Effect of mycoviruses on growth, spore germination and pathogenicity of the fungus Fusarium circinatumShort communication

  1. Flores-Pacheco, J. Asdrúbal
  2. Muñoz-Adalia, E. Jordán
  3. Martínez-Álvarez, Pablo
  4. Pando, Valentín
  5. Díez-Casero, Julio J.
  6. Martín-García, Jorge
Revista:
Forest systems

ISSN: 2171-5068

Año de publicación: 2017

Volumen: 26

Número: 3

Tipo: Artículo

DOI: 10.5424/FS/2017263-11060 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

Otras publicaciones en: Forest systems

Objetivos de desarrollo sostenible

Resumen

Aim of the study: To assess the impact on two mycoviruses recently described in F. circinatum mitovirus 1, 2-1 and 2-2 (FcMV1, FcMV2-1 and FcMV2-2) on i) mycelial growth, ii) spore germination and iii) relative necrosis.Material and methods: Fourteen monosporic strains of F. circinatum (one of each pair infected with mycoviruses and the other without them) of the pathogen with and without viruses were selected for the assay. The statistical analysis, were a linear mixed model of analysis of variance considering one between-subjects factor (isolate) and one within-subjects factor with four levels (1=without viruses, 2=only virus FcMV1, 3=only virus FcMV2-2 and 4=both viruses).Main results: Colony growth rates of F. circinatum isolates were significantly reduced in presence of mycoviruses (p=0.002). The spore germination was also reduced in the F. circinatum isolates containing mycovirus as compared to mycovirus-free isolates (p<0.001). No significant differences in lesion lengths caused by F. circinatum were found in relation to the presence/absence of mycovirus (p<0.61).Research highlights: Reduction of the percentage of spore germination in the isolates of F. circinatum with mycovirus infections, as compared to free isolates, provides indications of reduction of metabolic activity and plant physiology are discussed. The lack of significant differences found in the length of the lesions caused by F. circinatum with respect to the presence/absence of mycovirus, indicates that further studies with a larger number of variables are required.  

Información de financiación

The Ministry of Economy and Competitiveness of the Government of Spain (Projects AGL2012-39912 and AGL2015-69370-R); COST Action FP1406 PINESTRENGTH; Academic Mobility program for Inclusive Development in Latin America (AMIDILA)/Erasmus Mundus Action 2 in partnership with Bluefields Indian & Caribbean University (BICU) – Nicaragua (Scholarship to JAFP); Portuguese Foundation for Science and Technology (FCT) supported JMG (Post doc grant - SFRH/BPD/122928/2016).

