Towards an understanding of the genetic basis behind 1080 (sodium fluoroacetate) tolerance and an investigation of the candidate gene ACO2
Janine E. Deakin A G , Desmond W. Cooper B , Jennifer J. Sinclair B , Catherine A. Herbert C , Marilyn B. Renfree D and Matthew Wakefield E F
+ Author Affiliations
- Author Affiliations
A Divison of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
B School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.
C Faculty of Veterinary Science, The University of Sydney, NSW 2006, Australia.
D Department of Zoology, The University of Melbourne, Melbourne, Vic. 3010, Australia.
E Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research, Parkville, Vic. 3052, Australia.
F Department of Genetics, The University of Melbourne, Melbourne, Vic. 3010, Australia.
G Corresponding author. Email: janine.deakin@anu.edu.au
Australian Journal of Zoology 61(1) 69-77 https://doi.org/10.1071/ZO12108
Submitted: 22 October 2012 Accepted: 3 May 2013 Published: 23 May 2013
Abstract
Sodium fluoroacetate, commonly referred to as 1080, is a pesticide heavily used to control vertebrate pests. The development of tolerance to this poison by target species is a critical concern raised by its intensive use. Tolerance to 1080 is common amongst many native vertebrates in south-west Western Australia and is thought to be the result of a long period of coevolution with plant species that produce 1080 in their seeds and flowers. Among those vertebrate species tolerant to 1080 exposure is a subspecies of the tammar wallaby (Macropus eugenii). Tammars from Western Australia are tolerant while the subspecies present on Kangaroo Island is susceptible to 1080 exposure. The availability of genetic and genomic information, combined with a distinct difference in tolerance to 1080 between subspecies, makes the tammar wallaby an ideal species in which to study the genetic basis behind 1080 resistance. To date, research in this area has focussed on a candidate gene approach. Since 1080 inhibits the action of the mitochondrial aconitase enzyme, the aconitase gene ACO2 was considered a prime candidate for involvement in 1080 tolerance. However, sequencing of the full-length ACO2 transcript failed to identify a sequence variant between the two subspecies that would result in an amino acid change in the active site of the enzyme. Future studies will need to take a genome-wide approach to identify the gene(s) responsible for 1080 tolerance.
References
Alsop, A. E., Miethke, P., Rofe, R., Koina, E., Sankovic, N., Deakin, J. E., Haines, H., Rapkins, R. W., and Marshall Graves, J. A. (2005). Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby). Chromosome Research 13, 627–636.| Characterizing the chromosomes of the Australian model marsupial Macropus eugenii (tammar wallaby).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiu7vK&md5=31dac2aaa004000a1e4567b8c5a86659CAS | 16170627PubMed |
Boyle, C. M. (1960). Case of apparent resistance of Rattus norvegicus Berkenhout to anticoagulant poisons. Nature 188, 517.
| Case of apparent resistance of Rattus norvegicus Berkenhout to anticoagulant poisons.Crossref | GoogleScholarGoogle Scholar |
Cameron, J. M. R. (1977). Poison plants in Western Australia and colonizer problem solving. Journal of the Royal Society of Western Australia 59, 71–77.
Cooper, D. W., and Herbert, C. A. (2001). Genetics, biotechnology and population management of over-abundant mammalian wildlife in Australasia. Reproduction, Fertility and Development 13, 451–458.
| Genetics, biotechnology and population management of over-abundant mammalian wildlife in Australasia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383lvFyktA%3D%3D&md5=281700297b17d562c46f70d1e0a822bcCAS |
Deakin, J. E. (2010). Physical and comparative gene maps in marsupials. In ‘Marsupial Genetics and Genomics’. (Eds J. E. Deakin, P. D. Waters and J. A. M. Graves.) pp. 101–115. (Springer: Dordrecht.)
