A highly-simplified and inexpensive MALDI-TOF mass spectrometry sample-preparation method with broad applicability to microorganisms, plants, and insects
Main Article Content
Keywords
Reagent optimisation, Sample preparation, Species discrimination, Subspecies discrimination
Abstract
Matrix-assisted laser-desorption and ionization time-of-flight mass spectrometry prepares proteins intact in the gas phase with predominantly a single positive charge. The times-of-flight of charged proteins along a tube held at high vacuum after acceleration in an electrical field are proportional to the square root of the mass-over-charge ratios for the proteins, thereby allowing a mass spectrum to be generated, which can then be used to characterize or identify a protein-containing sample. Several sample-preparation methods are currently available but not all of these are applicable to some forms of fungal biomass and few of these are well suited to the analysis of plant or insect material. We have therefore developed a simplified method that: lyses cells, selectively solubilizes basic proteins, dissolves matrix to a suitable concentration, generates spectra with good intensity and peak richness, costs no more (and generally less) than current methods, and is not constrained in terms of throughput by the availability of centrifuges. Using this method, and a reagent formulation comprising α-cyano-4-hydroxycinnamic acid matrix close to saturation in 60%–65% (v/v) acetonitrile in water containing 2.5% (v/v) trifluoroacetic acid, we have been able to differentiate between strains for a representative subset of aflatoxin-producing and aflatoxin-non-producing strains of Aspergillus fungi, to differentiate between Indian and Pakistani strains of Himalayan balsam rust, to differentiate between closely-related Crassula spp. and regional biotypes of Crassula helmsii, and to differentiate between rubbervine introduced into Australia and Brazil. We have also analyzed fall armyworm and stem-borer samples stored in 70% (v/v) ethanol and old dried insect specimens.
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References
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[2] Knochenmuss R. Ion formation mechanisms in UV-MALDI. Analyst 2006; 131(9): 966-86 DOI: 101039/b605646f.
[3] Bader O. MALDI-TOF-MS-based species identification and typing approaches in medical mycology. Proteomics 2013; 13: 788–799 DOI: 101002/pmic201200468.
[4] Clark AE, Kaleta EJ, Arora A, Wolk DM. Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry: a fundamental shift in the routine practice of clinical microbiology. Clin Microbiol Rev. 2013 Jul: 26(3): 547–603 DOI: 101128/CMR00072-12.
[5] Adams LL, Salee P, Dionne K, Carroll K, Parrish N. A novel protein extraction method for identification of mycobacteria using MALDI-ToF MS. J Microbiol Methods 2015 Dec; 119: 1-3 DOI: 101016/jmimet201509010.
[6] MALDI Biotyper® Protocol Guide Edition 3 2015 Bruker Daltonik GmbH Bremen Germany
[7] Fraser M, Brown Z, Houldsworth M, Borman AM, Johnson EM. Rapid identification of 6328 isolates of pathogenic yeasts using MALDI-ToF MS and a simplified rapid extraction procedure that is compatible with the Bruker Biotyper platform and database. Medical Mycol. 2016; 54: 80–88 https://doiorg/101093/mmy/myv085.
[8] Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol. 2015 Aug 5; 6: 791 DOI: 103389/fmicb201500791.
[9] Cassagne C, Ranque S, Normand AC, Fourquet P, Thiebault S, Planard C, Hendrickx M, Piarroux R. Mould routine identification in the clinical laboratory by Matrix-Assisted Laser Desorption Ionization Time-Of-Flight Mass Spectrometry. PLoS ONE Published: December 14 2011 https://doiorg/101371/journalpone0028425.
[10] Mehta A, Silva LP. MALDI-TOF MS profiling approach: how much can we get from it? Front Plant Sci. 23 March 2015; https://doiorg/103389/fpls201500184.
[11] Murugaiyan J, Roesler U. MALDI-TOF MS Profiling-Advances in Species Identification of Pests Parasites and Vectors. Front Cell Infect Microbiol. 2017; 7: 184 DOI: 03389/fcimb201700184.
[12] Heathcote JG. Aflatoxins and related toxins. In: Betina V, editor. Mycotoxins: Production Isolation Separation and Purification (Developments in Food Science 8) Elsevier: Amsterdam Netherlands: 1984. pp 89-130.
