Microbial Control of Leptopharsa heveae Drake & Poor (Hemiptera: Tingidae) in Brazilian Rubber Tree Plantations: a Brief Historical Account and Identification of Entomopathogenic Fungi by Means of Multigene Phylogeny.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Springer Country of Publication: Netherlands NLM ID: 101189728 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1678-8052 (Electronic) Linking ISSN: 1519566X NLM ISO Abbreviation: Neotrop Entomol Subsets: MEDLINE
    • Publication Information:
      Publication: 2012- : Dordrecht : Springer
      Original Publication: Londrina, PR : Entomological Society of Brazil, 2001-
    • Subject Terms:
    • Abstract:
      Over the last decades, a few fungal species have been mentioned in the literature associated with the rubber tree lace bug, Leptopharsa heveae Drake & Poor (Hemiptera: Tingidae). The rubber plantation area treated with these biocontrol agents has been steady since the 1990s, estimated in 10,000-15,000 ha per year. A few large-scale rubber operations, one biocontrol company, and three government-owned laboratories were, and currently one still is, involved in their commercialization. One species, currently referred to as Sporothrix insectorum, has been historically deployed in biocontrol applications in Brazilian rubber farms. However, L. heveae-infecting isolates have only been identified through morphological examinations; therefore, proper molecular assessments are needed for accurate identifications. Hence, DNA of six L. heveae-infecting isolates (five of which have been deployed in field applications) were extracted and sequenced. Multigene phylogeny found that both Simplicillium lanosoniveum and Cordyceps (formerly Isaria) sp. have been sprayed on rubber plantations to manage L. heveae populations, although the former is the only one currently applied. Simplicillium lanosoniveum and Cordyceps sp. have no relation whatsoever to true Sporothrix species associated with human and animal diseases. Therefore, our molecular data may encourage biocontrol companies to register mycoinsecticides targeting L. heveae. We also added unpublished historical accounts after contacting key contributors to the launching of this not so well-known biocontrol program in the 1980s.
    • References:
      Almeida JM, Batista Filho A (2006) Microrganismos no controle de pragas. In: Pinto AS, Nava DE, Rossi MM, Malerbo-Souza DT (eds) Controle Biológico de Pragas: na Prática. CP 2, Piracicaba (SP), pp 35–44.
      Alves SB (1998) Fungos entomopatogênicos. In: Alves SB (ed) Controle Microbiano de Insetos, 2ª edn. FEALQ, Piracicaba, pp 289–381.
      Alves RT, da Silva EAF, de Sousa KM, Oliveira MAS, Pereira AV, Pereira EBC, Junqueira NTV, Icuma IM (2003) Controle biológico do percevejo-de-renda da seringueira com o uso de micoinseticida formulado em óleo emulsionável. Boletim de Pesquisa e Desenvolvimento n° 113. EMBRAPA, Planaltina (DF), p 23.
      Campanhola C, Bettiol W (2003) Métodos alternativos de controle fitossanitário. Embrapa Meio Ambiente, Jaguariúna, p 279.
      Castrillo LA, Wheeler MM (2017) ARSEF Database. http://ARSEF.fpsnl.cornell.edu/4DACTION/W_List_Tables/param . Accessed 10 Feb 2020.
      Celestino Filho P, Magalhães FEL (1986) Ocorrência do fungo Sporothrix insectorum Hoog & Evans, parasitando a mosca-de-renda (Leptopharsa heveae Drake & Poor) em seringal de cultivo. Pesquisa em Andamento n° 42. EMBRAPA-CNPSD, Manaus, p 2.
      Charles VK (1937) A fungus on lace bug. Mycologia 29:216–221.
      Chen W-H, Liu C, Y-Feng H, Liang J-D, Liang Z-Q (2018) Akanthomyces araneogenum, a new Isaria-like araneogenous species. Phytotaxa 379:66–072.
      Chiriví-Salomón JS, Danies G, Restrepo S, Sanjuan T (2015) Lecanicillium sabanense sp. nov. (Cordycipitaceae) a new fungal entomopathogen of coccids. Phytotaxa 234:63–74.
      Costa EDS (2015) Tendências e ciclos climáticos em Ouro Branco do Sul (Fazenda Michelin-MT) no período de 1980 a 2011. MSc Dissertation. Universidade Federal do Mato Grosso, Rondonópolis, p 226.
