Advertisement

BioControl

pp 1–11 | Cite as

Molecular identification of Botryosphaeria dothidea as a fungal associate of the gall midge Asphondylia prosopidis on mesquite in the United States

  • Ikju ParkEmail author
  • Soum Sanogo
  • Stephen F. Hanson
  • David C. Thompson
Article
  • 34 Downloads

Abstract

The gall midge, Asphondylia prosopidis Cockerell, is considered a potential biological control agent for invasive mesquite (Prosopis species) populations in South Africa. Asphondylia species induce galls on mesquite plants by inserting an egg into a bud, and also carry conidia of specific fungal associates in their mycangia that are transferred into the galls. However, fungal associates have not been characterized in flower bud galls formed by A. prosopidis on mesquite. It is essential to identify the fungal associates in the galls formed on natural populations of mesquite prior to host specificity testing. In this study, we showed that Botryosphaeria dothidea (Moug. ex Fr.) Ces. & De Not. is the fungal associate in the flower bud galls on mesquite induced by A. prosopidis in New Mexico by characterization of the internal transcribed spacer (ITS) region. Further, isolates of B. dothidea in A. prosopidis galls formed on mesquite were genetically identical to isolates of B. dothidea carried by other Asphondylia species, particularly on the confamilial Acacia species in South Africa. Our result suggests that A. prosopidis is safe to utilize as a biological control agent for mesquite, if A. prosopidis shows a narrow host range in the pre-release risk assessment, since B. dothidea appears to be ubiquitous. To our knowledge, this is the first report of the association between Asphondylia species and B. dothidea in the United States. We anticipate that A. prosopidis will associate with indigenous B. dothidea in South Africa.

Keywords

Asphondylia prosopidis Botryosphaeria dothidea Cecidomyiidae Galls Mesquite Prosopis 

Notes

Acknowledgements

We would like to thank colleagues in the department of Entomology, Plant Pathology, and Weed Science at New Mexico State University: Kevin Gardner, Howard Beuhler, Linda Liess, Deana Baucom, Jennifer Randall, Jorge Achata, Frank Solano, and many others. Special thanks to Robin Adair for providing DNA sequences and personal communication. This project was supported by the Weeds Division of ARC-PPRI and by the New Mexico Agricultural Experiment Station.

