Plant microRNAs in larval food regulate honeybee caste development

PLoS Genetics

Volumn 13, Issue 8, 2017, Pages

  Zhu, Kegan ^a   Liu, Minghui ^a   Fu, Zheng ^a   Zhou, Zhen ^a   Kong, Yan ^a   Liang, Hongwei ^a   Lin, Zheguang ^b   Luo, Jun ^a   Zheng, Huoqing ^b   Wan, Ping ^a   Zhang, Junfeng ^a   Zen, Ke ^a   Chen, Jiong ^a   Hu, Fuliang ^b   Zhang, Chen Yu ^a   Ren, Jie ^c   Chen, Xi ^a  

^a NANJING UNIVERSITY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MICRORNA; MICRORNA 162A; PLANT RNA; UNCLASSIFIED DRUG; FATTY ACID; ROYAL JELLY;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY HEIGHT; BODY SIZE; BODY WEIGHT; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FEMALE; FERTILITY; HONEYBEE; INSECT CASTE; INSECT DEVELOPMENT; INSECT LARVA; MALE; NONHUMAN; OVARY; PILOT STUDY; QUEEN (INSECT); WORKER (INSECT); ANIMAL; BEE; DRUG EFFECTS; FOOD; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; SOCIAL HIERARCHY;

ANIMALS; BEES; DROSOPHILA; FATTY ACIDS; FEMALE; FOOD; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIERARCHY, SOCIAL; LARVA; MICRORNAS;

EID: 85028802628     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006946     Document Type: Article

References (64)