Financiadores

Referencias bibliográficas

  • Zheng L, Zhang M, Chen Q, Zhu M, Zhou E, 2014. A novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology 456-457: 220-226. https://doi.org/10.1016/j.virol.2014.03.029
  • Alonso R, Bettucci L, 2009. First report of the pitch canker fungus Fusarium circinatum affecting Pinus taeda seedlings in Uruguay. Australas Plant Dis Notes 4: 91-92.
  • Barnard EL, Blakeslee GM, 1987. Pitch canker of southern pines. Plant Pathology Circular No. 302 1987: 1-11. http://library.rawlingsforestry.com/fs/fidl/35/fidl-35.pdf
  • Bodles WJA, Fossdal CG, Woodward S, 2006. Multiplex real-time PCR detection of pathogen colonization in the bark and wood of Picea sitchensis clones differing in resistance to Heterobasidion annosum. Tree Physiol 26: 775-782. https://doi.org/10.1093/treephys/26.6.775
  • BOE, 2006. Real Decreto 637/2006, de 26 de mayo, por el que se establece el programa nacional de erradicación y control del hongo Fusarium circinatum Nirenberg et O'Donnell. Boletín Oficial del Estado, Spain. http://www.boe.es/diario_boe/txt.php?id=BOE-A-2006-10287.
  • BOE, 2010. Real Decreto 65/2010, de 29 de enero, por el que se modifica el Real Decreto 637/2006, de 26 de mayo, por el que se establece el programa nacional de erradicación y control del hongo de las coníferas "Fusarium circinatum" Niremberg et O´Donnell. Boletín Oficial del Estado, Spain. https://www.boe.es/diario_boe/txt.php?id=BOE-A-2010-2695
  • Bottacin AM, Levesque CA, Punja ZK, 1994. Characterization of dsRNA in Chalara elegans and effects on growth and virulence. Phytopathology 84: 303-312. https://doi.org/10.1094/Phyto-84-303
  • Bragança H, Diogo E, Moniz F, Amaro P, 2009. First report of pitch canker on pines caused by Fusarium circinatum in Portugal. Plant Dis 95: 770. https://doi.org/10.1094/PDIS-93-10-1079A
  • Bryner SF, Rigling D, 2011. Temperature-dependent genotype-by-genotype interaction between a pathogenic fungus and its hyperparasitic virus. Am Nat 177: 65-74. https://doi.org/10.1086/657620
  • Carlucci A, Colatruglio L, Frisullo S, 2007. First report of pitch canker caused by Fusarium circinatum on Pinus halepensis and P. pinea in Apulia (Southern Italy). Plant Dis 91: 1683. https://doi.org/10.1094/PDIS-91-12-1683C
  • Carey WA, Oak SW, Enebak SA, 2005. Pitch canker ratings of longleaf pine clones correlate with Fusarium circinatum infestation of seeds and seedling mortality in containers. Forest Pathol 35: 205-212. https://doi.org/10.1111/j.1439-0329.2005.00404.x
  • Castro M, Kramer K, Valdivia, L, Ortiz S, Castillo A, 2003. A double-stranded RNA mycovirus confers hypovirulence-associated traits to Botrytis cinerea. FEMS Microb Lett 228: 87-91. https://doi.org/10.1016/S0378-1097(03)00755-9
  • Cho WD, Shin HD, 2004. List of plant diseases in Korea. The Korean Society of Plant Pathology. 779 pp, Seoul.
  • Correll JC, Gordon TR, McCain AH, Fox JW, Koehler CS, Wood DL, Schultz ME, 1991. Pitch canker disease in California - Pathogenicity, distribution, and canker development on Monterey Pine (Pinus radiata). Plant Dis 75: 676-682. https://doi.org/10.1094/PD-75-0676
  • Coutinho TA, Steenkamp ET, Mongwaketsi K, Wilmot M, Wingfield MJ, 2007. First outbreak of pitch canker in a South African pine plantation. Australas Plant Pathol 36: 256-261. https://doi.org/10.1071/AP07017
  • Dwinell D, 1999. Global distribution of the pitch canker fungus. Current and potential impacts of pitch canker in Radiata Pine. Proc Impact Monterey Workshop, Monterey, CA, USA, pp: 54-57.
  • Dwinell LD, Adams D, Guerra-Santos JJ, Aguirre JRM, 1998. Pitch canker disease of Pinus radiata. VII Int Cong Plant Pathol, 9-16 Aug, pp: 9-16. http://www.bspp.org.uk/icpp98/3.7/30.html
  • EPPO, 2006. First report of Gibberella circinata in France. European and Mediterranean Plant Protection Organization 104: 9.
  • Glazebrook J, 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopath 43: 205-227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
  • Gordon TR, Swett CL, Wingfield MJ, 2015. Management of Fusarium diseases affecting conifers. Crop Prot 73: 28-39. https://doi.org/10.1016/j.cropro.2015.02.018