[13] Rodrigues P, Santos C, Venancio A, Lima N. Species identification of Aspergillus section Flavi isolates from Portuguese almonds using phenotypic including MALDI-TOF ICMS and molecular approaches. J Appl Microbiol. 2011; 111: 877–892.
[14] International Agency for Research on Cancer. Traditional Herbal Medicines Some Mycotoxins Naphthalene and Styrene IARC Monograph on the Evaluation of Carcinogenic Risk of Chemicals to Humans 82 2002.
[15] Cotty PJ, Antilla L,Wakelyn PJ. Competitive exclusion of aflatoxin producers: farmer-driven research and development In: Vincent C Goettel MS Lazarovits G, editors. Biological Control: A Global Perspective CAB International: Oxon UK; 2007. pp 241–253.
[16] Da Silva FC, Chalfoun SM, Batista LR, Santos C, Lima N. Use of a polyphasic approach including MALDI-TOF MS for identification of Aspergillus section Flavi strains isolated from food commodities in Brazil. Ann Microbiol. 2015; 65: 2119-2129.
[17] Li T-Y, Liu B-H, Chen Y-C. Characterization of Aspergillus spores by matrix assisted laser desorption⁄ionization time-of-flight mass spectrometry. Rapid Commun Mass Sp. 2000; 14: 2393–2400.
[18] Tanner RA, Varia S, Eschen R, Wood S, Murphy ST, Gange AC. Impacts of an invasive non-native annual weed Impatiens glandulifera on above- and below-ground invertebrate communities in the United Kingdom. PLoS ONE 2013 8 e67271.
[19] Hulme P, Bremner ET. Assessing the impact of Impatiens glandulifera on riparian habitats: partitioning diversity components following species removal. J Appl Ecol. 2006; 43: 43–50.
[20] Greenwood P, Kuhn NJ. Does the invasive plant Impatiens glandulifera promote soil erosion along the riparian zone? An investigation on a small watercourse in northwest Switzerland. J Soils Sediments 2013; 14 (3): 637-650.
[21] Tanner RA, Pollard KM, Varia S, Evans HC, Ellison CA. First release of a fungal classical biocontrol agent against an invasive alien weed in Europe: biology of the rust Puccinia komarovii var glanduliferae. Plant Pathol. 2015; 64: 1130–1139.
[22] Shaw RH, Ellison CA, Marchante H, Pratt CF, Schaffner U, Sforza RFH, Deltoro V. Weed biological control in the European Union: from serendipity to strategy. Biocontrol 2017; 1-15 https://doiorg/101007/s10526-017-9844-6.
[23] Varia S, Pollard K, Ellison C. Implementing a novel weed management approach for Himalayan balsam: progress on biological control in the UK. Outlooks Pest Management 2016; 27(5): 198–203.
[24] Laundon JR. An Australasian species of Crassula introduced into Britain. Watsonia 1961; 5: 59-63.
[25] Skoracka A, Smith L, Oldfield G, Cristofaro M, Amrine JW. Host-plant specificity and specialization in eriophyoid mites and their importance for the use of eriophyoid mites as biocontrol agents of weeds. Exp Appl Acarol 2010; 51: 93-113.
[26] D’hont B, Denys L, Jambon W, De Wilde R, Adriens T, Packet J, van Valkenburg J. Reproduction of Crassula helmsii by seed in western Europe. Aquatic Invasions 2016; 11.
[27] Ellison CA, Evans HC, Ineson J. The significance of intraspecies pathogenicity in the selection of a rust pathotype for the classical biological control of Mikania micrantha (mile-a-minute weed) in Southeast Asia. In Proceedings of the 11th International Symposium on Biological Control of Weeds Cullen JM, Briese DT, Kriticos DJ, Lonsdale WM, Morin L, Scott JK. CSIRO Entomology: Canberra Australia; 2004. pp 102-107.
[28] Palmer B, Vogler W. Cryptostegia grandifolia (Roxb) R Br – rubber vine. In: Julien M, Cruttwell McFadyen R, Cullen J editors Biological control of weeds in Australia CSIRO: Melbourne; 2012. pp 190-197.
[29] Evans HC, Tomley AJ. Studies on the rust Maravalia cryptostegiae a potential biological control agent of rubber-vine weed Cryptostegia grandiflora (Asclepiadaceae: Periplocoidaea) in Australia III: Host range. Mycopathologia 1994; 126: 93-108.