      De Beer ZW, Duong TA, Wingfield MJ (2016) The divorce of Sporothrix and Ophiostoma: solution to a problematic relationship. Stud Mycol 83:165–191. (PMID: 276168025007658)
      de Camargo AP, Marin FR, Camargo MBP (2003) Zoneamento climático da heveicultura no Brasil. Embrapa Monitoramento por Satélite, Campinas, p 19.
      de Hoog GS (1974) The genera Blastobotrys, Sporothrix, Calcarisporium and Calcarisporiella gen. Nov. Stud Mycol 7:1–84.
      Dias LP, Araújo CAS, Pupin B, Ferreira PC, Braga GUL, Rangel DEN (2018) The Xenon Test Chamber Q-SUN® for testing realistic tolerances of fungi exposed to simulated full spectrum solar radiation. Fungal Biol 122:592–601. (PMID: 29801804)
      Dong QL, Lin TY, Xing XY, Chen B, Han Y (2013) Identification of a symbiotic fungus from blue–green alga and its extracellular polysaccharide. Lett Appl Microbiol 58:303–310. (PMID: 24261819)
      Drake CJ, Poor ME (1935) An underscribed rubber tingitid from Brazil (Hemiptera). J Wash Acad Sci 25:283–284.
      Gasparotto L (2003) Doenças da seringueira nas áreas tradicionais de cultivo e de escape da Amazônia. In: Frazão DAC, Cruz E d S, Viégas I d JM (eds) . Serinqueira na Amazônia - Situação atual e perspectivas. EMBRAPA, Belém, pp 207–215.
      Gasparotto L, Santos AF d, Pereira JCR, Ferreira FA (1997) Doenças da seringueira no Brasil. EMBRAPA-CPAA, Manaus, p 168.
      Gonçalves PS, Martins ALM, Furtado EL, Samburago R, Ottati EL, Ortolani AA, Junior GG (2002) Desempenho de clones de seringueira da série IAC 300 na região do planalto de São Paulo. Pesqui Agropecu Bras 37:131–138.
      Huang S, Maharachchikumbura SSN, Jeewon R, Bhat J, Phookamsak R, Hyde KD, Al-Sadi AM, Kang J (2018) Lecanicillium subprimulinum (Cordycipitaceae, Hypocreales), a novel species from Baoshan, Yunnan. Phytotaxa 348:99–108.
      Humber RA, Rocha LF, Inglis PW, Kipnis A, Luz C (2013) Morphology and molecular taxonomy of Evlachovaea-like fungi, and the status of this unusual conidial genus. Fungal Biol 117:1–12. (PMID: 23332828)
      Junqueira NTV, Lima MIPM, Martins MAM, Magalhães FEL (1987) Isolamento e cultivo do fungo Sporothrix insectorum Hoog & Evans a ser utilizado para o controle da mosca-de-renda da seringueira. Comunicado Técnico n° 56. EMBRAPA-CNPSD, Manaus, p 4.
      Junqueira NTV, Pinheiro E, Alves RT, Celestino Filho P, Pereira AV, Oliveira MAS, Fialho JF, Gasparotto L (1999) Controle biológico do percevejo-de-renda (Leptopharsa heveae Drake & Poor) em seringais de cultivo. Circular Técnica n° 3. EMBRAPA Cerrados, Planaltina, p 30.
      Kauffman CA (1999) Sporotrichosis. Clin Infect Dis 29:231–237. (PMID: 10476718)
      Kepler RM, Sung GH, Ban S, Nakagiri A, Chen MJ, Huang B, Li Z, Spatafora JW (2012) New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 104:182–197. (PMID: 22067304)
      Kepler RM, Luangsa-ard J, Hywel-Jones NL, Quandt CA, Sung G-H, Rehner SA, Aime AC, Henkel TW, Sanjuan T, Zare R, Chen M, Li Z, Rossman AY, Spatafora JW, Bhushan Shrestha B (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA Fungus 8:335–353. (PMID: 292427795729716)
      Leite LG, Batista Filho A, Oliveira SMC (1998) Infectividade do fungo Sporothrix insectorum, na forma de corpos hifais, contra o percevejo de renda da seringueira. In: Simpósio de controle biológico, 6, Rio de Janeiro. Resumos, pp138.
      Li Z, Alves SB, Roberts DW, Fan M, Delalibera I Jr, Tang J, Lopes RB, Faria M, Rangel DEN (2010) Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi. Biocontrol Sci Techn 20:117–136.
      Lim SY, Lee S, Kong HG, Lee J (2014) Entomopathogenicity of Simplicillium lanosoniveum isolated in Korea. Mycobiology 42:317–321. (PMID: 256060024298834)
      Liu YJ, Whelen S, Hall BD (1999) Phylogeentic relationships among Ascomycetes: evidence from an RNA polymerase II subunit. Mol Biol Evol 16:1799–1808. (PMID: 10605121)
      Luangsa-ard JJ, Hywel-Jones NL, Manoch L, Samson RA (2005) On the relationships of Paecilomyces sect. Isarioidea species. Mycol Res 109:581–589. (PMID: 16018312)
      Maddison WP, Maddison DR (2015) Mesquite: a modular system for evolutionary analysis. Version 3.04. http://mesquiteproject.org.