1. Michener CD, The social behavior of the bees; a comparative study. Cambridge, Mass.,: Belknap Press of Harvard University Press; 1974. xii, 404 p. p.
2. Snodgrass RE, Anatomy of the honey bee. Ithaca, N.Y.,: Comstock Pub. Associates; 1956. xiv, 334 p. p.
3. Gordon DM, The organization of work in social insect colonies. Nature. 1996;380(6570):121–4. doi: 10.1038/380121a0
4. Haydak MH, Honey Bee Nutrition. Annu Rev Entomol. 1970;15:143–&. doi: 10.1146/annurev.en.15.010170.001043
5. Fo Huber, New observations on the natural history of bees. 3d ed.Edinburgh,: Printed for W. & C. Tait, and Longman, Hurst, Rees, Orme, and Brown, London; 1821. 2 p. l., vii -xv, 440 p. p.
6. Kamakura M, Royalactin induces queen differentiation in honeybees. Nature. 2011;473(7348):478–83. doi: 10.1038/nature10093 21516106.
7. Mao W, Schuler MA, Berenbaum MR, A dietary phytochemical alters caste-associated gene expression in honey bees. Sci Adv. 2015;1(7):e1500795. doi: 10.1126/sciadv.1500795 26601244; PubMed Central PMCID: PMCPMC4643792.
8. Asencot M, Lensky Y, The effect of sugars and juvenile hormone on the differentiation of the female honeybee larvae (Apis mellifera L.) to queens. Life Sci. 1976;18(7):693–9. 1263752.
9. Asencot M, Lensky Y, The effect of soluble sugars in stored royal jelly on the differentiation of female honeybee (Apis mellifera L.) larvae to queens. Insect biochemistry. 1988;18(2):127–33.
10. Spannhoff A, Kim YK, Raynal NJM, Gharibyan V, Su MB, Zhou YY, et al. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO reports. 2011;12(3):238–43. doi: 10.1038/embor.2011.9 21331099
11. Bartel DP, MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–97. 14744438.
12. Zhang L, Hou D, Chen X, Li D, Zhu L, Zhang Y, et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 2012;22(1):107–26. doi: 10.1038/cr.2011.158 21931358; PubMed Central PMCID: PMCPMC3351925.
13. LaMonte G, Philip N, Reardon J, Lacsina JR, Majoros W, Chapman L, et al. Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell host & microbe. 2012;12(2):187–99.
14. Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z, Kaloshian I, et al. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science. 2013;342(6154):118–23. doi: 10.1126/science.1239705 24092744; PubMed Central PMCID: PMCPMC4096153.
15. Zhou Z, Li X, Liu J, Dong L, Chen Q, Liu J, et al. Honeysuckle-encoded atypical microRNA2911 directly targets influenza A viruses. Cell Res. 2015;25(1):39–49. doi: 10.1038/cr.2014.130 25287280; PubMed Central PMCID: PMCPMC4650580.
16. Chin AR, Fong MY, Somlo G, Wu J, Swiderski P, Wu X, et al. Cross-kingdom inhibition of breast cancer growth by plant miR159. Cell Res. 2016;26(2):217–28. doi: 10.1038/cr.2016.13 26794868; PubMed Central PMCID: PMCPMC4746606.
17. Liang G, Zhu Y, Sun B, Shao Y, Jing A, Wang J, et al. Assessing the survival of exogenous plant microRNA in mice. Food Sci Nutr. 2014;2(4):380–8. doi: 10.1002/fsn3.113 25473495; PubMed Central PMCID: PMCPMC4221836.
18. Mlotshwa S, Pruss GJ, MacArthur JL, Endres MW, Davis C, Hofseth LJ, et al. A novel chemopreventive strategy based on therapeutic microRNAs produced in plants. Cell Res. 2015;25(4):521–4. doi: 10.1038/cr.2015.25 25721325; PubMed Central PMCID: PMCPMC4387556.
19. Yang J, Farmer LM, Agyekum AA, Elbaz-Younes I, Hirschi KD, Detection of an Abundant Plant-Based Small RNA in Healthy Consumers. Plos One. 2015;10(9):e0137516. doi: 10.1371/journal.pone.0137516 26335106; PubMed Central PMCID: PMCPMC4559308.
20. Yang J, Farmer LM, Agyekum AA, Hirschi KD, Detection of dietary plant-based small RNAs in animals. Cell Res. 2015;25(4):517–20. doi: 10.1038/cr.2015.26 25721324; PubMed Central PMCID: PMCPMC4387557.
21. Jayachandran B, Hussain M, Asgari S, An insect trypsin-like serine protease as a target of microRNA: utilization of microRNA mimics and inhibitors by oral feeding. Insect Biochem Mol Biol. 2013;43(4):398–406. doi: 10.1016/j.ibmb.2012.10.004 23108205.
22. Patel A, Fondrk MK, Kaftanoglu O, Emore C, Hunt G, Frederick K, et al. The Making of a Queen: TOR Pathway Is a Key Player in Diphenic Caste Development. Plos One. 2007;2(6). ARTN e509 doi: 10.1371/journal.pone.0000509 17551589
23. Li X, Zhang M, Zhang H, RNA interference of four genes in adult Bactrocera dorsalis by feeding their dsRNAs. Plos One. 2011;6(3):e17788. doi: 10.1371/journal.pone.0017788 21445257; PubMed Central PMCID: PMCPMC3060817.