  • Guerra-Santos JJ, 1998. Pitch canker on Monterey pine in Mexico. In: Current and potential impacts of pitch canker in radiata pine; Devey TR, Matheson ME, Gordon AC (Eds). Proc IMPACT Monterey Workshop, Monterey, CA, USA. 30 Nov-3 Dec, 112: 58-61.
  • Hepting GH, Roth ER, 1953. Host relations and spread of the pine pitch canker disease. Phytopathology 43: 475.
  • Hepting GH, Roth ER, 1946. Pitch canker, a new disease of some southern pines. J Forest 44: 742-744.
  • Hunst PL, Latterell FM, Rossi AE, 1986. Variation in double-stranded RNA from isolates of Pyricularia oryzae. Phytopathology 76: 674-678. https://doi.org/10.1094/Phyto-76-674
  • Hyde R, Pennanen T, Hamberg L, Vainio EJ, Piri T, Hantula J, 2013. Two viruses of Heterobasidion confer beneficial, cryptic or detrimental effects to their hosts in different situations. Fung Ecol 6: 387-396. https://doi.org/10.1016/j.funeco.2013.05.005
  • Ihrmark K, Stenström E, Stenlid J, 2004. Double-stranded RNA transmission through basidiospores of Heterobasidion annosum. Mycol Res 108: 149-153. https://doi.org/10.1017/S0953756203008839
  • Kazmierczak P, Pfeiffer P, Zhang PL, Van-Alfen NK, 1996. Transcriptional repression of specific host genes by the mycovirus Cryphonectria Hypovirus 1. J Virol 1996: 1137-1142.
  • Kobayashi T, Muramoto M, 1989. Pitch canker of Pinus luchuensis, a new disease of Japanese forests. Forest Pests 40: 169-173.
  • Landeras E, García P, Fernández Y, Braña M, Fernández-Alonso O, Méndez-Lodos S, Pérez-Sierra A, 2005. Outbreak of pitch canker caused by Fusarium circinatum on Pinus spp. in Northern Spain. Plant Dis 89: 1015-1015. https://doi.org/10.1094/PD-89-1015A
  • Leslie JF, Summerell BA, 2006. The Fusarium Laboratory Manual Blackwell, 1st ed; Leslie JF &amp; Summerell BA (eds.). Blackwell Publ, Manhattan. https://doi.org/10.1002/9780470278376
  • Martínez-Álvarez P, Alves-Santos FM, Diez JJ, 2012a. In vitro and in vivo interactions between Trichoderma viride and Fusarium circinatum. Silva Fennica 46: 303-316. https://doi.org/10.14214/sf.42
  • Martínez-Álvarez P, Martin-García J, Rodríguez-Ceinos S, Diez JJ, 2012b. Monitoring endophyte populations in pine plantations and native oak forests in Northern Spain. Forest Syst 21: 373-382. https://doi.org/10.5424/fs/2012213-02254
  • Martínez-Álvarez P, Pando V, Diez JJ, 2014a. Alternative species to replace Monterey pine plantations affected by pitch canker caused by Fusarium circinatum in northern Spain. Plant Pathol 63: 1086-1094. https://doi.org/10.1111/ppa.12187
  • Martínez-Álvarez P, Vainio EJ, Botella L, Hantula J, Diez JJ, 2014b. Three mitovirus strains infecting a single isolate of Fusarium circinatum are the first putative members of the family Narnaviridae detected in a fungus of the genus Fusarium. Arch Virol 159: 2153-2155. https://doi.org/10.1007/s00705-014-2012-8
  • Martínez-Álvarez P, Fernández-González RA, Sanz-Ros AV, Pando V, Diez JJ, 2016. Two fungal endophytes reduce the severity of pitch canker disease in Pinus radiata seedlings. Biol Control 94: 1-10. https://doi.org/10.1016/j.biocontrol.2015.11.011
  • Moleleki N, Van Heerden SW, Wingfield MJ, Wingfield BD, Preisig O, 2003. Transfection of Diaporthe perjuncta with Diaporthe RNA virus. Appl Environ Microbiol 69: 3952-3956. https://doi.org/10.1128/AEM.69.7.3952-3956.2003
  • Muñoz-Adalia EJ, Fernández MM, Diez JJ, 2016a. The use of mycoviruses in the control of forest diseases. Biocontrol Sci Technol 26 (5): 577-604. https://doi.org/10.1080/09583157.2015.1135877
  • Muñoz-Adalia EJ, Flores-Pacheco JA, Martínez-Álvarez P, Martín-García J, Fernández M, and Diez JJ, 2016b. Effect of mycoviruses on the virulence of Fusarium circinatum and laccase activity. Physiol Mol Plant Pathol 94: 8-15. https://doi.org/10.1016/j.pmpp.2016.03.002
  • Oßwald W, Fleischmann F, Rigling D, Coelho AC, Cravador A, Diez JJ, Dalio RJ, 2014. Strategies of attack and defence in woody plant-Phytophthora interactions. Forest Pathol 44: 169-190. https://doi.org/10.1111/efp.12096
  • Pérez-Sierra A, Landeras E, León M, Berbegal M, García-Jiménez J, Armengol J, 2007. Characterization of Fusarium circinatum from Pinus spp. in northern Spain. Mycol Res 111: 832-839. https://doi.org/10.1016/j.mycres.2007.05.009
