Advertisement

Biologia

, Volume 74, Issue 6, pp 649–660 | Cite as

Mobilization of fat body glycogen and haemolymph trehalose under nutritional stress in Bombyx mori larvae in relation to their physiological age and the duration of food deprivation

  • Sanathoibi D. Kh.
  • Bela KeshanEmail author
Original Article
  • 51 Downloads

Abstract

In insects, fat body glycogen and haemolymph trehalose are principal carbohydrate reserves. Here, in Bombyx mori (Linnaeus, 1758), we report an accelerated fat body glycogen accumulation in feeding 5th instar larvae, when they reach the terminal growth period (TGP). Haemolymph trehalose and glucose levels, however, fluctuated between 7–21 mM and 0.8–10 mM, respectively, depending on the larval physiological age. Food deprivation triggered a dramatic increase in mobilization of glycogen in larvae at TGP than at active growth period (AGP), mobilized almost 78% of stored glycogen at an initial 12 h of food deprivation, possibly by increasing the percentage of active glycogen phosphorylase, as observed. This rapid glycogen mobilization, along with meeting the energy demand of starving tissues, might also have provided glucose for trehalose synthesis, as evident by observed hypertrehalosemia. A prolonged food deprivation (24–48 h) triggered hypotrehalosemia along with an increase in the enzyme activity of trehalase, and the transcript level of trehalase-2, indicating the utilization of trehalose as an energy source for the demanding tissues. Further, in TGP larvae, a prolonged food deprivation increased the level of haemolymph glucose (1.8–3.5 mM) as well as glucose/trehalose ratio, and this suggests that the fat body might have released the glucose molecules directly into the haemolymph, instead of utilizing it for trehalose synthesis, possibly to minimize the expenditure of energy. Thus, short-term food deprivation triggered an initial glycogen mobilization whereas, prolonged food deprivation led to the utilization of trehalose as an energy source. Hence, mobilization of carbohydrate reserves varied depending on the larval physiological age and the extent of food deprivation period. The future investigation can expand our understanding on the role of glucose as an important haemolymph sugar along with trehalose.

Keywords

Fat body Haemolymph Food deprivation Glycogen Trehalose Glucose 

Notes

Acknowledgments

We are thankful to The Director, Central Sericultural Germplasm Resource Centre (CSGRC), CSB, Hosur, Tamil Nadu, India for providing us disease-free layings of the silkworm. This study was supported by the Department of Biotechnology (DBT), Government of India under Basic Research and Emerging Areas, BT/PR14289/BRB/10/837/2010 (2011-14).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11756_2019_196_MOESM1_ESM.pdf (246 kb)
ESM 1 (PDF 245 kb)

