Evaluating the possibility of horizontal transfer of small RNAs from Sidr pollen to honey bee and their interaction in the host cell

Document Type : Research Paper

Authors

1 Department of Animal Science, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

2 Associate Professor, Department of Animal Science, Faculty of Agriculture, University of Zanjan, Zanjan, Iran

3 Animal Science Research Institute of Iran, Agricultural Research, Education and Extension Organization (AREEO), Karaj, Iran

Abstract

Objective
The existence of molecular relationship between different organisms through diet-derived plant miRNAs is one of the most challenging debates of the last decade. Considering the mutual relationship between plants and pollinating insects, including honey bee as the most important pollinating insect, the aim of the present study is to investigate the existence of molecular relationship in the interaction between plants and honey bee through plant-derived xenomiRs can be very important and create a new perspective of the beneficial effects of this relationship.
 
Materials and methods
Pollen was collected by pollen trap device from honey bee colonies that were located near Sidr trees. Honey bees were fed under controlled conditions in two groups (fed by Sidr pollen as treatment and fed by sugar syrup as control). Following the feeding experiments, the bees were anesthetized using cold and their midgut tissue was collected and used for RNA extraction. After the Small RNA sequencing of the samples, the identification of pollen miRNAs and their tracking in the bee body was done using different bioinformatics analysis. Finally, the target genes of the detected plant miRNAs in the bee body and the molecular pathway involved by them were determined.
 
Results
The results of bioinformatics analysis indicate the detection of eleven plant miRNAs including miR-148a, miR-26a, miR-21-5p, miR-143, miR-27a,miR-203, let-7g, miR-126, miR-206, miR-30d and miR-199b into the tissue of honey bees fed by Sidr pollen. miRNAs participate in various biological processes through their target genes. In the present study, 99 target genes for the detected plant miRNAs were predicted in honey bee genome. The result of KEGG pathway analysis showed that target genes are significantly involved in 23 different biological pathways.
 
Conclusions
The result of the current study clearly present the role of plant-derived xenomiRs in the regulation of honey bee gene expression. Therefore on one hand, these findings extend our understanding of the molecular interaction between honey bees and flowering plants, and on the other hand, it can be used as a practical road map for breeding studies in order to improve honey production and deal with diseases related to bees, as the most important pollinating insects in the 21st century’s agriculture.

Keywords


بهادر یاسر، محمدآبادی محمدرضا، خضری امین و همکاران (1395) مطالعه تنوع ژنتیکی جمعیتهای زنبور عسل استان کرمان با استفاده از نشانگرهای ISSR. پژوهش‌های تولیدات دامی، 13، 192-186.
طهماسـبی غلامحسین، پورقرایـی حسین ( 1379) بررسـی نقـش زنبورعسـل در گـرده‌افشـانی و افزایـش تولیـد محصـولات کشـاورزی ایـران. مجلـه اقتصـاد کشـاورزی و توسـعه. دوره 8، شـماره 30، صفحـه 131-144.
عرب‌پور رق‌آبادی زهرا، محمدآبادی محمدرضا، خضری امین (1400) الگوی بیانی ژن p32 در بافت‌های ران، دست، راسته و چربی پشت بره کرمانی. مجله بیوتکنولوژی کشاورزی، 13(4)، 183-200.
محمدآبادی محمدرضا، سفلایی محمد (1399). پروفایل بیانی mRNA مختص بافت ژن BMP15 در بز. مجله بیوتکنولوژی کشاورزی 12(3)، 208-191.
 