Deakin, J. E., Siddle, H. V., Cross, J. G., Belov, K., and Graves, J. A. (2007). Class I genes have split from the MHC in the tammar wallaby. Cytogenetic and Genome Research 116, 205–211.
| Class I genes have split from the MHC in the tammar wallaby.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitVCjtLw%3D&md5=ee4bd673aa17124a80dc1faee6b7f784CAS | 17317961PubMed |
Deakin, J. E., Koina, E., Waters, P. D., Doherty, R., Patel, V. S., Delbridge, M. L., Dobson, B., Fong, J., Hu, Y., van den Hurk, C., Pask, A. J., Shaw, G., Smith, C., Thompson, K., Wakefield, M. J., Yu, H., Renfree, M. B., and Graves, J. A. (2008). Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals. Chromosome Research 16, 1159–1175.
| Physical map of two tammar wallaby chromosomes: a strategy for mapping in non-model mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFarsrfP&md5=b8488a55e37c846cd4e129f68f38df71CAS | 18987984PubMed |
Eason, C. T., Shapiro, L., Adams, P., Hix, S., Cunningham, C., MacMorran, D., Statham, M., and Statham, H. (2010). Advancing a humane alternative to sodium fluoroacetate (1080) for wildlife management – welfare and wallaby control. Wildlife Research 37, 497–503.
| Advancing a humane alternative to sodium fluoroacetate (1080) for wildlife management – welfare and wallaby control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVCht73F&md5=159fbda09b4d6ae80cacde5d999a63b1CAS |
Fleming, P., Corbett, L., Harden, R., and Thomson, P. (2001). ‘Managing the Impacts of Dingoes and Other Wild Dogs.’ (Bureau of Rural Sciences: Canberra.)
Gardner, P. R., Nguyen, D. D. H., and White, C. W. (1994). Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs. Proceedings of the National Academy of Sciences of the United States of America 91, 12 248–12 252.
| Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisF2jsL8%3D&md5=6d51de01cc30ebf502fd53b2ac4770aeCAS |
Gillies, C. A., and Pierce, R. J. (1999). Secondary poisoning of mammalian predators during possum and rodent control operations at Trounson Kauri Park, Northland, New Zealand. New Zealand Journal of Ecology 23, 183–192.
Goncharov, N. V., Jenkins, R. O., and Radilov, A. S. (2006). Toxicology of fluoroacetate: a review, with possible directions for therapy research. Journal of Applied Toxicology 26, 148–161.
| Toxicology of fluoroacetate: a review, with possible directions for therapy research.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFerurs%3D&md5=f99df142b0fae50d5734473358cc371aCAS | 16252258PubMed |
Grandemange, A., Lasseur, R., Longin-Sauvageon, C., Benoit, E., and Berny, P. (2010). Distribution of VKORC1 single nucleotide polymorphism in wild Rattus norvegicus in France. Pest Management Science 66, 270–276.
| Distribution of VKORC1 single nucleotide polymorphism in wild Rattus norvegicus in France.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitFaqtr4%3D&md5=b0f60a93f2dd0d6195dbfd141c339582CAS | 19890940PubMed |
Green, W. (Ed.) (2004). ‘The Use of 1080 for Pest Control; A Discussion Document.’ (Animal Health Board and the Department of Conservation: Wellington, NZ.)
Hodroge, A., Longin-Sauvageon, C., Fourel, I., Benoit, E., and Lattard, V. (2011). Biochemical characterization of spontaneous mutants of rat VKORC1 involved in the resistance to antivitamin K anticoagulants. Archives of Biochemistry and Biophysics 515, 14–20.
| Biochemical characterization of spontaneous mutants of rat VKORC1 involved in the resistance to antivitamin K anticoagulants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12rur3F&md5=8d794ca7e02997e530bb4d88e6304570CAS | 21907178PubMed |
Howard, W. E., Marsh, R. E., and Palmateer, S. D. (1973). Selective breeding of rats for resistance to sodium monofluoroacetate. Journal of Applied Ecology 10, 731–736.
| Selective breeding of rats for resistance to sodium monofluoroacetate.Crossref | GoogleScholarGoogle Scholar |
King, D. R., Oliver, A. J., and Mead, R. J. (1978). Adaptation of some Western Australian mammals to food plants containing fluoroacetate. Australian Journal of Zoology 26, 699–712.
| Adaptation of some Western Australian mammals to food plants containing fluoroacetate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhvFynu7g%3D&md5=3c823f7b0c62719af744b61ee477bd90CAS |
Kinnear, J. E., Onus, M. L., and Sumner, N. R. (1998). Fox control and rock-wallaby population dynamics – II. An update. Wildlife Research 25, 81–88.
