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Spermosporella irenopsidis sp. nov. and Spermatoloncha maticola, parasitic on black mildew (Irenopsis vincensii) of rubber in Bahia, Brazil

Tacila Ribeiro Santos Edna Dora Martins Newman Luz Harry C. Evans José Luiz Bezerra Sobre os autores

Resumo

Uma nova espécie do gênero Spermosporella e um novo registro de Spermatoloncha maticola são reportados parasitando o Míldio Negro (Irenopsis vincensii) em folhas de Hevea brasiliensis na Bahia, Brasil. Ambas as espécies são descritas e ilustradas, e todas as espécies de Spermosporella são comparadas.

Palavras-chave:
fungos fungícolas; Hevea brasiliensis; Meliolales; taxonomia.

Abstract

A new species of the genus Spermosporella and a new record of Spermatoloncha maticola are reported parasitizing the black mildew (Irenopsis vincensii) on leaves of Hevea brasiliensis the Bahia, Brazil. Both species are described and illustrated and all Spermosporella species are compared.

Key words:
fungicolous fungi; Hevea brasiliensis; Meliolales; taxonomy.

Introduction

In Brazil, commercial rubber Hevea brasiliensis (Willd. ex A.Juss.) Müll. Arg., is attacked by several pathogenic fungi. Among them, Irenopsis vincensii D.B. Pinho & O.L. Pereira causes black mildew disease of rubber. Irenopsis vincensii was reported and well documented by Pinho et al. (2014)Pinho DB, Honorato Junior J, Firmino AL, Hora Junior BT, Mizubuti ESG & Pereira OL (2014) Reappraisal of the black mildews (Meliolales) on Hevea brasiliensis. Tropical Plant Pathology 39: 89-94. in the Brazilian states of Espírito Santo and Pará having as heterotypic synonyms the binomials Meliola heveae Vincens and Irenopsis heveae Hansf.

During a survey of fungi on rubber trees, conducted in August 2016 in Michelin Plantations of Bahia, municipality of Igrapiúna, leaf samples were collected showing colonies of the black mildew (I. vincensii).

In the laboratory, it was found that I. vincensii colonies were parasitized by two fungicolous fungi, corresponding to Spermatoloncha maticola Speg. and a new species of the genus Spermosporella Deighton.

The genus Spermosporella is a known parasite of Meliola Fr. species in Africa, Asia and North America (Deighton 1969Deighton FC (1969) Microfungi IV: some hyperparasitic Hyphomycetes, and a note on Cercosporella uredinophila Sacc. Mycological Papers 118: 1-41.; Deighton & Pirozinsky 1972; Sutton 1973Sutton BC (1973) Hyphomycetes from Manitoba and Saskatchewan, Canada. Mycological Papers 132: 1-143.; Hawksworth 1981Hawkswork DL (1981) A survery of the fungicolous conidial fungi. In: Cole GT & Kendrik B (eds.) Biology of conidial fungi. Vol. I. Academic Press, New York. Pp 171-244.; McKenzie 1992McKenzie EHC (1992) Fungi of the Kermadec Islands. Mycotaxon 45: 149-170.; Hughes 1993Hughes SJ (1993) Meliolina and its excluded species. Mycological Papers 166: 1-255. ; Matsushima & Matsushima 1995Matsushima K & Matsushima T (1995) Fragmenta Mycologica - I. Matsushima. Mycological Memoirs 8: 45-54.; Seifert & Gam 2011Seifert KA & Gams W (2011) The genera of Hyphomycetes - 2011 update. Persoonia 27: 119-129.), but has not yet been recorded on the genus Irenopsis F. Stevens. Four species of the genus Spermosporella are known (Deighton 1969; Deighton & Pirozinsky 1972Deighton FC & Pirozynski KA (1972) Microfungi V. More hyperparasitic Hyphomycetes. Mycological Papers 128: 1-110.; Sutton 1973; Matsushima & Matsushima 1995) which differ morphologically from the species studied.