      Mascarin GM, Lopes RB, Delalibera I Jr, Fernandes EKK, Luz C, Faria M (2019) Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. J Invert Pathol 165:46–53.
      Michereff Filho M, Faria M, Wraight SP, Silva KFAS (2009) Micoinseticidas e micoacaricidas no Brasil: Como estamos após quatro décadas? Arq Inst Biol 76:769–779.
      Mongkolsamrit S, Noisripoom W, Thanakitpipattana D, Wutikhun T, Spatafora JW, Luangsa-ard J (2018) Disentangling cryptic species with isaria-like morphs in Cordycipitaceae. Mycologia 110:230–257. (PMID: 29863995)
      Moreira IPS (1986) Biologia da Leptopharsa heveae (Drake & Poor, 1935) e seus danos nas mudas de Heveae brasiliensis (Müell, 1932). Silvicultura 11:47.
      Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
      Ordonez-Giraldo AIDH (1993) Sporothrix insectorum: Mèthode biologique de contrôle de la punaise Leptopharsa gibbicarina dans les cultures du palmier du palmier à huile en Amèrique Latine (Hemiptera, Tingidae). B Soc Entomol Fr 98:77–85.
      Raeder J, Broda P (1985) Rapid preparation of DNA from filamentous fungi. Lett Appl Microbiol 1:17–20.
      Rangel DEN (2000) Virulência de Aphanocladium album e Verticillium lecanii (Deuteromycotina: Hyphomycetes) para o percevejo-de-renda da seringueira, Leptopharsa hevea (Hemiptera: Tingidae) e comportamento de V. lecanii em meio de cultura, Microbiologia. MSc Dissertation, Universidade Estadual Paulista, Jaboticabal (SP), p 70.
      Rangel DEN, Correia ACB (2003) Virulência de Aphanocladium album (Preuss) Gams e Verticillium lecanii (zimm.) Viégas (Deuteromycotina: Hyphomycetes) para o percevejo-de-renda da seringueira, Leptopharsa heveae (Drake & Poor) (Demiptera: Tingidae). Ciência e Agrotecnologia 27:1636–1642.
      Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98. (PMID: 16389960)
      Rehner SA, Minnis AM, Sung G-H, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. (PMID: 21482632)
      Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Hohna S, Larget B, Liu L, Huelsenbeck JP (2012) MrBayes v.3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. (PMID: 2235772722357727)
      Santos RS, da Silva JM (2013) Dinâmica populacional do parasitoide de ovos Erythmelus tingitiphagus (Hymenoptera: Mymaridae) em clone de seringueira, em Itiquira, MT. Revista Árvore 37:237–244.
      Schoch CL, Robbertse B, Robert V. et al. (2014) Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi. https://doi.org/10.1093/database/bau061.
      Schroeder S, Kim SH, Cheung WT, Sterflinger K, Breuil C (2001) Phylogenetic relationship of Ophiostoma piliferum to other sapstain fungi based on the nuclear rRNA gene. FEMS Microbiol Lett 195:163–167. (PMID: 11179646)
      Shimazu M, Alves RT, Kishino K (1994) Investigation on entomogenous fungi in the Cerrado region and their utilization for microbial control of pests. In: Centro de Pesquisa Agropecuária dos Cerrados (Planaltina, DF). Relatório técnico do projeto nipo-brasileiro de cooperação em pesquisa agrícola nos Cerrados 1987/1992. EMBRAPA, Planaltina, pp 202–214.
      Souza RKF, Azevedo RFF, Lobo AO, Rangel DEN (2014) Conidial water affinity is an important characteristic for thermotolerance in entomopathogenic fungi. Biocontrol Sci Techn 24:448–461.
      Spatafora JW, Sung G-H, Sung JM, Hywel-Jones NL, White JF Jr (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16:1701–1711. (PMID: 17402984)
      Sterling A, Salas-Tobón YM, Virgüez-Díaz Y (2016) Erinnyis ello (Lepidoptera: Sphingidae) y Leptopharsa heveae (Hemiptera: Tingidae) en Hevea brasiliensis en sistema agroforestal. Rev Colomb Entomol 42:124–132.
      Stiller JW, Hall BD (1997) The origin of red algae: implications for plastid evolution. P Natl Acad Sci USA 94:4520–4525.