[30] Evans HC, Tomley AJ. Greenhouse and field evaluations of the rubber vine rust Maravalia cryotostegiae on Madagascan and Australian Asclepiadaceae. In Moran VC & Hoffman JH Proceedings of the 9th International Symposium on Biological Control of Weeds University of Cape Town: South Africa; 1996. pp 165-169.
[31] Marohasy J, Forster PI. A taxonomic revision of Cryptostegia R Br (Asclepiadaceae:Periplocoideae). Australian Syst Bot 1991; 4: 571-577.
[32] Klackenberg J. Revision of the genus Cryptostegia R Br (Apocynaceae Periplocoideae). Adansonia 2001; 23: 205-218.
[33] Tomley AJ, Evans HC. Establishment of and preliminary impact studies on the rust Maravalia cryptostegiae of the invasive alien weed Cryptostegia grandiflora in Queensland. Australia Plant Pathology 2004; 53: 475-484.
[34] Page AR, Lacey KL. Economic impact assessment of Australian weed biological control. CRC for Australian Weed Management 2006 Technical Series # 10 151 pp.
[35] De Souza TAF, Rodriguez-Echeverría S, de Andrade LA, Freitas H. Could biological invasion by Cryptostegia madagascariensis alter the composition of the arbuscular mycorrhizal fungal community in semi-arid Brazil? Acta Bot Bras 2016; 30: 93-101, dxdoiorg/101590/0102-33062015abb0190.
[36] Todd EL, Poole RW. Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western Hemisphere. Ann Entomol Soc Am. 1980; 73: 722–738 doi: 101093/aesa/736722.
[37] Datasheet Spodoptera frugiperda (fall army worm) Invasive Species Compendium http://wwwcabiorg/isc/datasheet/29810 (2016).
[38] Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera Noctuidae) a new alien invasive pest in West and Central Africa. PLoS ONE 2016; 11(10):e0165632 doi: 101371/journalpone0165632.
[39] Day R, Abrahams P, Bateman M, Beale T, Clottey V, Cock M, et al. Fall armyworm: impacts and implications for Africa Outlooks on Pest Management 2017; 28(5): 196-201.
[40] Pashley DP, Johnson SJ, Sparks AN. Genetic population structure of migratory moths: the fall armyworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 1985; 78: 756–762 doi: 101093/aesa/786756.
[41] Cock MJW, Beseh PK, Buddie AG, Cafá G, Crozier J. Molecular methods to detect Spodoptera frugiperda in Ghana and implications for monitoring the spread of invasive species in developing countries. Sci Rep 2017; 7(4103) 10 pp doi:101038/s41598-017-04238-y.
[42] Nagoshi RN, Koffi D, Agboka K, Tounou KA, Banerjee R, Jurat-Fuentes JL, Meagher RL. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS ONE 2017; 12(7): e0181982 https://doiorg/101371/journalpone0181982
[43] Lyal C, Kirk P, Smith D, Smith R. The value of taxonomy to biodiversity and agriculture. Biodiversity 2008; 9(1-2): 8–13.
[44] Cock MJW. Strategic entry points for funding taxonomic support to agriculture in developing countries CABI Working Papers 2011; 3: 32.
[45] Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA. DNA barcoding: how it complements taxonomy molecular genetics and population genetics. Trends Genet 2007; 23: 167-172.
[46] Miller SE, Hausmann A, Hallwachs W, Janzen DH. Advancing taxonomy and bioinventories with DNA barcodes Philos Trans R Soc London Ser B 2016; 371: 20150339.
[47]Shiraiwa K, Cong Q, Grishin NV. A new Heraclides swallowtail (Lepidoptera Papilionidae) from North America is recognized by the pattern on its neck. ZooKeys 2014; 468: 85-135.
[48] Hebert PDN, deWaard JR, Zakharov EV, Prosser SWJ, Sones JE, McKeown JTA, Mantle B, La Salle J. A DNA ‘barcode blitz’: rapid digitization and sequencing of a natural history collection. PLoS ONE 2013; 8(7): e68535 doi:101371/journalpone0068535.
