The characterization of Apis cerana and Apis mellifera mrjp2 gene in Indonesia and the phylogeny relationship with mrjp family genes
Karakterisasi gen mrjp2 Apis cerana dan Apis mellifera di Indonesia dan hubungan filogeni dengan gen mrjp famili
DOI:
https://doi.org/10.5994/jei.21.1.1Keywords:
evolution, exon-intron organization, honey bee, mrjp gene tree, royal jellyAbstract
The major royal jelly protein 2 (mrjp2) gene is one of the molecular markers that can discriminate between Apis cerana Fabricius and A. mellifera Linnaeus. Due to the lack of mrjp2 gene sequences registered in GenBank for Indonesian A. cerana and A. mellifera, DNA characterization and bioinformatics analysis were needed. This research aimed to characterize the exon-intron organization of mrjp2 genes for both Indonesian bee species and analyze the phylogenetic relationship with other mrjp family genes. DNA samples of Apis cerana and A. mellifera, collected from Bogor, were amplified using MF-MR primer at annealing temperatures of 47 oC and 50 oC, respectively. The length of A. cerana and A. mellifera DNA sequences were 579 and 597 bp, respectively. The DNA sequences of both species were comprised of partial exons 1, introns 1, exons 2, introns 2, and partial exon 3. The number of putative amino acids of A. cerana and A. mellifera mrjp2 genes were 111 and 123, respectively. We confirmed that the partial MRJP2 putative amino acids of both honey bees belong to the MRJP family and contained the peptide signal in the 14 first amino acid sites. Nucleotide variation of the mrjp2 gene in A. cerana was higher than A. mellifera. Phylogenetic tree construction showed that A. cerana and A. mellifera form a monophyletic clade with the A. mellifera mrjp7 gene and another mrjp family gene clustered as reported in a previous study.
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References
Abu-Serie MM, Habashy NH. 2019. Two purified proteins from royal jelly with in vitro dual anti-hepatic damage potency: Major royal jelly protein 2 & its novel isoform X1. International Journal of Biological Macromolecules. 128:782–795. DOI: https://doi.org/10.1016/j.ijbiomac.2019.01.210.
Albert S, Klaudiny J. 2007. MRJP9, an ancient protein of the honeybee MRJP family with non-nutritional function. Journal of Apicultural Research. 46:99–104. DOI: https://doi.org/10.3896/IBRA.1.46.2.06.
Botezan S, Baci GM, Bagameri L, Pașca C, Dezmirean DS. 2023. Current status of the bioactive properties of royal jelly: A comprehensive review with a focus on its anticancer, anti-inflammatory, and antioxidant effects. Molecules. 28:1510. DOI: https://doi.org/10.3390/molecules28031510.
Breathnach R, Benoist C, O’Hare K, Gannon F, Chambon P. 1978. Ovalbumin gene: Evidence for leader sequence in mRNA and DNA sequences at exon- intron boundaries. Proceedings of the National Academy of Sciences. 75:4853-4857. DOI: https://doi.org/10.1073/pnas.75.10.4853.
Buttstedt A, Moritz RF. Erler S. 2013. More than royal food-Major royal jelly protein genes in sexuals and workers of the honeybee Apis mellifera. Frontiers in Zoology. 10:72. DOI: https://doi.org/10.1186/1742-9994-10-72.
Buttstedt A, Moritz RFA, Erler S. 2014. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gen family. Biological Reviews. 89:255–269. DOI: https://doi.org/10.1111/brv.12052.
Claviere JM, Notredame C. 2007. Bioinformatics for Dummies. 2nd Ed. Indiana: Willey Publishing Inc.
Corzo E, Clement H, Corzo G, Peña G, Cid-Uribe JI. 2023. Transcriptomic comparison of the royal jelly proteins coded in the hypopharyngeal glands of Apis mellifera and Geotrigona acapulconis. Research Square Preprint. DOI: https://doi.org/10.21203/rs.3.rs-2948844/v1.
Dobritzsch D, Aumer D, Fuszard M, Erler S, Buttstedt. 2019. The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers’ life. Ecology and Evolution. 9:8771–8782. DOI: https://doi.org/10.1002/ece3.5429.
Drapeau MD, Albert S, Kucharski R, Prusko C, Maleszka R. 2006. Evolution of the yellow/major royal jelly protein family and the emergence of social behavior in honey bees. Genome Research. 16:1385–1394. DOI: https://doi.org/10.1101/gr.5012006.
Elsik CG, Worley KC, Bennett AK, Beye M, Camara F, Childers CP, de Graaf DC, Debyser G, Deng J, Devreese B et al. 2014. Finding the missing honey bee genes: Lessons learned from a genome upgrade. BMC Genomics. 15:86. DOI: https://doi.org/10.1186/1471-2164-15-86.
Fang Y, Feng M, Ma C, Rueppell O, Li J. 2023. Major royal jelly proteins influence the neurobiological regulation of the division of labor among honey bee workers. International Journal of Biological Macromolecules. 15:848–860. DOI: https://doi.org/10.1016/j.ijbiomac.2022.11.150.