The monotypic species Spermatoloncha maticola has been reported in association with Meliola clerodendricola Henn. on leaves of IIex paraguariensis A. St.-Hil. (yerba maté) in Argentina (Spegazzini 1908Spegazzini CL (1908) Hongos de layerba mate. Anales del Museo Nacional de Historia Natural de Buenos Aires (Series 3) 17: 111-141.; Hawksworth 1981Hawkswork DL (1981) A survery of the fungicolous conidial fungi. In: Cole GT & Kendrik B (eds.) Biology of conidial fungi. Vol. I. Academic Press, New York. Pp 171-244.) and later it was found in Uganda on Clerodendrun capitatum (Willd.) Schumcch. & Thonn. parasitizing the same species of Meliola (IMI 102852b).

Species of the Meliolales are subject to parasitism by several genera of fungicolous fungi. Phaeostigme Syd. & P. ​​Syd; Eriocercospora Deighton, Ramichloridium Stahel ex de Hoog and Spiropes Cif. have all been reported from Brazil (Batista et al. 1966Batista AC; Bezerra JL, Maia H da S & Garnier R (1966) Alguns hiperparasitas de Meliolaceae e outros Ascomycetes. In: Instituto de Micologia, Universidade do Recife 470 (Atas do Instituto de Micologia). Vol. 3. Universidade Federal de Pernambuco, Recife. Pp 10-30.; Caliman 2015Caliman ME (2015) Aspectos ecológicos e taxonômicos de Prillieuxina winteriana (Asterinaceae) e sua interação com Annona muricata. Dissertação de Mestrado. Universidade Estadual de Santa Cruz, Ilhéus. 60p.). However, there are no references to Spermosporella and Spermatoloncha associated with Meliolales in Brazil.

Here, we describe a new species of the genus Spermosporella and report a new record of Spermatoloncha maticola associated with Irenopsis vincensii on Hevea brasiliensis leaves in Bahia, Brazil.

Materials and Methods

Leaf samples from the rubber tree clone CDC 312, colonized by a black mildew in a clonal garden located in Michelin Plantations of Bahia, Igrapiúna municipality, Bahia, Brazil, were collected in August 2016.

In the Fungal Diversity Laboratory, at the Cocoa Research Center (Cepec), municipality of Ilhéus, Bahia, the material was examined under a stereoscopic microscope (MOTIC SMZ -168). Reproductive and somatic structures of the fungi associated with the black mildew were morphologically characterized and photographed using a LeicaDM500 microscope coupled with a digital camera Sony Cyber-shot DSC-WX30. The measurements of the structures were performed using a calibrated ocular micrometer. For observation of intact mycelia, a modified Callan & Carris (2004)Callan BE & Carris LM (2004) Fungi on living plant substrata, including fruits. In: Mueller GM, Bills GF & Foster MS (eds.) Biodiversity of fungi-inventory and monitoring methods. Elsevier, Amsterdan. Pp 105-126. technique was used, with the cellulose acetate being replaced with fast drying colorless nail enamel (Risqué Technology), and followed by mounting in PVLG (polyvinyl alcohol + lactic acid + glycerol) (Hosagoudar & Kapoor 1985Hosagoudar VB & Kapoor JN (1985) New technique of mounting Meliolaceous fungi. Indian Phytopathology 38: 548-549.). The micrographs were done by camera lucida drawings, copied on drawing paper with India ink and scanned.

For taxonomic identification, keys and descriptions of genera and species of mycoparasitic fungi on Meliolales were consulted in the literature (Deighton 1969Deighton FC (1969) Microfungi IV: some hyperparasitic Hyphomycetes, and a note on Cercosporella uredinophila Sacc. Mycological Papers 118: 1-41.; Deighton & Pirozinsky 1972; Sutton 1973Sutton BC (1973) Hyphomycetes from Manitoba and Saskatchewan, Canada. Mycological Papers 132: 1-143.; McKenzie 1992McKenzie EHC (1992) Fungi of the Kermadec Islands. Mycotaxon 45: 149-170.; Matsushima & Matsushima 1995Matsushima K & Matsushima T (1995) Fragmenta Mycologica - I. Matsushima. Mycological Memoirs 8: 45-54.; Seifert & Gam 2011Seifert KA & Gams W (2011) The genera of Hyphomycetes - 2011 update. Persoonia 27: 119-129.). Samples were deposited in the CEPEC-Fungi Fungarium (Ceplac, Ilhéus-Bahia, Brazil).