[49] Timmermans MJTN, Viberg C, Martin G, Hopkins K, Vogler AP. Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections. Biol J Linn Soc 2016; 117: 83–95.
[50] Kitching IJ, Cadiou J-M. Hawkmoths of the World; An Annotated and Illustrated Revisionary Checklist (Lepidoptera: Sphingidae) : Cornell University Press: Ithaca USA and London UK; 2000. viii + 227 p
[51] Kitching IJ. Sphingidae Taxonomic Inventory 2017 Available at http://sphingidaemyspeciesinfo/
[2] Knochenmuss R. Ion formation mechanisms in UV-MALDI. Analyst 2006; 131(9): 966-86 DOI: 101039/b605646f.
[3] Bader O. MALDI-TOF-MS-based species identification and typing approaches in medical mycology. Proteomics 2013; 13: 788–799 DOI: 101002/pmic201200468.
[4] Clark AE, Kaleta EJ, Arora A, Wolk DM. Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry: a fundamental shift in the routine practice of clinical microbiology. Clin Microbiol Rev. 2013 Jul: 26(3): 547–603 DOI: 101128/CMR00072-12.
[5] Adams LL, Salee P, Dionne K, Carroll K, Parrish N. A novel protein extraction method for identification of mycobacteria using MALDI-ToF MS. J Microbiol Methods 2015 Dec; 119: 1-3 DOI: 101016/jmimet201509010.
[6] MALDI Biotyper® Protocol Guide Edition 3 2015 Bruker Daltonik GmbH Bremen Germany
[7] Fraser M, Brown Z, Houldsworth M, Borman AM, Johnson EM. Rapid identification of 6328 isolates of pathogenic yeasts using MALDI-ToF MS and a simplified rapid extraction procedure that is compatible with the Bruker Biotyper platform and database. Medical Mycol. 2016; 54: 80–88 https://doiorg/101093/mmy/myv085.
[8] Singhal N, Kumar M, Kanaujia PK, Virdi JS. MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis. Front Microbiol. 2015 Aug 5; 6: 791 DOI: 103389/fmicb201500791.
[9] Cassagne C, Ranque S, Normand AC, Fourquet P, Thiebault S, Planard C, Hendrickx M, Piarroux R. Mould routine identification in the clinical laboratory by Matrix-Assisted Laser Desorption Ionization Time-Of-Flight Mass Spectrometry. PLoS ONE Published: December 14 2011 https://doiorg/101371/journalpone0028425.
[10] Mehta A, Silva LP. MALDI-TOF MS profiling approach: how much can we get from it? Front Plant Sci. 23 March 2015; https://doiorg/103389/fpls201500184.
[11] Murugaiyan J, Roesler U. MALDI-TOF MS Profiling-Advances in Species Identification of Pests Parasites and Vectors. Front Cell Infect Microbiol. 2017; 7: 184 DOI: 03389/fcimb201700184.
[12] Heathcote JG. Aflatoxins and related toxins. In: Betina V, editor. Mycotoxins: Production Isolation Separation and Purification (Developments in Food Science 8) Elsevier: Amsterdam Netherlands: 1984. pp 89-130.
[13] Rodrigues P, Santos C, Venancio A, Lima N. Species identification of Aspergillus section Flavi isolates from Portuguese almonds using phenotypic including MALDI-TOF ICMS and molecular approaches. J Appl Microbiol. 2011; 111: 877–892.
[14] International Agency for Research on Cancer. Traditional Herbal Medicines Some Mycotoxins Naphthalene and Styrene IARC Monograph on the Evaluation of Carcinogenic Risk of Chemicals to Humans 82 2002.
[15] Cotty PJ, Antilla L,Wakelyn PJ. Competitive exclusion of aflatoxin producers: farmer-driven research and development In: Vincent C Goettel MS Lazarovits G, editors. Biological Control: A Global Perspective CAB International: Oxon UK; 2007. pp 241–253.
[16] Da Silva FC, Chalfoun SM, Batista LR, Santos C, Lima N. Use of a polyphasic approach including MALDI-TOF MS for identification of Aspergillus section Flavi strains isolated from food commodities in Brazil. Ann Microbiol. 2015; 65: 2119-2129.
[17] Li T-Y, Liu B-H, Chen Y-C. Characterization of Aspergillus spores by matrix assisted laser desorption⁄ionization time-of-flight mass spectrometry. Rapid Commun Mass Sp. 2000; 14: 2393–2400.
