Development of single nucleotide polymorphism markers specific to Apis mellifera (Hymenoptera: Apidae) line displaying high hygienic behavior against Varroa destructor, an ectoparasitic mite

다국어 초록 (Multilingual Abstract)

To control Varroa destructor, an ectoparasitic mite, a honey bee line possessing high hygienic behavior (HHB) against this mite has been bred in South Korea. However, a method that can diagnose and assess the HHB line from control (the low hygienic behavior, LHB) line has not been reported yet. Thus, the objective of this study was to develop single nucleotide polymorphism (SNP) markers through whole-genome sequencing of worker bees from HHB line of A. mellifera caucasica and LHB line of A. m. carnica (Hymenoptera: Apidae). A total of 319,445,977 sequence reads were mapped to the known A. mellifera reference genome (average coverage of 87.46%). In 2,316,128 and 3,266,756 SNPs from HHB and LHB line, respectively, 20 SNPs that showed homozygosity in each line were selected and eight SNPs were used to diagnose the HHB line either by typical PCR-restriction fragment length polymorphism or allele-specific PCR. Six of remaining SNPs were of different sizes, enabling relatively easy differentiation of these two honey bee lines on typical agarose gel. Another remaining six SNPs had different sequences, including SNP sites. These SNP markers can be used to diagnose and assess V. destructor-specific HHB line of honey bees.

참고문헌 (Reference)

1 Francis L. W. Ratnieks, "Worker policing in the honeybee" Springer Science and Business Media LLC 342 (342): 796-797, 1989

2 Choi, J. W., "Whole-genome resequencing analyses of five pig breeds, including Korean wild and native, and three European origin breeds" 22 : 259-267, 2015

3 최정우, "Whole-Genome Resequencing Analysis of Hanwoo and Yanbian Cattle to Identify Genome-Wide SNPs and Signatures of Selection" 한국분자세포생물학회 38 (38): 466-473, 2015

4 Palmer, M., "WatCut : An on-Line Tool for Restriction Analysis, Silent Mutation Scanning, and SNP-RFLP Analysis" University of Waterloo 2007

5 Aronstein, K, "Validation of genetic markers associated with chalkbrood resistance" 11 : 47-53, 2015

6 Daisuke Funabara, "Twitchin as a regulator of catch contraction in molluscan smooth muscle" Springer Science and Business Media LLC 26 (26): 455-460, 2006

7 Bolger, A. M., "Trimmomatic : a flexible trimmer for Illumina sequence data" 30 : 2114-2120, 2014

8 Li, H., "The sequence alignment/map format and SAMtools" 25 : 2078-2079, 2009

9 Gianluigi Bigio, "The effect of one generation of controlled mating on the expression of hygienic behaviour in honey bees" Informa UK Limited 53 (53): 563-568, 2015

10 A. McKenna, "The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data" Cold Spring Harbor Laboratory 20 (20): 1297-1303, 2010

11 Erwin L. van Dijk, "Ten years of next-generation sequencing technology" Elsevier BV 30 (30): 418-426, 2014

12 PETER R. OXLEY, "Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera)" Wiley 19 (19): 1452-1461, 2010

13 Gaudet, M., "Single Nucleotide Polymorphisms. Methods in Molecular Biology™" Humana Press 415-424, 2009

14 Keryn L. Lapidge, "Seven suggestive quantitative trait loci influence hygienic behavior of honey bees" Springer Science and Business Media LLC 89 (89): 565-568, 2002

15 Marla Spivak, "Resistance to American foulbrood disease by honey bee colonies Apis mellifera bred for hygienic behavior" Springer Science and Business Media LLC 32 (32): 555-565, 2001

16 T. Nishizawa, "Rapid Detection of Point Mutations Conferring Resistance to Fluoroquinolone in gyrA of Helicobacter pylori by Allele-Specific PCR" American Society for Microbiology 45 (45): 303-305, 2007

17 Ignazio Floris, "Persistence and Effectiveness of Pyrethroids in Plastic Strips Against Varroa jacobsoni (Acari: Varroidae) and Mite Resistance in a Mediterranean Area" Oxford University Press (OUP) 94 (94): 806-810, 2001

18 Swofford, D. L., "PAUP*. Phylogenetic analysis using parsimony (*and other methods)"

19 Jorge S Reis-Filho, "Next-generation sequencing" Springer Science and Business Media LLC 11 (11): 2009

20 Nizar Haddad, "Next generation sequencing of Apis mellifera syriaca identifies genes for Varroa resistance and beneficial bee keeping traits" Wiley 23 (23): 579-590, 2016

21 Alexandre S. Cristino, "Neuroligin-associated microRNA-932 targets actin and regulates memory in the honeybee" Springer Science and Business Media LLC 5 (5): 1-11, 2014

22 N.D. BEUZEN, "Molecular markers and their use in animal breeding" Elsevier BV 160 (160): 42-52, 2000

23 김혜경, "Microsatellite markers developed by next-generation sequencing differentiate inbred lines of Apis mellifera" 한국응용곤충학회 18 (18): 801-805, 2015

24 Hazel C. Levy, "Line identification of Spodoptera frugiperda (Lepidoptera: Noctuidae) insects and cell line: PCR-RFLP of cytochrome oxidase C subunit I gene" Florida Entomological Society 85 (85): 186-190, 2002