      Summerbell RC, Gueidan C, Schroers HJ, de Hoog GS, Starink M, Rosete YA, Guarro J, Scott JA (2011) Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium. Stud Mycol 68:139–162. (PMID: 215231923065988)
      Sung G-H, Spatafora JW, Zare R, Hodge KT, Gams W (2001) A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae. Nova Hedwigia 72:311–328.
      Sung G-H, Hywel-Jones NL, Sung JM, Luangsa-Ard JJ, Shrestha B, Spatafora JW (2007) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol 57:5–59. (PMID: 184909932104736)
      Tanzini MR (1996) Resistência de clones de seringueira [Hevea brasiliensis (Willd. Ex. Adr. de jus.) Muell. Arg.] a Leptopharsa heveae Drake & Poor, 1935 (Hemiptera: Tingidae) e sua biologia. MSc Dissertation, Universidade Estadual Paulista, Jaboticabal (SP), p 138.
      Tanzini MR (2002) Controle do percevejo-de-renda-da-seringueira (Leptopharsa heveae) com fungos entomopatogênicos. PhD. Thesis, Universidade de São Paulo (ESALQ), Piracicaba (SP), Brasil, p 140.
      Tanzini MR, Lara FM (1998) Biologia do percevejo-de-renda-da-seringueira Leptopharsa heveae Drake & Poor (Heteroptera: Tingidae). Ecossistema 23:65–67.
      Torres MS, White JF Jr, Bischoff JF (2005) Cordyceps spegazzinii sp. nov., a new species of the C. militaris group. Mycotaxon 94:253–263.
      Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucl Acids Res 44(W1):W232–W235. (PMID: 27084950)
      Val AJ d (1994) Névoa Protetora: os fungos pulverizados nos seringais controlam a mosca-de-renda, uma praga nos cultivos do Mato Grosso. Revista Globo Rural, Rio de Janeiro, Março, pp 43–46.
      Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. (PMID: 2376561213247)
      Vu D, Groenewald M, de Vries M, Gehrmann T, Stielow B, Eberhardt U, Al-Hatmi A, Groenewald JZ, Cardinali G, Houbraken J, Boekhout T, Crous PW, Robert V, Verkley GJM (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Stud Mycol 92:135–154. (PMID: 29955203)
      Ward NA, Schneider RW, Aime MC (2011) Colonization of soybean rust sori by Simplicillium lanosoniveum. Fungal Ecol 4:303–308.
      White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322.
      Zancope-Oliveira RM, Almeida-Paes R, Oliveira MME, Freitas DFS, Gutierrez-Galhardo MC (2012) Outbreaks of sporotrichosis in humans and animals in Brazil. Mycoses 55:33–33.
      Zare R, Gams W (2001) A revision of Verticillium section Prostrata. IV. The genera Lecanicillium and Simplicillium gen. nov. Nova Hedwigia 73:1–50.
      Zare R, Gams W, Culham A (2000) A revision of Verticillium sect. Prostrata. I. Phylogenetic studies using ITS sequences. Nova Hedwigia 71:465–480.
      Zha L-S, Wen T-C, Huang S-K, Boonmee S, Eungwanichayapant PD (2019) Taxonomy and biology of Cordyceps qingchengensis sp. nov. and its allies. Phytotaxa 416:14–24.
      Zhou X, Rodrigues AM, Feng P, de Hoog GS (2014) Global ITS diversity in the Sporothrix schenckii complex. Fungal Divers 66:153–165.
      Zhou Y-M, Zhi J-R, Ye M, Zhang Z-Y, Yue W-B, Zou X (2018) Lecanicillium cauligalbarum sp. nov. (Cordycipitaceae, Hypocreales), a novel fungus isolated from a stemborer in the Yao Ren National Forest Mountain Park, Guizhou. MycoKeys 43:59–74.
      Zimmermann G (2008) The entomopathogenic fungi Isaria farinosa (formerly Paecilomyces farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus): biology, ecology and use in biological control. Biocontrol Sci Tech 18:865–901.
    • Grant Information:
      SEG11.15.02.001.03.06 Empresa Brasileira de Pesquisa Agropecuária
    • Contributed Indexing:
      Keywords: Biocontrol; Cordyceps; Leptopharsa; Simplicillium; Sporothrix; entomopathogenic fungi
    • Accession Number:
      0 (Biological Control Agents)
    • Publication Date:
      Date Created: 20200924 Date Completed: 20210802 Latest Revision: 20210802
    • Publication Date:
      20221213
    • Accession Number:
      10.1007/s13744-020-00808-4
    • Accession Number:
      32970286