| Fox control and rock-wallaby population dynamics – II. An update.Crossref | GoogleScholarGoogle Scholar |
Martin, G. R., and Twigg, L. E. (2002). Sensitivity to sodium fluoroacetate (1080) of native animals from north-western Australia. Wildlife Research 29, 75–83.
| Sensitivity to sodium fluoroacetate (1080) of native animals from north-western Australia.Crossref | GoogleScholarGoogle Scholar |
McIlroy, J. C. (1981). The sensitivity of Australian animals to 1080 Poison. 2. Marsupial and eutherian carnivores. Australian Wildlife Research 8, 385–399.
| The sensitivity of Australian animals to 1080 Poison. 2. Marsupial and eutherian carnivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XotFShtg%3D%3D&md5=c8c3dd21746b581e64a1f6b41cf2be35CAS |
McIlroy, J. C. (1982a). The sensitivity of Australian animals to 1080 poison. 3. Marsupial and eutherian herbivores. Australian Wildlife Research 9, 487–503.
| The sensitivity of Australian animals to 1080 poison. 3. Marsupial and eutherian herbivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhtValtL8%3D&md5=2c2d669f42f7f9c473a5a65cf2fedc30CAS |
McIlroy, J. C. (1982b). The sensitivity of Australian animals to 1080 poison. 4. Native and introduced rodents. Australian Wildlife Research 9, 505–517.
| The sensitivity of Australian animals to 1080 poison. 4. Native and introduced rodents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhtValtLw%3D&md5=a1280ab421b1bfd023afff99ecc4013fCAS |
McIlroy, J. C., and Gifford, E. J. (1991). Effects on nontarget animal populations of a rabbit trail-baiting campaign with 1080-Poison. Wildlife Research 18, 315–325.
| Effects on nontarget animal populations of a rabbit trail-baiting campaign with 1080-Poison.Crossref | GoogleScholarGoogle Scholar |
McKenzie, J. A., and Batterham, P. (1994). The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends in Ecology & Evolution 9, 166–169.
| The genetic, molecular and phenotypic consequences of selection for insecticide resistance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFSgtA%3D%3D&md5=aa5116c891c2d6afa76354201bcb91c7CAS |
McKenzie, L. M., Collet, C., and Cooper, D. W. (1993). Use of a subspecies cross for efficient development of a linkage map for a marsupial mammal, the tammar wallaby (Macropus eugenii). Cytogenetics and Cell Genetics 64, 264–267.
| Use of a subspecies cross for efficient development of a linkage map for a marsupial mammal, the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2Fgsl2ktA%3D%3D&md5=eb57babe79b0acb8c688aa5ed4ca7319CAS | 8404052PubMed |
Mead, R. J., Oliver, A. J., King, D. R., and Hubach, P. H. (1985). The co-evolutionary role of fluoroacetate in plant–animal interactions in Australia. Oikos 44, 55–60.
| The co-evolutionary role of fluoroacetate in plant–animal interactions in Australia.Crossref | GoogleScholarGoogle Scholar |
Mirel, D. B., Marder, K., Graziano, J., Freyer, G., Zhao, Q. Q., Mayeux, R., and Wilhelmsen, K. C. (1998). Characterization of the human mitochondrial aconitase gene (ACO2). Gene 213, 205–218.
| Characterization of the human mitochondrial aconitase gene (ACO2).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktlyqtLY%3D&md5=a5f4523b5a83df472499d0764428c0faCAS | 9630632PubMed |
Montague, T. L. (2000). ‘The Brushtail Possum: Biology, Impact and Management of an Introduced Marsupial.’ (Manaaki Whenua Press: Lincoln.)
Morrison, J. F. (1954). The kinetics of the reactions catalyzed by aconitase. The Australian Journal of Experimental Biology and Medical Science 32, 867–876.
| The kinetics of the reactions catalyzed by aconitase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2MXosVKnuw%3D%3D&md5=3327b1faa1d7410c4c000b88dce90f99CAS | 14363060PubMed |
Oliver, A. J., King, D. R., and Mead, R. J. (1977). Evolution of resistance to fluoroacetate intoxication in mammals. Search 8, 130–132.
| 1:CAS:528:DyaE2sXltFaktr8%3D&md5=cde9cfbe9002a586421619a05674338bCAS |
Oliver, A. J., King, D. R., and Mead, R. J. (1979). Fluoroacetate tolerance, a genetic marker in some Australian mammals. Australian Journal of Zoology 27, 363–372.