References

  1. Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Frøslev T, Rosendahl S, Boomsma JJ (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci 99:14887–14892CrossRefGoogle Scholar
  2. Adair RJ, Burgess T, Serdani M, Barber P (2009) Fungal associations in Asphondylia (Diptera: Cecidomyiidae) galls from Australia and South Africa: implications for biological control of invasive acacias. Fungal Ecol 2:121–134CrossRefGoogle Scholar
  3. Axelrod DI (1937) A Pliocene flora from the Mount Eden beds, southern California. Carnegie Inst Wash Publ 476:125–183Google Scholar
  4. Batra LR, Lichtwardt RW (1963) Association of fungi with some insect galls. J Kans Entomol Soc 36:262–278Google Scholar
  5. Bergeron MJ, Leal I, Foord B, Ross G, Davis C, Slippers B, De Groot P, Hamelin RC (2011) Putative origin of clonal lineages of Amylostereum areolatum, the fungal symbiont associated with Sirex noctilio, retrieved from Pinus sylvestris, in eastern Canada. Fungal Biol 115:750–758CrossRefGoogle Scholar
  6. Bernardo U, Nugnes F, Gualtieri L, Nicoletti R, Varricchio P, Sasso R, Viggiani G (2018) A new gall midge species of Asphondylia (Diptera: Cecidomyiidae) inducing flower galls on Clinopodium nepeta (Lamiaceae) from Europe, its phenology, and associated fungi. Environ Entomol 47:609–622CrossRefGoogle Scholar
  7. Bissett J, Borkent A (1988) Ambrosia galls: the significance of fungal nutrition in the evolution of the Cecidomyiidae (Diptera). In: Pirozynski KA, Hawksworth DL (eds) Coevolution of fungi with plants and animals. Academic Press, London, pp 203–205Google Scholar
  8. Burgess TI, Crous CJ, Slippers B, Hantula J, Wingfield MJ (2016) Tree invasions and biosecurity: eco-evolutionary dynamics of hitchhiking fungi. AoB PLANTS 8:plw076CrossRefGoogle Scholar
  9. Carneiro MAA, Branco CSA, Braga CED, Almada ED, Costa MBM, Maia VC, Fernandes GW (2009) Are gall midge species (Diptera, Cecidomyiidae) host-plant specialists? Rev Bras Entomol 53:365–378CrossRefGoogle Scholar
  10. Center TD, Purcell MF, Pratt PD, Rayamajhi MB, Tipping PW, Wright SA, Dray FA Jr (2012) Biological control of Melaleuca quinquenervia: an Everglade invader. BioControl 57:151–165CrossRefGoogle Scholar
  11. Cockerell T (1898) XXXVII.—New North-American insects. Ann Mag Nat Hist 2:321–331CrossRefGoogle Scholar
  12. Coetzer W, Hoffmann JH (1997) Establishment of Neltumius arizonensis (Coleoptera: Bruchidae) on mesquite (Prosopis species: Mimosaceae) in South Africa. Biol Control 10:187–192CrossRefGoogle Scholar
  13. Dean W, Anderson M, Milton S, Anderson T (2002) Avian assemblages in native Acacia and alien Prosopis drainage line woodland in the Kalahari, South Africa. J Arid Environ 51:1–19CrossRefGoogle Scholar
  14. Dorchin N, Joy JB, Hilke LK, Wise MJ, Abrahamson WG (2015) Taxonomy and phylogeny of the Asphondylia species (Diptera: Cecidomyiidae) of North American goldenrods: challenging morphology, complex host associations, and cryptic speciation. Zool J Linn Soc 174:265–304CrossRefGoogle Scholar
  15. Gagné RJ (1989) The plant-feeding gall midges of North America. Cornell University Press, IthacaGoogle Scholar
  16. Gagné RJ (2004) A catalog of the Cecidomyiidae (Diptera) of the world. Mem Entomol Soc Wash 24:1–408Google Scholar
  17. Gagné RJ (2010) Update for a catalog of the Cecidomyiidae (Diptera) of the world. Entomol Soc Wash, WashingtonGoogle Scholar
  18. Gagné RJ, Waring GL (1990) The Asphondylia (Cecidomyiidae, Diptera) of creosote bush (Larrea tridentata) in North America. Proc Entomol Soc Wash 92:649–671Google Scholar
  19. Gagné RJ, Woods WM (1988) Native American plant hosts of Asphondylia websteri (Diptera, Cecidomyiidae). Ann Entomol Soc Am 81:447–448CrossRefGoogle Scholar
  20. Goloboff PA (1999) NONA, version 2.0. Fundación e instituto Miguel Lillo, Tucumán, ArgentinaGoogle Scholar
  21. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  22. Harding GB (1987) The status of Prosopis spp. as a weed. Appl Plant Sci 1:43–48Google Scholar
  23. Harding GB, Bate GC (1991) The occurrence of invasive Prosopis species in the north-western Cape, South Africa. S Afr J Sci 87:188–192Google Scholar
  24. Hawkins BA, Goeden RD, Gagné RJ (1986) Ecology and taxonomy of the Asphondylia spp. (Diptera: Cecidomyiidae) forming galls on Atriplex spp. (Chenopodiaceae) in Southern California. Entomography 4:55–107Google Scholar
  25. Heard TA (2000) Concepts in insect host-plant selection behavior and their application to host specificity testing. In: van Driesche RG, Heard T, McClay A, Reardon R (eds) Proceedings: host specificity testing of exotic arthropod biological control agents: the biological basis for improvement in safety. US Forest Service, Forest Health Technology Enterprise Team, Morgantown, pp 1–10Google Scholar