References

  1. Al Baki MA, Jung JK, Kim Y (2018) Regulation of hemolymph trehalose titers by insulin signaling in the legume pod borer, Maruca vitrata (Lepidoptera: Crambidae). Peptides 106:28–36.  https://doi.org/10.1016/j.peptides.2018.06.006 CrossRefPubMedGoogle Scholar
  2. Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism, and regulation. Annu Rev Entomol 55:207–225.  https://doi.org/10.1146/annurev-ento-112408-085356 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Becker A, Schloder P, Steele JE, Wegener G (1996) The regulation of trehalose metabolism in insects. Experientia 52:433–439.  https://doi.org/10.1007/bf01919312 CrossRefPubMedGoogle Scholar
  4. Cornette R, Kikawada T (2011) The induction of anhydrobiosis in the sleeping chironomid: current status of our knowledge. IUBMB Life 63:419–429.  https://doi.org/10.1002/iub.463 CrossRefGoogle Scholar
  5. DeVries ZC, Reid WR, Kells SA, Appel AG (2015) Effects of starvation on deltamethrin tolerance in bed bugs, Cimex lectularius L. (Hemiptera: Cimicidae). Insects 6:102–111.  https://doi.org/10.3390/insects6010102 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400Google Scholar
  7. Fraga A,  Ribeiro L,  Lobato M,  Santos V,  Silva JR,  Gomes H,  da Cunha Moraes JL,  de Souza Menezes J,  de Oliveira CJ,  Campos E,  da Fonseca RN  (2013) Glycogen and glucose metabolism are essential for early embryonic development of the red flour beetle Tribolium castaneum. PLoS One 8:e65125.  https://doi.org/10.1371/journal.pone.0065125
  8. Gu JH, Shao Y, Zhang CW, Liu ZW, Zhang YJ (2009) Characterization of putative soluble and membrane-bound trehalases in a hemipteran insect, Nilaparvata lugens. J Insect Physiol 55:997–1002.  https://doi.org/10.1016/j.jinsphys.2009.07.003 CrossRefPubMedGoogle Scholar
  9. Hou L, Cai MJ, Liu W, Song Q, Zhao XF (2012) Small GTPase Rab4b participates in the gene transcription of 20-hydroxyecdysone and insulin pathways to regulate glycogen level and metamorphosis. Dev Biol 371:13–22.  https://doi.org/10.1016/j.ydbio.2012.06.015 CrossRefPubMedGoogle Scholar
  10. Inagaki S, Yamashita O (1986) Metabolic shift from lipogenesis to glycogenesis in the last instar larval fat body of the silkworm, Bombyx mori. Insect Biochem 16:327–331.  https://doi.org/10.1016/0020-1790(86)90043-0 CrossRefGoogle Scholar
  11. Isabel I, Martin JR, Chidami S, Veenstra JA, Rosay P (2005) AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am J Phys Regul Integr Comp Phys 288:R531–R538.  https://doi.org/10.1152/ajpregu.00158.2004 CrossRefGoogle Scholar
  12. Kamei Y, Hasegawa Y, Niimi T, Yamashita O, Yaginuma T (2011) Trehalase-2 protein contributes to trehalase activity enhanced by diapause hormone in developing ovaries of the silkworm, Bombyx mori. J Insect Physiol 57:608–613.  https://doi.org/10.1016/j.jinsphys.2010.10.001 CrossRefPubMedGoogle Scholar
  13. Keshan B, Ray AK (1998) Subcellular localization of trehalase in different tissues of the silkworm, Bombyx mori.  Demonstration of the highest activity in mitochondria. Sericologia 38:411–418Google Scholar
  14. Keshan B, Thounaojam B, Kh. SD (2015) A comprehensive study of the changes in ecdysteroid levels during the feeding phase of fifth instar larvae of the silkworm, Bombyx mori (Lepidoptera: Bombycidae). Eur J Entomol 112:632–641. https://doi.org/10.14411/eje.2015.088Google Scholar
  15. Keshan B, Thounaojam B, Kh. SD (2017) Insulin and 20-hydroxyecdysone action in Bombyx mori: Glycogen content and expression pattern of insulin and ecdysone receptors in fat body. Gen Comp Endocrinol 241:108–117. https://doi.org/10.1016/j.ygcen.2016.06.022Google Scholar
  16. Kim Y, Hong Y (2015) Regulation of hemolymph trehalose level by an insulin-like peptide through diel feeding rhythm of the beet armyworm, Spodoptera exigua. Peptides 68:91–98.  https://doi.org/10.1016/j.peptides.2015.02.003 CrossRefPubMedGoogle Scholar