[18] Tanner RA, Varia S, Eschen R, Wood S, Murphy ST, Gange AC. Impacts of an invasive non-native annual weed Impatiens glandulifera on above- and below-ground invertebrate communities in the United Kingdom. PLoS ONE 2013 8 e67271.
[19] Hulme P, Bremner ET. Assessing the impact of Impatiens glandulifera on riparian habitats: partitioning diversity components following species removal. J Appl Ecol. 2006; 43: 43–50.
[20] Greenwood P, Kuhn NJ. Does the invasive plant Impatiens glandulifera promote soil erosion along the riparian zone? An investigation on a small watercourse in northwest Switzerland. J Soils Sediments 2013; 14 (3): 637-650.
[21] Tanner RA, Pollard KM, Varia S, Evans HC, Ellison CA. First release of a fungal classical biocontrol agent against an invasive alien weed in Europe: biology of the rust Puccinia komarovii var glanduliferae. Plant Pathol. 2015; 64: 1130–1139.
[22] Shaw RH, Ellison CA, Marchante H, Pratt CF, Schaffner U, Sforza RFH, Deltoro V. Weed biological control in the European Union: from serendipity to strategy. Biocontrol 2017; 1-15 https://doiorg/101007/s10526-017-9844-6.
[23] Varia S, Pollard K, Ellison C. Implementing a novel weed management approach for Himalayan balsam: progress on biological control in the UK. Outlooks Pest Management 2016; 27(5): 198–203.
[24] Laundon JR. An Australasian species of Crassula introduced into Britain. Watsonia 1961; 5: 59-63.
[25] Skoracka A, Smith L, Oldfield G, Cristofaro M, Amrine JW. Host-plant specificity and specialization in eriophyoid mites and their importance for the use of eriophyoid mites as biocontrol agents of weeds. Exp Appl Acarol 2010; 51: 93-113.
[26] D’hont B, Denys L, Jambon W, De Wilde R, Adriens T, Packet J, van Valkenburg J. Reproduction of Crassula helmsii by seed in western Europe. Aquatic Invasions 2016; 11.
[27] Ellison CA, Evans HC, Ineson J. The significance of intraspecies pathogenicity in the selection of a rust pathotype for the classical biological control of Mikania micrantha (mile-a-minute weed) in Southeast Asia. In Proceedings of the 11th International Symposium on Biological Control of Weeds Cullen JM, Briese DT, Kriticos DJ, Lonsdale WM, Morin L, Scott JK. CSIRO Entomology: Canberra Australia; 2004. pp 102-107.
[28] Palmer B, Vogler W. Cryptostegia grandifolia (Roxb) R Br – rubber vine. In: Julien M, Cruttwell McFadyen R, Cullen J editors Biological control of weeds in Australia CSIRO: Melbourne; 2012. pp 190-197.
[29] Evans HC, Tomley AJ. Studies on the rust Maravalia cryptostegiae a potential biological control agent of rubber-vine weed Cryptostegia grandiflora (Asclepiadaceae: Periplocoidaea) in Australia III: Host range. Mycopathologia 1994; 126: 93-108.
[30] Evans HC, Tomley AJ. Greenhouse and field evaluations of the rubber vine rust Maravalia cryotostegiae on Madagascan and Australian Asclepiadaceae. In Moran VC & Hoffman JH Proceedings of the 9th International Symposium on Biological Control of Weeds University of Cape Town: South Africa; 1996. pp 165-169.
[31] Marohasy J, Forster PI. A taxonomic revision of Cryptostegia R Br (Asclepiadaceae:Periplocoideae). Australian Syst Bot 1991; 4: 571-577.
[32] Klackenberg J. Revision of the genus Cryptostegia R Br (Apocynaceae Periplocoideae). Adansonia 2001; 23: 205-218.
[33] Tomley AJ, Evans HC. Establishment of and preliminary impact studies on the rust Maravalia cryptostegiae of the invasive alien weed Cryptostegia grandiflora in Queensland. Australia Plant Pathology 2004; 53: 475-484.
[34] Page AR, Lacey KL. Economic impact assessment of Australian weed biological control. CRC for Australian Weed Management 2006 Technical Series # 10 151 pp.