Feng M, Fang Y, Ma C, Duan X, Zhang Y, Han B, Hu H, Meng L, Wang F, Li J. 2021. Mechanistic insight into royal protein inhibiting the gram-positive bacteria. Biomolecules. 11:64. DOI: https://doi.org/10.3390/biom11010064.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 41:95–98.
Hayashi T, Takamatsu N, Nakashima T, Arita T. 2011. Immunological characterization of honey proteins and identification of MRJP 1 as an IgE-binding protein. Bioscience, Biotechnology, and Biochemistry. 75:556–560. DOI: https://doi.org/10.1271/bbb.100778.
Helbing S, Lattorff HMG, Mortz RF, Buttstedt A. 2017. Comparative analyses of the major royal jelly protein gene cluster in three Apis species with long amplicon sequencing. DNA Research. 24:279–287. DOI: https://doi.org/10.1093/dnares/dsw064.
Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology. 42:182–192. DOI: https://doi.org/10.1093/sysbio/42.2.182.
Imjongjirak C, Klinbunga S, Sittipraneed S. 2005. Cloning, expression and genomic organization of genes encoding major royal jelly protein 1 and 2 of the honey bee (Apis cerana). BMB Report. 38:49–57. DOI: https://doi.org/10.5483/BMBRep.2005.38.1.049.
Jiang CM, Liu X, Li CX, Qian HC, Chen D, Lai CQ, Shen LR. 2018. Anti-senescence effect & molecular mechanism of the major royal jelly proteins on human embryonic lung fibroblast (HFL-I) cell line. Journal of Zhejiang University SCIENCE B. 19:960–972. DOI: https://doi.org/10.1631/jzus.B1800257.
Jiang W, Ying M, Zhang J, Cui Z, Chen Q, Chen Y, Wang J, Fang F, Shen L. 2021. Quantification of major royal jelly proteins using ultra performance liquid chromatography tandem triple quadrupole mass spectrometry and application in honey authenticity. Journal of Food Composition and Analysis. 97:103801. DOI: https://doi.org/10.1016/j.jfca.2021.103801.
Kim BY. 2021. Antiapoptotic role of major royal jelly protein 8 of honeybee (Apis mellifera) venom. Journal of Asia-Pacific Entomology. 24:666–670. DOI: https://doi.org/10.1016/j.aspen.2021.05.014.
Kim CK, Lee DC, Choi SH. 2017. Detection of Korean native honey and European honey by using duplex polymerase chain reaction and immunochromatographic assay. Korean Journal for Food Science of Animal Resources. 37:599–605. DOI: https://doi.org/10.5851/kosfa.2017.37.4.599.
Kim BY, Lee KS, Jung B, Choi YS, Kim HY, Yoon HJ, Gui Z, Lee J, Jin BR. 2019. Honeybee (Apis cerana) major royal jelly protein 4 exhibits antimicrobial activity. Journal of Asia Pacific Entomology. 22:175-182. DOI: https://doi.org/10.1016/j.aspen.2018.12.020.
Kitamura-Abe S, Itoh H, Washio T, Tsutsumi A, Tomita M. 2004. Characterization of the splice sites in GT-AG and GC-AG introns in higher eukaryotes using full-length cDNAs. Journal of Bioinformatics and Computational Biology. 2:309–331. DOI: https://doi.org/10.1142/S0219720004000570.
Koc Ucak A, Karacaoglu M, Bakır ZB, Kızılkaya K. 2022. Determination of total protein, trans- 10-Hydroxy-2-Decenoic Acid (10-HDA) and major royal jelly proteins in royal jelly produced at different harvest times in queenless and queenright colonies. Harran Tarım ve Gıda Bilimleri Dergisi. 26:109–116. DOI: https://doi.org/10.29050/harranziraat.1016909.
Kumar S, Stecher G, Li M, Knyaz C,Tamura K. 2018. Mega x: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution. 35:1547–1549. DOI: https://doi.org/10.1093/molbev/msy096.
Lee S, Lee KS, Ok M, Kim BY, Jin BR. 2022. Antimicrobial activity of major royal jelly protein 8 and 9 of honeybee (Apis mellifera) venom. Journal of Asia-Pacific Entomology. 25:101964. DOI: https://doi.org/10.1016/j.aspen.2022.101964.
Lin N, Li J, Shao R, Zhang H. 2019. Site-Specific analysis of N-linked glycosylation heterogeneity from royal jelly glycoproteins. Journal of Agricultural and Food Chemistry. 67:9411–9422. DOI: https://doi.org/10.1021/acs.jafc.9b03080.
Mureşan CI, Dezmirean DS, Marc BD, Suharoschi R, Pop OL, Buttstedt A. 2022. Biological properties and activities of major royal jelly proteins and their derived peptides. Journal of Functional Foods. 98:105286. DOI: https://doi.org/10.1016/j.jff.2022.105286.
Nei M, Kumar S. 2000. Molecular Evolution and Phylogenetics. New York: Oxford University Press. DOI: https://doi.org/10.1093/oso/9780195135848.001.0001.