 
References
Anders S, Huber W (2012) Differential expression of RNA-Seq data at the gene level–the DESeq package. Heidelberg, Germany: EMBL 10, f1000research.
Arabpour Z, Mohammadabadi MR, Khezri A (2021) The expression pattern of p32 gene in femur, humeral muscle, back muscle and back fat tissues of Kermani lambs. Agric Biotechnol J 13 (4), 183-200 (In Persian).
Ashby R, Forêt S, Searle I, Maleszka R (2016) MicroRNAs in honey bee caste determination. Sci Rep 6(1), 1-5.
Bahador Y, Mohammadabadi MR, Khezri A et al. (2016) Study of Genetic Diversity in Honey Bee Populations in Kerman Province using ISSR Markers. Res Anim Prod 7 (13), 186-192 (In Persian).
Behura SK, Whitfield CW (2010) Correlated expression patterns of microRNA genes with age-dependent behavioural changes in honeybee. Insect Mol Biol 19(4), 431-9.
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics Btu 170, 1-7.
Cocucci E, Racchetti G, Meldolesi J (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol 19(2), 43–51.
Du J, Li M, Yuan Z et al. (2016) A decision analysis model for KEGG pathway analysis. BMC Bioinform 17(1), e407.
Enright AJ, John B, Gaul U. et al. (2003) MicroRNA targets in Drosophila. Genome Biol 5, R1 e2003.
Fire A, Xu S, Montgomery MK et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391(6669), e806.
Garbian Y, Maori E, Kalev H et al. (2012) Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces Varroa population. PLoS Pathog 8, e1003035.
Ghag SB, Shekhawat UK, Ganapathi TR (2014) Host‐induced post‐transcriptional hairpin RNA‐mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana. Plant Biotechnol J 12(5), 541-53.
Greenberg JK, Xia J, Zhou X et al. (2012) Behavioral plasticity in honey bees is associated with differences in brain microRNA transcriptome. Genes Brain Behav 11(6), 660-70.
Ibrahim HM, Alkharouf NW, Meyer SL et al. (2011) Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Exp Parasitol 127(1), 90-9.
Ivashuta S, Zhang Y, Wiggins BE et al. (2015) Environmental RNAi in herbivorous insects. RNA 21(5), 840-50.
Jarosch A, Moritz RFA (2011) Systemic RNA-interference in the honeybee Apis mellifera: tissue dependent uptake of fluorescent siRNA after intra-abdominal application observed by laser-scanning microscopy. J Insect Physiol 57, 851-857.
Kertesz M, Iovino N, Unnerstall U et al. (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39, 1278-1284.
Kim K, Kim JH, Kim YH et al. ( 2018) Pathway profiles based on gene-set enrichment analysis in the honey bee Apis mellifera under brood rearing-suppressed conditions. Genomics 110(1), 43-9.
Koch A, Kumar N, Weber L et al. (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. PNAS 110(48), 19324-9.
Li X, Zhang M, Zhang H (2011) RNA interference of four genes in adult Bactrocera dorsalis by feeding their dsRNAs. PloS One 6(3), e17788.
Liu F, Peng W, Li Z et al. (2012) Next‐generation small RNA sequencing for microRNAs profiling in Apis mellifera: comparison between nurses and foragers. Insect Mol Biol 21(3), 297-303.
Liu F, Shi T, Qi L et al. (2019) lncRNA profile of Apis mellifera and its possible role in behavioural transition from nurses to foragers. BMC Genom 20(1), e101.
Liu H, Wang X, Wang HD et al. (2012) Escherichia coli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nat Commun 3(1), e1073.
Liu S, Xia Q, Zhao P et al. (2007) Characterization and expression patterns of let-7 microRNA in the silkworm (Bombyx mori). BMC Dev Biol 7(1), 1-7.
Martin JA, Wang Z (2011) Next-generation transcriptome assembly. Nat Rev Genet 12(10), 671-682.
Masood M, Everett CP, Chan SY, Snow JW (2016) Negligible uptake and transfer of diet-derived pollen microRNAs in adult honey bees. RNA Biol 13(1), 109-118.
Mohammadabadi M, Soflaei M (2020) Tissue-specific mRNA expression profile of BMP15 gene in goat. Agric Biotechnol J 12, 191-208 (In Persian).
Morse RA, Calderone NW (2000) The value of honey bees as pollinators of US crops in 2000. Bee culture 28(3), 1-15.
Nazzi F, Brown SP, Annoscia D et al. (2012) Synergistic parasitepathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. PLoS Pathog 8, e1002735.
Nie H, Liu X, Pan J et al. (2017) Identification of genes related to high royal jelly production in the honey bee (Apis mellifera) using microarray analysis. Genet Mol 40(4), 781-9.
Oliva CA, Montecinos-Oliva C, Inestrosa NC (2018) Wnt signaling in the central nervous system: new insights in health and disease. Prog Mol Biol Transl Sci 153, 81-130.
Ramadan H, Li J (2019) In-Depth Brain Phosphoproteome Study Reveals Neurobiological Underpinnings For Nurse Honeybee Workers (Apis mellifera ligustica). Fayoum J Agric Res Dev 33(1), 589-597.
Rehmsmeier M, Steffen P, Hochsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10, 1507–1517.
Reinhart BJ, Slack FJ, Basson M et al. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403(6772), 901-906.
Rusek A M, Abba M, Eljaszewicz A et al. (2015) MicroRNA modulators of epigenetic regulation, the tumor microenvironment and the immune system in lung cancer. Mol Cancer 14(1), e34.
Safaei SMH, Dadpasand M, Mohammadabadi M et al. (2022) An Origanum majorana Leaf Diet Influences Myogenin Gene Expression, Performance, and Carcass Characteristics in Lambs. Animals 13 (1), e14.
Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27, 863-864.
Sempere LF, Sokol NS, Dubrovsky EB (2003) Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-Complex gene activity. Dev Biol 259(1), 9-18.
Tahmasebi Gh, Porgharaei H (2000) Investigating the role of bee in pollination and increasing the production of agricultural products in Iran. Agric Econ Dev J 8(30), 131-144 (In Persian).
Timmons L, Court DL, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
Vitsios DM, Kentepozidou E, Quintais L et al. (2017) Mirnovo: genome-free prediction of microRNAs from small RNA sequencing data and single-cells using decision forests. Nucleic Acids Res 45(21), e177.
Wang ZZ, Ye XQ, Shi M et al. (2018) Parasitic insect-derived miRNAs modulate host development. Nat Commun 9 (1), 1-9.
Waster NM, Ollerton J (2006) Plant-pollinator interactions: From specialization to generalization. University of Chicago Press. 98(4), 899-900.
Weiberg A, Wang M, Lin FM et al. (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342(6154), 118-23.
Yu N, Christiaens O, Liu J et al. (2012) Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Sci 20, 4-14.
Zhang L, Hou D, Chen X et al. (2012) Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 22(1), 107-126.
Zhou G, Zhou Y, Chen X (2017) New insight into inter-kingdom communication: horizontal transfer of mobile small RNAs. Front Microbiol 8, e768.
Zhou W, Li Y, Wang X et al. (2011) MiR-206-mediated dynamic mechanism of the mammalian circadian clock. BMC Syst Biol 5(1), 1-7.
Zhou Z, Li X, Liu J et al. (2015) Honeysuckle-encoded atypical microRNA2911 directly targets influenza a viruses. Cell Res 25(1), 39.
Zhu K, Liu M, Fu Z et al. (2017) Plant microRNAs in larval food regulate honeybee caste development. Plos Genet 13(8), e1006946.