24. Ashby R, Foret S, Searle I, Maleszka R, MicroRNAs in Honey Bee Caste Determination. Sci Rep. 2016;6:18794. doi: 10.1038/srep18794 26739502; PubMed Central PMCID: PMC4704047.
25. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell. 2009;136(3):461–72. doi: 10.1016/j.cell.2008.12.038 19203581; PubMed Central PMCID: PMC2661848.
26. Martínez G, Panda K, Köhler C, Slotkin RK, Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nature Plants. 2016;16030 (2016). doi: 10.1038/nplants.2016.30 27249563
27. Chen X, Li Q, Wang J, Guo X, Jiang X, Ren Z, et al. Identification and characterization of novel amphioxus microRNAs by Solexa sequencing. Genome biology. 2009;10(7):R78. doi: 10.1186/gb-2009-10-7-r78 19615057; PubMed Central PMCID: PMC2728532.
28. Wolschin F, Mutti NS, Amdam GV, Insulin receptor substrate influences female caste development in honeybees. Biol Letters. 2011;7(1):112–5. doi: 10.1098/rsbl.2010.0463 20591854
29. Whitfield CW, Ben-Shahar Y, Brillet C, Leoncini I, Crauser D, Leconte Y, et al. Genomic dissection of behavioral maturation in the honey bee. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(44):16068–75. doi: 10.1073/pnas.0606909103 17065327; PubMed Central PMCID: PMC1622924.
30. Mutti NS, Dolezal AG, Wolschin F, Mutti JS, Gill KS, Amdam GV, IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. The Journal of experimental biology. 2011;214(Pt 23):3977–84. Epub 2011/11/11. doi: 10.1242/jeb.061499 22071189; PubMed Central PMCID: PMC3212421.
31. Wheeler DE, Buck NA, Evans JD, Expression of insulin/insulin-like signalling and TOR pathway genes in honey bee caste determination. Insect Mol Biol. 2014;23(1):113–21. Epub 2013/11/15. doi: 10.1111/imb.12065 24224645.
32. Rajewsky N, Socci ND, Computational identification of microRNA targets. Dev Biol. 2004;267(2):529–35. doi: 10.1016/j.ydbio.2003.12.003 15013811
33. Peixoto LG, Calabria LK, Garcia L, Capparelli FE, Goulart LR, de Sousa MV, et al. Identification of major royal jelly proteins in the brain of the honeybee Apis mellifera. J Insect Physiol. 2009;55(8):671–7. doi: 10.1016/j.jinsphys.2009.05.005 19463826.
34. Rembold H, Lackner B, Geistbec. I, Chemical Basis of Honeybee, Apis-Mellifera, Caste Formation Partial-Purification of Queen Bee Determinator from Royal Jelly. J Insect Physiol. 1974;20(2):307–14. doi: 10.1016/0022-1910(74)90063-8
35. Buttstedt A, Ihling CH, Pietzsch M, Moritz RFA, Royalactin is not a royal making of a queen. Nature. 2016;537(7621):E10–E2. doi: 10.1038/nature19349http://www.nature.com/nature/journal/v537/n7621/abs/nature19349.html#supplementary-information. 27652566
36. Kucharski R, Maleszka J, Foret S, Maleszka R, Nutritional control of reproductive status in honeybees via DNA methylation. Science. 2008;319(5871):1827–30. doi: 10.1126/science.1153069 18339900
37. Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C, Ray A, et al. Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science. 2016;351(6268):aac6633. doi: 10.1126/science.aac6633 26722000.
38. Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L, Nature versus nurture in social insect caste differentiation. Trends in ecology & evolution. 2010;25(5):275–82. doi: 10.1016/j.tree.2009.12.001 20106547.
39. Zhou GY, Zhou Y, Chen X, New Insight into Inter-kingdom Communication: Horizontal Transfer of Mobile Small RNAs. Front Microbiol. 2017;8. Artn 768 doi: 10.3389/Fmicb.2017.00768 28507539
40. Liu H, Wang X, Wang HD, Wu J, Ren J, Meng L, et al. Escherichia coli noncoding RNAs can affect gene expression and physiology of Caenorhabditis elegans. Nature communications. 2012;3:1073. 10.1038/ncomms2071. doi: 10.1038/ncomms2071 23011127; PubMed Central PMCID: PMC3658002.
41. Nowara D, Gay A, Lacomme C, Shaw J, Ridout C, Douchkov D, et al. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell. 2010;22(9):3130–41. doi: 10.1105/tpc.110.077040 20884801; PubMed Central PMCID: PMC2965548.
42. Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel KH, Host-induced gene silencing of cytochrome P450 lanosterol C14alpha-demethylase-encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci U S A. 2013;110(48):19324–9. doi: 10.1073/pnas.1306373110 24218613; PubMed Central PMCID: PMC3845197.