25 Lodesani, M., "Limits of chemotherapy in beekeeping : development of resistance and the problem of residues" 86 : 102-109, 2005

26 Harpur, B. A., "Integrative genomics reveals the genetics and evolution of the honey bee’s social immune system" 11 : 937-948, 2019

27 김혜경, "Hygienic Behavior Test of Six Inbred Lines in Apis mellifera Through Freeze-killed Brood Method" 한국양봉학회 30 (30): 187-190, 2015

28 Peter Neumann, "Honey bee colony losses" Informa UK Limited 49 (49): 1-6, 2015

29 Jennifer M. Tsuruda, "High-Resolution Linkage Analyses to Identify Genes That Influence Varroa Sensitive Hygiene Behavior in Honey Bees" Public Library of Science (PLoS) 7 (7): e48276-, 2012

30 Marianna Zhukovskaya, "Grooming Behavior as a Mechanism of Insect Disease Defense" MDPI AG 4 (4): 609-630, 2013

31 Anderson Messias Rodrigues, "Genotyping species of the Sporothrix schenckii complex by PCR-RFLP of calmodulin" Elsevier BV 78 (78): 383-387, 2014

32 Spötter, A., "Genome-wide association study of a Varroa-specific defense behavior in honeybees(Apis mellifera)" 107 : 220-227, 2016

33 Beth Holloway, "Fine mapping identifies significantly associating markers for resistance to the honey bee brood fungal disease, Chalkbrood" Informa UK Limited 52 (52): 134-140, 2015

34 Spivak, M., "Field assays for hygienic behavior in honey bees(Hymenoptera : Apidae)" 91 : 64-70, 1998

35 Andrews, S., "FastQC: A Quality Control Tool for High Throughput Sequence Data"

36 Fabian Sievers, "Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega" EMBO 7 (7): 539-, 2011

37 Ben Langmead, "Fast gapped-read alignment with Bowtie 2" Springer Science and Business Media LLC 9 (9): 357-359, 2012

38 H.S. Arathi, "Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioral repertoire of hygienic bees" Wiley 106 (106): 365-379, 2000

39 Kwok, S., "Effects of primer-template mismatches on the polymerase chain reaction : human immunodeficiency virus type 1 model studies" 18 : 999-1005, 1990

40 A. Ayme-Southgate, "Drosophila has a twitchin/titin-related gene that appears to encode projectin." Proceedings of the National Academy of Sciences 88 (88): 7973-7977, 1991

41 Sébastien Boutin, "Differential gene expression between hygienic and non-hygienic honeybee (Apis mellifera L.) hives" Springer Science and Business Media LLC 16 (16): 2015

42 Haodong Chen, "Development and application of a set of breederfriendly SNP markers for genetic analyses and molecular breeding of rice (Oryza sativa L.)" Springer Science and Business Media LLC 123 (123): 869-879, 2011

43 S. K. Behura, "Correlated expression patterns of microRNA genes with age-dependent behavioural changes in honeybee" Wiley 19 : 431-439, 2010

44 Hideaki Takeuchi, "Blackwell science ltd identification of a novel gene, Mblk-1, that encodes a putative transcription factor expressed preferentially in the large-type Kenyon cells of the honeybee brain" Wiley 10 (10): 487-494, 2001

45 Walter C. Rothenbuhler, "Behaviour genetics of nest cleaning in honey bees. I. Responses of four inbred lines to disease-killed brood" Elsevier BV 12 (12): 578-583, 1964

46 Jeanette Palmquist Momot, "Behaviour Genetics of Nest Cleaning in Honeybees. VI. Interactions of Age and Genotype of Bees, and Nectar Flow" Informa UK Limited 10 (10): 11-21, 2015

47 Victor C. Thompson, "Behaviour Genetics of Nest Cleaning in Honeybees. III. Effect of Age of Bees of a Resistant Line on Their Response to Disease-Killed Brood" Informa UK Limited 3 (3): 25-30, 2015

48 S. Chandrasekaran, "Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states" Proceedings of the National Academy of Sciences 108 (108): 18020-18025, 2011

49 Jeremy P. Gillespie and, "BIOLOGICAL MEDIATORS OF INSECT IMMUNITY" Annual Reviews 42 (42): 611-643, 1997

50 Beth Holloway, "Association of single nucleotide polymorphisms to resistance to chalkbrood in Apis mellifera" Informa UK Limited 51 (51): 154-163, 2015

51 Devendra H. Shah, "Allele-specific PCR method based on rfbS sequence for distinguishing Salmonella gallinarum from Salmonella pullorum: serotype-specific rfbS sequence polymorphism" Elsevier BV 60 (60): 169-177, 2005

52 Ludmila Alves Sanches Dutra, "Allele-specific PCR assay to genotype SNP rs7903146 in TCF7L2 gene for rapid screening of diabetes susceptibility" FapUNIFESP (SciELO) 52 (52): 1362-1366, 2008

53 Alain Vignal, "A review on SNP and other types of molecular markers and their use in animal genetics" Springer Science and Business Media LLC 34 (34): 2002

54 Pablo Cingolani, "A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff" Informa UK Limited 6 (6): 80-92, 2014

55 Eliana Drenkard, "A Simple Procedure for the Analysis of Single Nucleotide Polymorphisms Facilitates Map-Based Cloning in Arabidopsis" American Society of Plant Biologists (ASPB) 124 (124): 1483-1492, 2000