  26. Heath JJ, Stireman JO (2010) Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea. Entomol Exp Appl 137:36–49CrossRefGoogle Scholar
  27. Impson F, Moran V, Hoffmann J, Olckers T, Hill M (1999) A review of the effectiveness of seed-feeding bruchid beetles in the biological control of mesquite, Prosopis species (Fabaceae), in South Africa. In: Olckers T, Hill MP (Eds). Biological control of weeds in South Africa (1990–1998). African Entomol Mem 1:81–88Google Scholar
  28. Jami F, Slippers B, Wingfield MJ, Loots MT, Gryzenhout M (2015) Temporal and spatial variation of Botryosphaeriaceae associated with Acacia karroo in South Africa. Fungal Ecol 15:51–62CrossRefGoogle Scholar
  29. Janson EM, Peeden ER, Stireman JO, Abbot P (2010) Symbiont-mediated phenotypic variation without co-evolution in an insect-fungus association. J Evol Biol 23:2212–2228CrossRefGoogle Scholar
  30. Klein H (2011) A catalogue of the insects, mites and pathogens that have been used or rejected, or are under consideration, for the biological control of invasive alien plants in South Africa. Afr Entomol 19:515–549CrossRefGoogle Scholar
  31. Kobune S, Kajimura H, Masuya H, Kubono T (2012) Symbiotic fungal flora in leaf galls induced by Illiciomyia yukawai (Diptera: Cecidomyiidae) and in its mycangia. Microb Ecol 63:619–627CrossRefGoogle Scholar
  32. Lebel T, Peele C, Veenstra A (2012) Fungi associated with Asphondylia (Diptera: Cecidomyiidae) galls on Sarcocornia quinqueflora and Tecticornia arbuscula (Chenopodiaceae). Fungal Divers 55:143–154CrossRefGoogle Scholar
  33. Marsberg A, Kemler M, Jami F, Nagel JH, Postma-Smidt A, Naidoo S, Wingfield MJ, Crous PW, Spatafora JW, Hesse CN (2017) Botryosphaeria dothidea: a latent pathogen of global importance to woody plant health. Mol plant pathol 18:477–488CrossRefGoogle Scholar
  34. Meyer J (1987) Plant galls and gall inducers. Gebrüder Bornträger, BerlinGoogle Scholar
  35. Miller JR, Strickler KL (1984) Finding and accepting host plants. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Sinauer Associates, Boston, pp 127–157CrossRefGoogle Scholar
  36. Montgomery ME (2011) Understanding federal regulations as guidelines for classical biological control programs. In: Onken B, Reardon R (eds) Implementation and status of biological control of the hemlock woolly adelgid. US Department of Agriculture, Forest Service Forest Health Technology Enterprise Team, Morgantown, pp 25–40Google Scholar
  37. Moran V, Hoffmann J, Zimmermann H (1993) Objectives, constraints, and tactics in the biological control of mesquite weeds (Prosopis) in South Africa. Biol Control 3:80–83CrossRefGoogle Scholar
  38. Neger FW (1910) Ambrosiapilze III. Weitere beobachtungen an ambrosia gallen. Ber Deut Bot Ges 28:455–482Google Scholar
  39. Nixon KC (2002) WinClada, version 1.00. 08. Published by the author, IthacaGoogle Scholar
  40. Nylander JAA (2004) MrModeltest v2.2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  41. Osorio JA, Crous CJ, De Beer ZW, Wingfield MJ, Roux J (2017) Endophytic Botryosphaeriaceae, including five new species, associated with mangrove trees in South Africa. Fungal Biol 121:361–393CrossRefGoogle Scholar
  42. Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comp Appl Biosci 12:357–358Google Scholar
  43. Painter RH (1935) The biology of some dipterous gall-makers from Texas. J Kansas Entomol Soc 8:81–97Google Scholar
  44. Palvic D, Wingfield MJ, Barber P, Slippers B, Hardy GE, Burgess TI (2008) Seven new species of the Botryosphaeriaceae from baobab and other native trees in Western Australia. Mycologia 100:851–866CrossRefGoogle Scholar
  45. Park I (2010) Asphondylia prosopidis complex (Diptera: Cecidomyiidae) and fungal associates: potential biological control candidates for South African mesquite. Master thesis, New Mexico State UniversityGoogle Scholar
  46. Park I, Thompson D (2018) Unisexual broods of Asphondylia species in new floral bud galls on mesquite in New Mexico. Southwest Entomol 43:585–589CrossRefGoogle Scholar
  47. Park I, Eigenbrode SD, Cook SP, Harmon BL, Hinz HL, Schaffner U, Schwarzländer M (2018) Examining olfactory and visual cues governing host-specificity of a weed biological control candidate species to refine pre-release risk assessment. BioControl 63:377–389CrossRefGoogle Scholar