  17. Lee GH, Park JH (2004) Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167:311–323CrossRefPubMedPubMedCentralGoogle Scholar
  18. Lohr P, Gade G (1983) Carbohydrate metabolism in the stick insect, Carausius morosus. J Insect Physiol 29:287.  https://doi.org/10.1016/0022-1910(83)90097-5 CrossRefGoogle Scholar
  19. Łopieńska-Biernat E, Żółtowska K, Zaobidna EA, Dmitryjuk M, Bąk B (2018) Developmental changes in gene expression and enzyme activities of anabolic and catabolic enzymes for storage carbohydrates in the honeybee, Apis mellifera. Insect Soc 65:571–580.  https://doi.org/10.1007/s00040-018-0648-1
  20. Mariano AC, Santos R, Gonzalez MS, Feder D, Machado EA, Pascarelli B, Gondim KC, Meyer-Fernandes JR (2009) Synthesis and mobilization of glycogen and trehalose in adult male Rhodnius prolixus. Arch Insect Biochem Physiol 72:1–15.  https://doi.org/10.1002/arch.20319 CrossRefPubMedGoogle Scholar
  21. Masumura M, Satake SI, Saegusa H, Mizoguchi A (2000) Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori. Gen Comp Endocrinol 118:393–399.  https://doi.org/10.1006/gcen.1999.7438 CrossRefPubMedGoogle Scholar
  22. Merzendorfer H (2011) The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur J Cell Biol 90:759–769.  https://doi.org/10.1016/j.ejcb.2011.04.014 CrossRefPubMedGoogle Scholar
  23. Meyer-Fernandes JR, Clark CP, Gondim KC, Wells MA (2001) Fat body fructose-2,6-bisphosphate content and phosphorylase activity correlate with changes in hemolymph glucose concentration during fasting and re-feeding in larval Manduca sexta. Insect Biochem Mol Biol 31:165–170.  https://doi.org/10.1016/s0965-1748(00)00114-4 CrossRefPubMedGoogle Scholar
  24. Mirth CK, Riddiford LM (2007) Size assessment and growth control: how adult size is determined in insects. Bioessays 29:344–355.  https://doi.org/10.1002/bies.20552 CrossRefPubMedGoogle Scholar
  25. Mitsumasu K, Azuma M, Niimi T, Yamashita O, Yaginuma T (2005) Membrane-penetrating trehalase from silkworm Bombyx mori. Molecular cloning and localization in larval midgut. Insect Mol Biol 14:501–508.  https://doi.org/10.1111/j.1365-2583.2005.00581.x CrossRefPubMedGoogle Scholar
  26. Mitsumasu K, Kanamori Y, Fujita M, Iwata K, Tanaka D, Kikuta S, Watanabe M, Cornette R, Okuda T, Kikawada T (2010) Enzymatic control of anhydrobiosis-related accumulation of trehalose in the sleeping chironomid, Polypedilum vanderplanki. FEBS J 277:4215–4228.  https://doi.org/10.1111/j.1742-4658.2010.07811.x CrossRefPubMedPubMedCentralGoogle Scholar
  27. Mochanová M, Tomčala A, Svobodová Z, Kodrik D (2018) Role of adipokinetic hormone during starvation in Drosophila. Comp Biochem Physiol B 226:26–35.  https://doi.org/10.1016/j.cbpb.2018.08.004
  28. Morishima I, Suizu T (1982) Glycogen phosphorylase activity in fat body during development of the silkworm, Bombyx mori. Agric Biol Chem 46:575–576.  https://doi.org/10.1080/00021369.1982.10865106 CrossRefGoogle Scholar
  29. Oda Y, Uejima M, Iwami M, Sakurai S (2000) Role of ecdysteroids in the dynamics of insect haemolymph sugar. Zool Sci 17:785–789.  https://doi.org/10.2108/zsj.17.785 CrossRefGoogle Scholar
  30. Satake S, Kawabe Y, Mizoguchi A (2000) Carbohydrate metabolism during starvation in the silkworm Bombyx mori. Arch Insect Biochem Physiol 44:90–98.  https://doi.org/10.1002/1520-6327(200006)44:2<90::aid-arch4>3.0.co;2-0 CrossRefPubMedGoogle Scholar
  31. Shi ZK, Wang S, Wang SG, Zhang L, Xu YX, Guo XJ, Zhang F, Tang B (2017) Effects of starvation on the carbohydrate metabolism in Harmonia axyridis (Pallas). Biol Open 6:1096–1103.  https://doi.org/10.1242/bio.025189 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Shingleton AW, Frankino WA, Flatt T, Nijhout HF, Emlen DJ (2007) Size and shape: the developmental regulation of static allometry in insects. Bioessays 29:536–548.  https://doi.org/10.1002/bies.20584 CrossRefPubMedGoogle Scholar
