sp. Urena sp. Saccharum officinarum L. Melampodium sp. Alternanthera polygonoide R. Br. var. diffusa Mart. Vernonia sp. Digitaria horizontalis Willd. Macroscepis sp. Oxalis sp. Leonotis sp. Pelargonium zonale Psidium guajava L., Myrcia sp. Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 Ciências Agrárias Table1 – Rust species on plants from Ceará State (Brazil). (continuation) Species P. polysora Underw. P. porophylli Henn.* P. posadensis Sacc. & Trott. P. purpurea Cke. P. sorghi Schw. P. thalliae Diet. P. tianguensis R. Berndt & F. Freire* P. ventanensis Mont.* P. verbesinae Schw. Pucciniosira pallidula (Speg.) Lagh. Ravenelia cassiaecola G.F. Atk. var. cassiaecola* Ravenelia cebil Speg. R. cohniana Henn. R. indigoferae Tranz. & Dietel R. oligotheles Speg.* R. pileolariodes Syd. & P. Syd. R. pithecolobii Arth. Sphaerophragmium acaciae (Cke.) Magn. Sphenospora smilacina H. Syd.* Uredo anthurii (Har.) Sacc.* Uredo cf. borreriae (Henn.) Kern & Whetzel Uredo calatheae R. Berndt & F. Freire* U. centrosemae Viégas* U. cf. chrysophylli Syd.* U. coccolobae Henn. Hosts Zea mays L. Porophyllum sp. Andropogon condensatus H.B.K. Sorghum vulgare Pers., S. bicolor (L.) Moench Zea mays L. Canna indica L. Hyptis sp. Alternanthera brasiliana Moq. Verbesina diversifolia DC. Triumfetta sp. Chamaecrista hispidula (Vahl) Irv. & Barn. Anadenanthera colubrina (Vell.) Brenan var. cebil (Griseb.) Altschul Caesalpinia pulcherrima Sw. Indigofera suffruticosa Mill. Albizzia inundata (Mart.) Barneby & Grimes Caesalpinia pyramidalis Tul. Pithecellobium multiflorum Benth. Albizzia lebbek Benth. Smilax sp. Anthurus sp. Borreria sp. Calathea neoviedii Petersen Centrosema brasilianum (L.) Benth. Chrysophyllum sp., Sideroxylon sp. Coccoloba sp. Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 59 Ciências Agrárias Table1 – Rust species on plants from Ceará State (Brazil). (continuation) Species U. cypericola Henn. U. cf. guettardae Hirats. & Hashioka* U. hymenaeae Mayor U. ignava Arth. U. stryphnodendri R. Berndt & F. Freire * Uromyces appendiculatus var. appendiculatus (Pers.) Unger Hosts Cyperus sp. Guettarda angelica Mart. Hymenaea sp. Bambusa sp.; Guadua tagora Kunth. Stryphnodendron coriaceum Benth. Phaseolus vulgaris L. U. appendiculatus (Pers.) Unger var. brasiliensis R. Alm. Phaseolus lathyroides L., P. martii Benth. , P. panduratus Mart. U. asclepiadis Cke. U. bauhiniae Henn. U. bidenticola Arth. U. blainvilleae Berk. U. bradburyae Jacks. & Holw. U. castaneus P. Syd. & Syd. U. cearensis R. Berndt & F. Freire* U. cestri Bert. ex Mont. U. commelinae Cke. U. cucullatus Syd. & P. Syd. U. euphorbiae Cke. & Pk. U. decoratus Syd.* U. manihoticola Henn. U. neurocarpi Diet. Asclepias curassavica L. Bauhinia sp. Bidens pilosa L. Blainvillea rhomboidea Cass. Centrosema pubescens Benth. Desmodium incanum DC. Ipomoea sp. Cestrum sp. Commelina nudiflora L. Wedelia scaberrima Benth. Euphorbia hyssopifolia L. Crotalaria retusa L. Manihot esculenta Crantz Clitoria laurifolia Poir , Galactia sp. Bauhinia sp. Euphorbia hirta L. Panicum maximum Jacq., Setaria viridis Beauv. U. perlebiae Vestergren U. proeminens (DC) Pass. U. setariae-italicae Yosh. 60 Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 Ciências Agrárias Table1 – Rust species on plants from Ceará State (Brazil). (conclusion) Species U. transversalis Winter* U. vignae Barcl.* Ypsilospora tucumanensis Hernandez et J.F.Hennen* Hosts Gladiolus sp. Vigna unguiculata (L.) Walp. Inga sp. 4 CONCLUSIONS Despite its small geographic area Ceará State presents a remarkable variation in its vegetation and a wide mycological biodiversity as shown in the table above. Many other rust species may be present in the ecologically different habitats waiting to be collected and described. AN UPDATED LIST OF PLANT FUNGI FROM CEARÁ STATE (BRAZIL) II. RUSTS ABSTRACT - This work presents an updated list of rust fungi (Basidiomycota, Uredinales) from plants of Ceará State (Brazil). A total of 113 species and 129 host plants are included. Puccinia is the most common genus presenting a total of 46 species, followed by Uromyces with 21 species. Achrotelium, Chaconia, Dasyspora, Esalque, Hemileia, Kimuromyces, Maravalia, Melampsora, Phragmidium, Porotenus, Physopella, Prospodium, Pucciniosira, Sphaerophragmium, Sphenospora and Ypsilospora are represented by only one species each. The species Maravalia allophyli, Phakopsora merremiae, Prospodium bicristatum, Puccinia tianguensis, Uredo calatheae, Uredo stryphnodendri and Uromyces cearensis represent new species. Coleosporium solidaginis, Phakopsora euvitis, Puccinia horiana and Uromyces transversalis were recently introduced into Ceará State through infected seedlings from southeast region. Key words: Rust. Survey. New species. Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013 61 Ciências Agrárias REFERENCES ALMEIDA, R.T. Espécies de Uredinales do estado do Ceará. Fortaleza: Universidade Federal do Ceará. 1988. 39p. (Boletim Técnico Científico, Série Fitotecnia 1). BERNDT, R. New species, reports and observations on rust fungi. Nova Hedwigia, v. 75, n.3/4, p. 415 – 431, 2002. BERNDT, R.; FREIRE, F.C.O. New species of rust fungi from Brazil. Mycological Progress, v. 3, n. 3, p. 257 – 263, 2004. BERNDT, R.; ROSSEL, A.; FREIRE, F.C.O. New species and reports of rust fungi (Basidiomycota, Uredinales) of South américa. Mycological Progress, v. 6, n. 1, p. 27 – 34, 2007. BERNDT, R.; FREIRE, F.C.O.; PIATEK, M. New species of Phakopsora (Basidiomycota, Uredinales) on Dissotis, Melhania and Merremia from Cameroon, South Africa and Brazil. Sydowia, v. 60, p. 15-60, 2008. FREIRE, F.C.O.; COSTA, A.K.F.; VIANA, F.M.P. Introduction of four plant rust fungi in Ceará State (Brazil). In: CONGRESSO BRASILEIRO DE MICOLOGIA, 4., 2004, Ouro Preto. Anais... Ouro Preto: Sociedade Brasileira de Micologia, 2004. p. 55. 62 Essentia, Sobral, vol. 14, n° 2, p. 53-62, dez. 2012/maio 2013