  • Pfenning LH, Da Silva Costa S, Pereira De Melo M, Costa H, Ventura JA, Auer CG, Figueredo A, Santos D, 2014. First report and characterization of Fusarium circinatum, the causal agent of pitch canker in Brazil. Trop Plant Pathol 39: 210-216. https://doi.org/10.1590/S1982-56762014000300004
  • Robin C, Lanz S, Soutrenon A, Rigling D, 2010. Dominance of natual over released biological control agents of the chestnut blight fungus Cryphonectria parasitica in south-eastern France is associated with fitness-related trains. Biol Control 53: 55-61. https://doi.org/10.1016/j.biocontrol.2009.10.013
  • Rodríguez-García C, Medina V, Alonso A, Ayllón M, 2014. Mycoviruses of Botrytis cinerea isolates from different hosts. Ann Appl Biol 164: 46-61. https://doi.org/10.1111/aab.12073
  • Romeralo C, Botella L, Santamaria O, Diez JJ, 2012. Effect of putative mitoviruses on in vitro growth of Gremmeniella abietina isolates under different laboratory conditions. Forest Syst 21: 515-525. https://doi.org/10.5424/fs/2012213-02266
  • Sánchez-Fernández RE, Sánchez-Ortiz B, Sandoval-Espinosa YK, Ulloa-Benítez A, Armendáriz-Guillén B, García-Méndez M, Macías-Rubalcava M, 2013. Hongos endófitos: fuente potencial de metabolitos secundarios bioactivos con utilidad en agricultura y medicina. TIP 16: 132-146. https://doi.org/10.1016/S1405-888X(13)72084-9
  • Steenkamp ET, Rodas CA, Kvas M, Wingfield MJ, 2012. Fusarium circinatum and pitch canker of Pinus in Colombia. Australas Plant Pathol 41: 483-491. https://doi.org/10.1007/s13313-012-0120-z
  • Vainio EJ, Korhonen K, Tuomivirta TT, Hantula J, 2010. A novel putative partitivirus of the saprotrophic fungus Heterobasidion ecrustosum infects pathogenic species of the Heterobasidion annosum complex. Fung Biol 114: 955-965. https://doi.org/10.1016/j.funbio.2010.09.006
  • Vainio EJ, Hyder R, Aday G, Hansen E, Piri T, Doǧmuş-Lehtijärvi T, Lehtijärvi A, 2012. Population structure of a novel putative mycovirus infecting the conifer root-rot fungus Heterobasidion annosum sensu lato. Virology 422: 366-376. https://doi.org/10.1016/j.virol.2011.10.032
  • Vainio EJ, Martínez-Álvarez P, Bezos D, Hantula J, Diez JJ, 2015. Fusarium circinatum isolates from northern Spain are commonly infected by three distinct mitoviruses. Archiv Virol 160: 2093-2098. https://doi.org/10.1007/s00705-015-2462-7
  • Viljoen A, Wingfield MJ, Marasas WFO, 1994. First report of Fusarium subglutinans f. sp. pini on pine-seedlings in South-Africa. Plant Dis 78: 309-312. https://doi.org/10.1094/PD-78-0309
  • Wang L, Jiang J, Wang Y, Hong N, Zhang F, Xu W, Wang G, 2014. Hypovirulence of the phytopathogenic fungus Botryosphaeria dothidea: association with a coinfecting chrysovirus and a partitivirus. J Virol 88: 7517-7527. https://doi.org/10.1128/JVI.00538-14
  • Wingfield MJ, Jacobs A, Coutinho TA, Ahumada R, Wingfield BD, 2002. First report of the pitch canker fungus, Fusarium circinatum, on pines in Chile. New Dis Rep 4. https://doi.org/10.1046/j.1365-3059.2002.00710.x
  • Wingfield MJ, Hammerbacher A, Ganley RJ, Steenkamp ET, Gordon TR, Wingfield BD, Coutinho TA, 2008. Pitch canker caused by Fusarium circinatum - A growing threat to pine plantations and forests worldwide. Australas Plant Pathol 37: 319-334. https://doi.org/10.1071/AP08036
  • Yu L, Sang W, De Wu M, Zhang J, Yang L, Zhou YJ, Chen WD, Li GQ, 2015. Novel hypovirulence-associated RNA mycovirus in the plant-pathogenic fungus Botrytis cinerea: Molecular and biological characterization. Appl Environ Microbiol 81: 2299-2310. https://doi.org/10.1128/AEM.03992-14
  • Zamora P, González Casas A, Dueñas M, San Martin R, Diez JJ, 2017. Factors influencing growth, sporulation and virus transfer in Cryphonectria parasitica isolates from Castilla and León (Spain). Eur J Plant Pathol 148: 65-73. https://doi.org/10.1007/s10658-016-1069-5
  • Zamora P, Martín AB, Rigling D, Diez JJ, 2012. Diversity of Cryphonectria parasitica in western Spain and identification of hypovirus-infected isolates. For Pathol 42: 412-419.
  • Zheng L, Zhang M, Chen Q, Zhu M, Zhou E, 2014. A novel mycovirus closely related to viruses in the genus Alphapartitivirus confers hypovirulence in the phytopathogenic fungus Rhizoctonia solani. Virology 456-457: 220-226. https://doi.org/10.1016/j.virol.2014.03.029