  33. Steele JE (1982) Glycogen phosphorylase in insects. Insect Biochem 12:131–147.  https://doi.org/10.1016/0020-1790(82)90001-4 CrossRefGoogle Scholar
  34. Steele JE (2016) Evidence that ecdysis in the larval cockroach, Periplaneta americana L. is triggered by an increase in the concentration of hemolymph sugar. Arch Insect Biochem Physiol 92:159–172.  https://doi.org/10.1002/arch.21323 CrossRefPubMedGoogle Scholar
  35. Sumida M, Yamashita O (1983) Purification and some properties of soluble trehalase from midgut of pharate adult of the silkworm, Bombyx mori. Insect Biochem 13:257–265.  https://doi.org/10.1016/0020-1790(83)90047-1 CrossRefGoogle Scholar
  36. Suren-Castillo S, Abrisqueta M, Maestro JL (2014) FoxO is required for the activation of hypertrehalosemic hormone expression in cockroaches. Biochim Biophys Acta Gen Subj 1840:86–94.  https://doi.org/10.1016/j.bbagen.2013.08.015 CrossRefGoogle Scholar
  37. Sutherland EW, Wosilait WD (1956) The relationship of epinephrine and glucagon to liver phosphorylase: 1. Liver phosphorylase; preparation and properties. J Biol Chem 218:459–468PubMedGoogle Scholar
  38. Takiguchi M, Niimi T, Su ZH, Yaginuma T (1992) Trehalase from male accessory-gland of an insect, Tenebrio molitor - cDNA sequencing and developmental profile of the gene-expression. Biochem J 288:19–22.  https://doi.org/10.1042/bj2880019 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Tang B, Chen XF, Liu Y, Tian HG, Liu J, Hu J, Xu WH, Zhang WQ (2008) Characterization and expression patterns of a membrane-bound trehalase from Spodoptera exigua. BMC Mol Biol 9:51.  https://doi.org/10.1186/1471-2199-9-51 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Tang B, Qin Z, Shi ZK, Wang S, Guo XJ, Wang SG, Zhang F (2014) Trehalase in Harmonia axyridis (Coleoptera: Coccinellidae): effects on beetle locomotory activity and the correlation with trehalose metabolism under starvation conditions. Appl Entomol Zool 49:255–264.  https://doi.org/10.1007/s13355-014-0244-4 CrossRefGoogle Scholar
  41. Thompson SN (2003) Trehalose - the insect 'blood' sugar. Adv Insect Physiol 31:205–285.  https://doi.org/10.1016/s0065-2806(03)31004-5 CrossRefGoogle Scholar
  42. Thounaojam B, Keshan B (2017) Modulation of gene expression by nutritional state and hormones in Bombyx larvae in relation to its growth period. Gene Expr Patterns 25-26:175–183.  https://doi.org/10.1016/j.gep.2017.08.003 CrossRefPubMedGoogle Scholar
  43. Wang Y, Campbell JB, Kaftanoglu O, Page RE, Amdam GV, Harrison JF (2016) Larval starvation improves metabolic response to adult starvation in honey bees (Apis mellifera L.). J Exp Biol 219:960–968.  https://doi.org/10.1242/jeb.136374 CrossRefPubMedGoogle Scholar
  44. Xu JJ, Sheng ZT, Palli SR (2013) Juvenile hormone and insulin regulate trehalose homeostasis in the red flour beetle, Tribolium castaneum. PLoS Genet 9:e1003535.  https://doi.org/10.1371/journal.pgen.1003535 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xu HJ, Xue J, Lu B, Zhang XC, Zhuo JC, He SF, Ma XF, Jiang YQ, Fan HW, Xu JY, Ye YX, Pan PL, Li Q, Bao YY, Nijhout HF, Zhang CX (2015) Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519:464–467.  https://doi.org/10.1038/nature14286 CrossRefPubMedGoogle Scholar
  46. Yamada T, Habara O, Kubo H, Nishimura T (2018) Fat body glycogen serves as a metabolic safeguard for the maintenance of sugar levels in Drosophila. Development 145:dev158865.  https://doi.org/10.1242/dev.158865 CrossRefPubMedGoogle Scholar
  47. Zhou LH, Li HH, Hao FH, Li N, Liu X, Wang GL, Wang YL, Tang HR (2015) Developmental changes for the hemolymph metabolome of silkworm (Bombyx mori L.). J Proteome Res 14:2331–2347.  https://doi.org/10.1021/acs.jproteome.5b00159 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Institute of Zoology, Slovak Academy of Sciences 2019

Authors and Affiliations

  1. 1.Department of ZoologyNorth-Eastern Hill UniversityShillongIndia

Personalised recommendations