Results

Taxonomy

1. Spermosporella irenopsidis J.L. Bezerra, T. R. Santos, E.D. Luz sp. nov. Figs. 1; 2a-b

Figure 1
Spermosporella irenopsidis – a. conidia; b. conidiogenous cells formed in the hyphae; c. conidiogenous cells.

Figure 2
Spermosporella irenopsidis – a. conidiogenous cells formed in the hyphae; b. conidia.

MycoBank 819220

Etymology: Referring to the host fungus Irenopsis.

Diagnosis: Colonies whitish, effuse. Mycelium of repent, hyaline, septate hyphae, 2-2.5 µm diam. Conidiogenous cells intercalary, continuous, 1-celled, ampulliform, 8-20 × 4-8 µm. Conidia hyaline, smooth, fusiform, straight to slightly curved, 3-septate, attenuated at both ends, 24-32 × 2-3 µm.

Whitish colonies, effuse, thin, overgrowing colonies of I. vincensii. Superficial mycelium composed of repent, hyaline, smooth, septate, branched hyphae, 2-2.5 µm in diam. Conidiogenous cells produced by intercalary growth in the hyphae; hyaline, unicellular, simple, smooth, ampulliform, measuring 8-20 × 4-8 µm with an attenuated apical beak where the spores are formed. Scars not observed. Conidia hyaline, smooth, thin-walled, fusiform, straight to slightly bent, 3-septate, not constricted at the septa, 24-32 × 2-3 µm, attenuated at both ends.

Material examined: Igrapiúna, Michelin Plantations of Bahia, on Hevea brasiliensis leaves (clone CDC 312). 29.07.2016, Santos et al. (CEPEC, Holotype 2483).

Spermosporella aggregata Deighton (Tab. 1) is the closest species to S. irenopsidis which is distinguished by having intercalary conidiogenous cells and not rostrate, recurved and constricted conidia.

2. Spermatoloncha maticola Speg., Anal. Mus. Nac. Buenos Aires t. XVII (1908) p. 139 Figs. 3; 4a-c

Figure 3
Spermatoloncha maticola – a. conidia; b. hyphal aggregates and conidiogenous cells; c. hyphae of S. maticola contact hyphae of Irenopsis vincensii.

Figure 4
Spermatoloncha maticola – a,b,c. conidia and hyphal aggregates.

Colonies whitish, thin, overgrowing colonies of I. vincensii. Superficial mycelium composed of repent, hyaline, smooth, septate, branched, hyphae, 3-5 µm diam. Hyphal aggregates pseudo parenchymatous, irregular, 20-40 µm diam. with conidiogenous simple, hyaline, continuous, smooth, subglobose to angular, peripheral cells, 4-6 µm diam. Conidial scars not observed. Conidia hyaline, smooth, thick walled, obclavate, straight to slightly bent, 1-septate, not constricted at the septum, 26-56 × 4-6 µm, attenuated towards the apex.

Material examined: Igrapiúna, Michelin Plantations of Bahia, on Hevea brasiliensis leaves (clone CDC 312). 29.VII.2016, Santos et al. (CEPEC 2484).

The examined material is scarce. The cylindrical conidiophores described by Spegazzini (1908)Spegazzini CL (1908) Hongos de layerba mate. Anales del Museo Nacional de Historia Natural de Buenos Aires (Series 3) 17: 111-141. were not observed. This is the first report of S. maticola in Brazil, and I. vincensii is a new host of S. maticola.