  48. Philips AJP, Alves A, Correia A, Luque J (2005) Two new species of Botryosphaeria with brown, 1-septate ascospores and Dothiorella anamorphs. Mycologia 97:513–529CrossRefGoogle Scholar
  49. Philips AJP, Oudemans PV, Correia A, Alves A (2006) Characterization and epitypifaction of Botryosphaeria corticis, the cause of blueberry cane canker. Fungal Divers 21:141–155Google Scholar
  50. Phillips AJP, Alves A, Abdollahzadeh J, Slippers B, Wingfield MJ, Groenewald J, Crous PW (2013) The Botryosphaeriaceae: genera and species known from culture. Stud Mycol 76:51–167CrossRefGoogle Scholar
  51. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefGoogle Scholar
  52. Pratt PD, Blackwood S, Wright SA, Purcell M, Rayamajhi MB, Giblin-Davis RM, Scheffer SJ, Tipping PW, Center TD (2013) The release and unsuccessful establishment of the Melaleuca biological control agent Fergusonina turneri and its mutualistic nematode Fergusobia quinquenerviae. BioControl 58:553–561CrossRefGoogle Scholar
  53. Raman A, Suryanarayanan TS (2017) Fungus–plant interaction influences plant-feeding insects. Fungal Ecol 29:123–132CrossRefGoogle Scholar
  54. Rogers C (1973) Bionomics of a gall midge, Asphondylia prosopidis Cockerell, attacking mesquite buds. Cecid Indica 8:131–142Google Scholar
  55. Rohfritsch O (2008) Plants, gall midges, and fungi: a three-component system. Entomol Exp Appl 128:208–216CrossRefGoogle Scholar
  56. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  57. Schachtschneider K, February EC (2013) Impact of Prosopis invasion on a keystone tree species in the Kalahari Desert. Plant Ecol 214:597–605CrossRefGoogle Scholar
  58. Slippers B, Wingfield MJ (2007) Botryosphaeriaceae as endophytes and latent pathogens of woody plants: diversity, ecology and impact. Fungal Biol Rev 21:90–106CrossRefGoogle Scholar
  59. Slippers B, Crous PW, Denman S, Coutinho TA, Wingfield BD, Wingfield MJ (2004) Combined multiple gene genealogies and phenotypic characters differentiate several species previously identified as Botryosphaeria dothidea. Mycologia 96:83–101CrossRefGoogle Scholar
  60. Smith H, Kemp GHJ, Wingfield MJ (1994) Canker and dieback of eucalyptus in South Africa caused by Botryosphaeria dothidea. Plant Pathol 43:1031–1034CrossRefGoogle Scholar
  61. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefGoogle Scholar
  62. Stone GN, Schönrogge K (2003) The adaptive significance of insect gall morphology. Trends Ecol Evol 18:512–522CrossRefGoogle Scholar
  63. Swofford DL (2001) Phylogenetic analysis using parsimony (and other methods) version 4.0b10. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  64. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefGoogle Scholar
  65. Tokuda M (2012) Biology of Asphondyliini (Diptera: Cecidomyiidae). Entomol Sci 15:361–383CrossRefGoogle Scholar
  66. van Niekerk JM, Pedro WC, Groenewald JZ, Paul HF, Francois H (2004) DNA phylogeny, morphology and pathogenicity of Botryosphaeria species on grapevines. Mycologia 96:781–798CrossRefGoogle Scholar
  67. Veenstra-Quah AA, Milne J, Kolesik P (2007) Taxonomy and biology of two new species of gall midge (Diptera: Cecidomyiidae) infesting Sarcocornia quinqueflora (Chenopodiaceae) in Australian salt marshes. Aust J Entomol 46:198–206CrossRefGoogle Scholar
  68. White TJ, Bruns T, Lee S, Taylor J (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, New York, pp 315–322Google Scholar
  69. Williams MAJ (1994) Plant galls: organisms, interactions, populations. Clarendon Press, OxfordGoogle Scholar
  70. Winston R, Schwarzländer M, Hinz HL, Day MD, Cock MJ, Julien M (2014) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. USDA Forest Service, Forest Health Technology Enterprise Team, MorgantownGoogle Scholar
  71. Zachariades C, Hoffmann JH, Roberts AR (2011) Biological control of mesquite (Prosopis species) (Fabaceae) in South Africa. Afr Entomol 19:402–415CrossRefGoogle Scholar
  72. Zimmermann H (1991) Biological control of mesquite, Prosopis spp. (Fabaceae), in South Africa. Agric Ecosyst Environ 37:175–186CrossRefGoogle Scholar
  73. Zimowska B, Viggiani G, Nicoletti R, Furmańczyk A, Becchimanzi A, Kot I (2017) First report of the gall midge Asphondylia serpylli on thyme (Thymus vulgaris), and identification of the associated fungal symbiont. Ann Appl Biol 171:89–94CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2019

Authors and Affiliations

  • Ikju Park
    • 1
    Email author
  • Soum Sanogo
    • 1
  • Stephen F. Hanson
    • 1
  • David C. Thompson
    • 1
  1. 1.Department of Entomology, Plant Pathology and Weed ScienceNew Mexico State UniversityLas CrucesUSA

Personalised recommendations