| Fluoroacetate tolerance, a genetic marker in some Australian mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlsFygtg%3D%3D&md5=90a2cbe22ab27ffb9e0b4f7922c1aa28CAS |
Pallanca, J. E., Denney, R. C., and Rose, G. A. (1989). The automated enzymic assay of D-isocitrate in human urine. Annals of Clinical Biochemistry 26, 78–82.
| 1:CAS:528:DyaL1MXkvFeis78%3D&md5=3f22188fc321e35af1799a2fb80fcebcCAS | 2735751PubMed |
Pelz, H. J., Rost, S., Hunerberg, M., Fregin, A., Heiberg, A. C., Baert, K., MacNicoll, A. D., Prescott, C. V., Walker, A. S., Oldenburg, J., and Muller, C. R. (2005). The genetic basis of resistance to anticoagulants in rodents. Genetics 170, 1839–1847.
| The genetic basis of resistance to anticoagulants in rodents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFeis77L&md5=42d7769aacfbcd8b50a5bacebdcae5bcCAS | 15879509PubMed |
Renfree, M. B., Papenfuss, A. T., Deakin, J. E., Lindsay, J., Heider, T., Belov, K., Rens, W., Waters, P. D., Pharo, E. A., Shaw, G., Wong, E. S., Lefevre, C. M., Nicholas, K. R., Kuroki, Y., Wakefield, M. J., Zenger, K. R., Wang, C., Ferguson-Smith, M., Nicholas, F. W., Hickford, D., Yu, H., Short, K. R., Siddle, H. V., Frankenberg, S. R., Chew, K. Y., Menzies, B. R., Stringer, J. M., Suzuki, S., Hore, T. A., Delbridge, M. L., Mohammadi, A., Schneider, N. Y., Hu, Y., O’Hara, W., Al Nadaf, S., Wu, C., Feng, Z. P., Cocks, B. G., Wang, J., Flicek, P., Searle, S. M., Fairley, S., Beal, K., Herrero, J., Carone, D. M., Suzuki, Y., Sugano, S., Toyoda, A., Sakaki, Y., Kondo, S., Nishida, Y., Tatsumoto, S., Mandiou, I., Hsu, A., McColl, K. A., Lansdell, B., Weinstock, G., Kuczek, E., McGrath, A., Wilson, P., Men, A., Hazar-Rethinam, M., Hall, A., Davis, J., Wood, D., Williams, S., Sundaravadanam, Y., Muzny, D. M., Jhangiani, S. N., Lewis, L. R., Morgan, M. B., Okwuonu, G. O., Ruiz, S. J., Santibanez, J., Nazareth, L., Cree, A., Fowler, G., Kovar, C. L., Dinh, H. H., Joshi, V., Jing, C., Lara, F., Thornton, R., Chen, L., Deng, J., Liu, Y., Shen, J. Y., Song, X. Z., Edson, J., Troon, C., Thomas, D., Stephens, A., Yapa, L., Levchenko, T., Gibbs, R. A., Cooper, D. W., Speed, T. P., Fujiyama, A., Graves, J. A., O’Neill, R. J., Pask, A. J., Forrest, S. M., and Worley, K. C. (2011). Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development. Genome Biology 12, 1–25.
| Genome sequence of an Australian kangaroo, Macropus eugenii, provides insight into the evolution of mammalian reproduction and development.Crossref | GoogleScholarGoogle Scholar |
Rost, S., Fregin, A., Ivaskevicius, V., Conzelmann, E., Hortnagel, K., Pelz, H. J., Lappegard, K., Seifried, E., Scharrer, I., Tuddenham, E. G., Muller, C. R., Strom, T. M., and Oldenburg, J. (2004). Mutations in VKORC1 cause warfarin resistance and multiple coagulation factor deficiency type 2. Nature 427, 537–541.
| Mutations in VKORC1 cause warfarin resistance and multiple coagulation factor deficiency type 2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsFWhtQ%3D%3D&md5=775b3051fb6fcb9cd21ad60d7e5f42a9CAS | 14765194PubMed |
Sambrook, J., Maniatis, T., and Fritsch, E. F. (1989). ‘Molecular Cloning: a Laboratory Manual.’ (Cold Spring Harbor Laboratory: Cold Spring Harbor.)