[35] De Souza TAF, Rodriguez-Echeverría S, de Andrade LA, Freitas H. Could biological invasion by Cryptostegia madagascariensis alter the composition of the arbuscular mycorrhizal fungal community in semi-arid Brazil? Acta Bot Bras 2016; 30: 93-101, dxdoiorg/101590/0102-33062015abb0190.
[36] Todd EL, Poole RW. Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the Western Hemisphere. Ann Entomol Soc Am. 1980; 73: 722–738 doi: 101093/aesa/736722.
[37] Datasheet Spodoptera frugiperda (fall army worm) Invasive Species Compendium http://wwwcabiorg/isc/datasheet/29810 (2016).
[38] Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M. First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera Noctuidae) a new alien invasive pest in West and Central Africa. PLoS ONE 2016; 11(10):e0165632 doi: 101371/journalpone0165632.
[39] Day R, Abrahams P, Bateman M, Beale T, Clottey V, Cock M, et al. Fall armyworm: impacts and implications for Africa Outlooks on Pest Management 2017; 28(5): 196-201.
[40] Pashley DP, Johnson SJ, Sparks AN. Genetic population structure of migratory moths: the fall armyworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 1985; 78: 756–762 doi: 101093/aesa/786756.
[41] Cock MJW, Beseh PK, Buddie AG, Cafá G, Crozier J. Molecular methods to detect Spodoptera frugiperda in Ghana and implications for monitoring the spread of invasive species in developing countries. Sci Rep 2017; 7(4103) 10 pp doi:101038/s41598-017-04238-y.
[42] Nagoshi RN, Koffi D, Agboka K, Tounou KA, Banerjee R, Jurat-Fuentes JL, Meagher RL. Comparative molecular analyses of invasive fall armyworm in Togo reveal strong similarities to populations from the eastern United States and the Greater Antilles. PLoS ONE 2017; 12(7): e0181982 https://doiorg/101371/journalpone0181982
[43] Lyal C, Kirk P, Smith D, Smith R. The value of taxonomy to biodiversity and agriculture. Biodiversity 2008; 9(1-2): 8–13.
[44] Cock MJW. Strategic entry points for funding taxonomic support to agriculture in developing countries CABI Working Papers 2011; 3: 32.
[45] Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA. DNA barcoding: how it complements taxonomy molecular genetics and population genetics. Trends Genet 2007; 23: 167-172.
[46] Miller SE, Hausmann A, Hallwachs W, Janzen DH. Advancing taxonomy and bioinventories with DNA barcodes Philos Trans R Soc London Ser B 2016; 371: 20150339.
[47]Shiraiwa K, Cong Q, Grishin NV. A new Heraclides swallowtail (Lepidoptera Papilionidae) from North America is recognized by the pattern on its neck. ZooKeys 2014; 468: 85-135.
[48] Hebert PDN, deWaard JR, Zakharov EV, Prosser SWJ, Sones JE, McKeown JTA, Mantle B, La Salle J. A DNA ‘barcode blitz’: rapid digitization and sequencing of a natural history collection. PLoS ONE 2013; 8(7): e68535 doi:101371/journalpone0068535.
[49] Timmermans MJTN, Viberg C, Martin G, Hopkins K, Vogler AP. Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections. Biol J Linn Soc 2016; 117: 83–95.
[50] Kitching IJ, Cadiou J-M. Hawkmoths of the World; An Annotated and Illustrated Revisionary Checklist (Lepidoptera: Sphingidae) : Cornell University Press: Ithaca USA and London UK; 2000. viii + 227 p
[51] Kitching IJ. Sphingidae Taxonomic Inventory 2017 Available at http://sphingidaemyspeciesinfo/
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Nov 22, 2018
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Reeve MA, Buddie AG, Pollard KM, Varia S, Seier MK, Offord LC, Cock MJ. A highly-simplified and inexpensive MALDI-TOF mass spectrometry sample-preparation method with broad applicability to microorganisms, plants, and insects. J Biol Methods [Internet]. 2018 Nov. 22 [cited 2024 Apr. 20];5(4):e103. Available from: https://jbmethods.org/index.php/jbm/article/view/261
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Author Biography
Michael A. Reeve, CABI
Innovations Manager, CABI