Park C, Zhang J. 2011. Genome-wide evolutionary conservation of N-glycosylation sites. Molecular Biology and Evolution. 28:2351–2357. DOI: https://doi.org/10.1093/molbev/msr055.
Park MJ, Kim BY, Deng Y, Park H, Choi YS, Lee KS, Jin BR. 2020. Antioxidant capacity of major royal jelly proteins of honeybee (Apis mellifera) royal jelly. Journal of Asia-Pacific Entomology. 23:445–448. DOI: https://doi.org/10.1016/j.aspen.2020.03.007.
Park MJ, Kim BY, Park HG, Deng y, Yoon HJ, Choi YS, Jin BR. 2019. Major royal jelly protein 2 acts as an antimicrobial agent and antioxidant in royal jelly. Journal of Asia-Pacific Entomology. 22:684–689. DOI: https://doi.org/10.1016/j.aspen.2019.05.003.
Parpinelli RS, Ruvolo-Takasusuki MC, Toledo VA. 2014. MRJP microsatellite markers in Africanized Apis mellifera colonies selected on the basis of royal jelly production. Genetics and Molecular Research. 13:6724–33. DOI: https://doi.org/10.4238/2014.August.28.16.
Pearson WR. 2013. An introduction to sequence similarity (‘homology”) searching. Current Protocols in Bioinformatics. 42:311–318. DOI: https://doi.org/10.1002/0471250953.bi0301s42.
Peiren N, de Graaf DC, Vanrobaeys F, Danneels EL, Devreese B, Van Beeumen J, Jacobs FJ. 2008. Proteomic analysis of the honey bee worker venom gland focusing on the mechanisms of protection against tissue damage. Toxicon. 52:72–83. DOI: https://doi.org/10.1016/j.toxicon.2008.05.003.
Raffiudin R, Crozier RH. 2007. Phylogenetic analysis of honey bee behavioral evolution. Molecular Phylogenetics and Evolution. 43:543–552. DOI: https://doi.org/10.1016/j.ympev.2006.10.013.
Raffiudin R, Shullia NI, Damayanti, A.U. Wahyudi DT. Febiriani TV, Atmowidi T, JSA, Widjaja MC. 2022. New haplotypes of Apis cerana in Indonesia: Identification from mitochondrial and major royal jelly protein 2 genes. International Journal of Tropical Insect Science. 42:389–401. DOI: https://doi.org/10.1007/s42690-021-00556-x.
Raffiudin R, Shullia NI, Febiriani TV, Nisa NR, Rahmadini J, Purwanto H, Atmowidi T. 2023. Entomological origin detection of honey from Apis mellifera and Apis cerana javana in Indonesia based on the Major Royal Jelly Protein 2 (mrjp2) gene. Journal of Apicultural Research. 62:330–333. DOI: https://doi.org/10.1080/00218839.2021.1989795.
Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular Cloning: A Laboratorium Manual. 2nd Ed. New York: Cold Spring Harbor Laboratory Press.
Schmitzova J, Klaudiny J, Albert S, Schroder W, Schreckengost W, Hanes J, Judova J, Simuth J. 1998. A family of major royal jelly proteins of the honeybee Apis mellifera L. Cellular and Molecular Life Sciences. 54:1020–1030. DOI: https://doi.org/10.1007/s000180050229.
Su S, Albert S, Chen S, Zhong B. 2005. Molecular cloning and analysis of four cDNAs from the heads of Apis cerana cerana nurse honeybees coding for major royal jelly proteins. Apidologie. 35:389–401. DOI: https://doi.org/10.1051/apido:2005026.
The Honeybee Genome Sequencing Consortium. 2006. Insight intosocial insects from the genome of the honeybee Apis mellifera. Nature. 443:931–949. DOI: https://doi.org/10.1038/nature05260.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research. 25:4876–4882. DOI: https://doi.org/10.1093/nar/25.24.4876.
Wallberg A, Bunikis I, Pettersson OV, Mosbech MB, Childers AK, Evans JD, Mikheyev AS, Robetson HM, Robinson GE, Webster MT. 2019. A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds. BMC Genomics. 20:275. DOI: https://doi.org/10.1186/s12864-019-5642-0.
Wang X, Dong J, Qiao J, Zhang G, Zhang H. 2020. Purification and characteristics of individual major royal jelly protein 1–3. Journal of Apicultural Research. 1–12. DOI: https://doi.org/10.1080/00218839.2020.1761071.
Yu F, Mao F, Jianke L. 2009. Royal jelly proteome comparison between A. mellifera and A. cerana cerana. Journal of Proteome Research. 9:2207–2215. DOI: https://doi.org/10.1021/pr900979h.
Zhang YZ, Wang S, Chen YF, Wu YQ, Tian J, Si JJ, Zhang CP, Zheng HQ, Hu FL. 2019. Authentication of Apis cerana and Apis mellifera honey based on major royal jelly protein 2 gene. Molecules. 24:1–10. DOI: https://doi.org/10.3390/molecules24020289.
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