Discussion

Spermosporella is biologically and morphologically very similar to Annellospermosporella P.R. Johnst. The two genera are distinguished by sympodial conidiogenesis in Spermosporella and percurrent-anellidic conidiogenesis in Annellospermosporella. Thus far, no molecular studies have been done with the genera Spermosporella and Spermatoloncha and hence there are no DNA sequences available. Because neither of these genera have been cultured in vitro, DNA extraction depends on processing fungal fragments from fresh specimens. However, during the present study, attempts to extract DNA were unsuccessful.

Acknowledgements

Thanks are due to Comissão Executiva do Plano da Lavoura Cacaueira (Ceplac), Bahia, Brazil, Michelin Plantations of Bahia, Brazil and the Universidade Estadual de Santa Cruz, Bahia, Brazil for research support; to Marília Leniuza Soares Ribeiro for the illustrations; to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support/scholarships to J.L. Bezerra, T.R. Santos and E.D.M.N. Luz; and, finally, to Armínio Santos for help with the literature search.

References

  • Batista AC; Bezerra JL, Maia H da S & Garnier R (1966) Alguns hiperparasitas de Meliolaceae e outros Ascomycetes. In: Instituto de Micologia, Universidade do Recife 470 (Atas do Instituto de Micologia). Vol. 3. Universidade Federal de Pernambuco, Recife. Pp 10-30.
  • Caliman ME (2015) Aspectos ecológicos e taxonômicos de Prillieuxina winteriana (Asterinaceae) e sua interação com Annona muricata Dissertação de Mestrado. Universidade Estadual de Santa Cruz, Ilhéus. 60p.
  • Callan BE & Carris LM (2004) Fungi on living plant substrata, including fruits. In: Mueller GM, Bills GF & Foster MS (eds.) Biodiversity of fungi-inventory and monitoring methods. Elsevier, Amsterdan. Pp 105-126.
  • Deighton FC (1969) Microfungi IV: some hyperparasitic Hyphomycetes, and a note on Cercosporella uredinophila Sacc. Mycological Papers 118: 1-41.
  • Deighton FC & Pirozynski KA (1972) Microfungi V. More hyperparasitic Hyphomycetes. Mycological Papers 128: 1-110.
  • Hawkswork DL (1981) A survery of the fungicolous conidial fungi. In: Cole GT & Kendrik B (eds.) Biology of conidial fungi. Vol. I. Academic Press, New York. Pp 171-244.
  • Hosagoudar VB & Kapoor JN (1985) New technique of mounting Meliolaceous fungi. Indian Phytopathology 38: 548-549.
  • Hughes SJ (1993) Meliolina and its excluded species. Mycological Papers 166: 1-255.
  • Matsushima K & Matsushima T (1995) Fragmenta Mycologica - I. Matsushima. Mycological Memoirs 8: 45-54.
  • McKenzie EHC (1992) Fungi of the Kermadec Islands. Mycotaxon 45: 149-170.
  • Pinho DB, Honorato Junior J, Firmino AL, Hora Junior BT, Mizubuti ESG & Pereira OL (2014) Reappraisal of the black mildews (Meliolales) on Hevea brasiliensis Tropical Plant Pathology 39: 89-94.
  • Seifert KA & Gams W (2011) The genera of Hyphomycetes - 2011 update. Persoonia 27: 119-129.
  • Sutton BC (1973) Hyphomycetes from Manitoba and Saskatchewan, Canada. Mycological Papers 132: 1-143.
  • Spegazzini CL (1908) Hongos de layerba mate. Anales del Museo Nacional de Historia Natural de Buenos Aires (Series 3) 17: 111-141.

Editado por

Editor de área: Dr. Anibal de Carvalho Junior

Datas de Publicação

  • Publicação nesta coleção
    20 Dez 2019
  • Data do Fascículo
    2019

Histórico

  • Recebido
    14 Set 2017
  • Aceito
    17 Abr 2018
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