Saunders, G. R., Gentle, M. N., and Dickman, C. R. (2010). The impacts and management of foxes Vulpes vulpes in Australia. Mammal Review 40, 181–211.
| The impacts and management of foxes Vulpes vulpes in Australia.Crossref | GoogleScholarGoogle Scholar |
Tahori, A. S. (1963). Selection for a fluoroacetate resistant strain of house flies and investigation of its resistance pattern. Journal of Economic Entomology 56, 67–69.
| 1:CAS:528:DyaF3sXmvVaruw%3D%3D&md5=da68028eb257cd505cdebb3e7f94d8f0CAS |
Twigg, L. E., and King, D. R. (1989). Tolerance to sodium fluoroacetate in some Australian birds. Australian Wildlife Research 16, 49–62.
| Tolerance to sodium fluoroacetate in some Australian birds.Crossref | GoogleScholarGoogle Scholar |
Twigg, L. E., and King, D. R. (1991). The impact of fluoroacetate-bearing vegetation on native Australian fauna – a review. Oikos 61, 412–430.
| The impact of fluoroacetate-bearing vegetation on native Australian fauna – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslaktrs%3D&md5=6ec55a070edb61480914b0dc5682763bCAS |
Twigg, L. E., and Mead, R. J. (1990). Comparative metabolism of, and sensitivity to, fluoroacetate in geographically separated populations of Tiliqua rugosa (Gray) (Scincidae). Australian Journal of Zoology 37, 617–626.
| Comparative metabolism of, and sensitivity to, fluoroacetate in geographically separated populations of Tiliqua rugosa (Gray) (Scincidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkvFejt7k%3D&md5=a054c0132dd84b07cde6ff69c5197c21CAS |
Twigg, L. E., Martin, G. R., and Lowe, T. J. (2002). Evidence of pesticide resistance in medium-sized mammalian pests: a case study with 1080 poison and Australian rabbits. Journal of Applied Ecology 39, 549–560.
| Evidence of pesticide resistance in medium-sized mammalian pests: a case study with 1080 poison and Australian rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVCis74%3D&md5=6d993c73472e87b2adf4d4b9eacac450CAS |
Twigg, L. E., Martin, G. R., Eastman, A. F., King, D. R., and Kirkpatrick, W. E. (2003). Sensitivity of some Australian animals to sodium fluoroacetate (1080): additional species and populations, and some ecological considerations. Australian Journal of Zoology 51, 515–531.
| Sensitivity of some Australian animals to sodium fluoroacetate (1080): additional species and populations, and some ecological considerations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslyk&md5=91b26f531ea4a1bb4e52bbd70ca506feCAS |
Twigg, L. E., Lowe, T., and Martin, G. (2005). Sodium fluoroacetate residues and carcass degradation of free-ranging feral pigs poisoned with 1080. Wildlife Research 32, 573–580.
| Sodium fluoroacetate residues and carcass degradation of free-ranging feral pigs poisoned with 1080.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFajtLjP&md5=d6ba595f3181e20c63e6a9eff62e904dCAS |
Wang, C., Deakin, J. E., Rens, W., Zenger, K. R., Belov, K., Marshall Graves, J. A., and Nicholas, F. W. (2011a). A first-generation integrated tammar wallaby map and its use in creating a tammar wallaby first-generation virtual genome map. BMC Genomics 12, 1–12.
| A first-generation integrated tammar wallaby map and its use in creating a tammar wallaby first-generation virtual genome map.Crossref | GoogleScholarGoogle Scholar |
Wang, C., Webley, L., Wei, K. J., Wakefield, M. J., Patel, H. R., Deakin, J. E., Alsop, A., Graves, J. A., Cooper, D. W., Nicholas, F. W., and Zenger, K. R. (2011b). A second-generation anchored genetic linkage map of the tammar wallaby (Macropus eugenii). BMC Genetics 12, 1–16.
| A second-generation anchored genetic linkage map of the tammar wallaby (Macropus eugenii).Crossref | GoogleScholarGoogle Scholar |
Zenger, K. R., McKenzie, L. M., and Cooper, D. W. (2002). The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii). Genetics 162, 321–330.
| 1:CAS:528:DC%2BD38Xotl2gsbk%3D&md5=eedc7bec66484671bd37a50fdc21f2d1CAS | 12242243PubMed |