43. Ghag SB, Shekhawat UK, Ganapathi TR, Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against Fusarium wilt in banana. Plant biotechnology journal. 2014;12(5):541–53. doi: 10.1111/pbi.12158 24476152.
44. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N, A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell. 2011;23(10):3812–23. doi: 10.1105/tpc.111.089813 21972259; PubMed Central PMCID: PMC3229151.
45. Ibrahim HM, Alkharouf NW, Meyer SL, Aly MA, Gamal El-Din Ael K, Hussein EH, et al. Post-transcriptional gene silencing of root-knot nematode in transformed soybean roots. Experimental parasitology. 2011;127(1):90–9. doi: 10.1016/j.exppara.2010.06.037 20599433.
46. Mao YB, Cai WJ, Wang JW, Hong GJ, Tao XY, Wang LJ, et al. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nature biotechnology. 2007;25(11):1307–13. doi: 10.1038/nbt1352 17982444.
47. Winston WM, Molodowitch C, Hunter CP, Systemic RNAi in C. elegans requires the putative transmembrane protein SID-1. Science. 2002;295(5564):2456–9. doi: 10.1126/science.1068836 11834782.
48. Feinberg EH, Hunter CP, Transport of dsRNA into cells by the transmembrane protein SID-1. Science. 2003;301(5639):1545–7. doi: 10.1126/science.1087117 12970568.
49. Alder MN, Dames S, Gaudet J, Mango SE, Gene silencing in Caenorhabditis elegans by transitive RNA interference. Rna. 2003;9(1):25–32. doi: 10.1261/rna.2650903 12554873; PubMed Central PMCID: PMC1370367.
50. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP, Prediction of plant microRNA targets. Cell. 2002;110(4):513–20. 12202040.
51. Tang G, Reinhart BJ, Bartel DP, Zamore PD, A biochemical framework for RNA silencing in plants. Genes Dev. 2003;17(1):49–63. doi: 10.1101/gad.1048103 12514099; PubMed Central PMCID: PMC195971.
52. Olsen PH, Ambros V, The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol. 1999;216(2):671–80. doi: 10.1006/dbio.1999.9523 10642801.
53. Bertholf LM, The utilization of carbohydrates as food by honeybee larvae. J Agric Res. 1927;35:0429–52.
54. Rembold H, Lackner B, Rearing of Honeybee Larvae Invitro—Effect of Yeast Extract on Queen Differentiation. J Apicult Res. 1981;20(3):165–71.
55. Velich AV, Development mechanical research on bee larvae. (The physiology of cocoon formation. The development-mechanical importance of the cocoon. A method for the breeding of bee larvae outside the honeycomb cells. The genesis of midget bees.). Z Wiss Zool Abt A. 1930;136(2):210–22.
56. Vandenberg JD, Shimanuki H, Technique for Rearing Worker Honeybees in the Laboratory. J Apicult Res. 1987;26(2):90–7.
57. Peng Y-SC, Mussen E, Fong A, Montague MA, Tyler T, Effects of chlortetracycline of honey bee worker larvae reared in vitro. J Invertebr Pathol. 1992;60(2):127–33.
58. Aupinel P, Fortini D, Dufour H, Tasei J, Michaud B, Odoux J, et al. Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bulletin of insectology. 2005;58(2):107.
59. Weaver N, Rearing of Honeybee Larvae on Royal Jelly in the Laboratory. Science. 1955;121(3145):509–10. doi: 10.1126/science.121.3145.509 17817382
60. De Souza DA, Wang Y, Kaftanoglu O, De Jong D, Amdam GV, Goncalves LS, et al. Morphometric Identification of Queens, Workers and Intermediates in In Vitro Reared Honey Bees (Apis mellifera). Plos One. 2015;10(4):e0123663. doi: 10.1371/journal.pone.0123663 25894528; PubMed Central PMCID: PMC4404332.
61. Fleming JC, Schmehl DR, Ellis JD, Characterizing the Impact of Commercial Pollen Substitute Diets on the Level of Nosema spp. in Honey Bees (Apis mellifera L.). PloS one. 2015;10(7):e0132014. doi: 10.1371/journal.pone.0132014 26226229; PubMed Central PMCID: PMC4520664.
62. Basualdo M, Barragan S, Antunez K, Bee bread increases honeybee haemolymph protein and promote better survival despite of causing higher Nosema ceranae abundance in honeybees. Environmental microbiology reports. 2014;6(4):396–400. doi: 10.1111/1758-2229.12169 24992539.
63. Kruger J, Rehmsmeier M, RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic acids research. 2006;34(Web Server issue):W451–4. doi: 10.1093/nar/gkl243 16845047; PubMed Central PMCID: PMC1538877.
64. Betel D, Wilson M, Gabow A, Marks DS, Sander C, The microRNA.org resource: targets and expression. Nucleic acids research. 2008;36(Database issue):D149–53. doi: 10.1093/nar/gkm995 18158296; PubMed Central PMCID: PMC2238905.