De novo transcriptome analysis of the excretory tubules of Carausius morosus (Phasmatodea) and possible functions of the midgut ‘appendices’ (original) (raw)
Abstract
The Malpighian tubules are the insect excretory organs, responsible for ion and water homeostasis and elimination of nitrogenous wastes. Post-genomic assays suggest they also metabolize and detoxify xenobiotic compounds and have antimicrobial properties. The Phasmatodea have an additional, unique set of excretory organs referred to predominantly as midgut appendices. Their function and how it compares to phasmid and other insect Malpighian tubules is unknown. Hypotheses include carbonic anhydrase activity, calcium and metal cation sequestration, and xenobiotic transport. This work presents the first comparative transcriptomic analysis of the Phasmatodean excretory organs, using the model insect Carausius morosus. I produced de novo transcriptomes of the midgut appendices, midgut wall, and Malpighian tubules, and looked for differentially expressed genes associated with putative organ functions. The appendices differentially and highly express lipid transport and metabolism proteins, and the biomineralization gene otopetrin. The Malpighian tubules differentially and highly express acid phosphatases and multiple transporter types, while appendices express fat-soluble vitamin and peptide transporters. Many defense proteins such as multidrug resistance proteins, ABC transporters, cytochrome P450's, and glutathione-S-transferases were differentially expressed in specific excretory organs. I hypothesize that the appendices and Malpighian tubules both have defensive / xenobiotic metabolism functions, but each likely target different substrates. Phasmid Malpighian tubules excrete as in other insects, while the appendices may predominantly regulate amino acids, fats, and fat-soluble compounds. Lipid metabolism in insects is poorly understood, and the Phasmatodea may thus serve as a model for studying this further.
Loading Preview
Sorry, preview is currently unavailable. You can download the paper by clicking the button above.
References (69)
- O'Donnell M. Insect Excretory Mechanisms. In: Simpson SJ, editor. Advances in Insect Physiology. 1 ed. Oxford, UK: Academic Press; 2008. p. 1-122.
- Ramsay JA. The Excretion of Sodium and Potassium by the Malpighian Tubules of Rhodnius. J Exp Biol. 1952; 29:110-26.
- Ramsay JA. Active Transport of Water by the Malpighian Tubules of the Stick Insect, Dixippus morosus (Orthoptera, Phasmidae). J Exp Biol. 1954; 31(1):104-13.
- Ramsay JA. The Excretion of Sodium, Potassium and Water by the Malpighian Tubules of the Stick Insect, Dixippus morosus (Orthoptera, Phasmidae). J Exp Biol. 1955; 32:200-16.
- Ramsay JA. Excretion by the Malpighian Tubules of the Stick Insect, Dixippus morosus (Orthoptera, Phasmidae): Calcium, Magnesium, Chloride, Phosphate and Hydrogen Ions. J Exp Biol. 1956; 33:697- 708.
- Ramsay JA. Excretion by the Malpighian Tubules of the Stick Insect, Dixippus morosus (Orthoptera, Phasmidae): Amino Acids, Sugars and Urea. J Exp Biol. 1958; 35:871-91.
- Taylor HH. Water and Solute Transport by the Malpighian Tubules of the Stick Insect, Carausius moro- sus: The Normal Ultrastructure of the Type 1 Cells. Z Zellforsch. 1971; 118:333-68. PMID: 4327755
- Taylor HH. The Fine Structure of the Type 2 Cells in the Malpighian Tubules of the Stick Insect, Carau- sius morosus. Z Zellforsch. 1971; 122:411-24. PMID: 4330610
- Taylor HH. Structural and Functional Changes in the Malpighian Tubules of Carausius morosus during Dehydration and Starvation. Z Zellforsch. 1973; 141:479-92. PMID: 4747682
- Taylor HH. The Osmolarity of Fluid Secreted by the Malpighian Tubules of Carausius morosus. Comp Biochem Physiol. 1974; 47A:1129-34.
- Lison L. E ´tudes Histophysiologiques sur les Tubes de Malpighi des Insectes. III. L'e ´limination des color- ants basiques chez les orthoptères. Cell and tissue research. 1937; 28(2):179-209.
- Lison L. Recherches sur l'histophysiologie compare ´e de l'excre ´tion chez les arthropodes. Brussels: Palais des acade ´mies; 1942. 106 p. p.
- Atzbacher U, Hevert F, Weber-Von Grotthuss E, Wessing A. The influence of ouabain on the elimination of injected and orally applied dyes in Drosophila hydei. J Insect Physiol. 1974; 20(10):1989-97. PMID: 4421313
- Maddrell SHP, Gardiner BOC, Pilcher DE, Reynolds SE. Active transport by insect malpighian tubules of acidic dyes and of acylamides. J Exp Biol. 1974; 61(2):357-77. PMID: 4443733
- Maddrell SHP, Gardiner BOC. Excretion of Alkaloids by Malpighian Tubules of Insects. J Exp Biol. 1976; 64:267-81. PMID: 932618
- Meulemans W, De Loof A. Transport of the cationic fluorochrome rhodamine 123 in an insect's Malpi- ghian tubule: indications of a reabsorptive function of the secondary cell type. Journal of cell science. 1992; 101 (Pt 2):349-61.
- O'Donnell MJ, Dow JA, Huesmann GR, Tublitz NJ, Maddrell SH. Separate control of anion and cation transport in malpighian tubules of Drosophila melanogaster. J Exp Biol. 1996; 199(Pt 5):1163-75. PMID: 8786336
- Maddrell SHP, O'Donnell MJ. Insect Malpighian Tubules: V-ATPase Action in Ion and Fluid Transport. J Exp Biol. 1992; 172:417-29. PMID: 9874752
- Maddrell S. Active transport of water by insect Malpighian tubules. J Exp Biol. 2004; 207(Pt 6):894-6. PMID: 14766947
- Pannabecker T. Physiology of the Malpighian Tubule. Annu Rev Entomol. 1995; 40:493-510.
- Wang J, Kean L, Yang J, Allan AK, Davies SA, Herzyk P, et al. Function-informed transcriptome analy- sis of Drosophila renal tubule. Genome biology. 2004; 5(9):R69. https://doi.org/10.1186/gb-2004-5-9- r69 PMID: 15345053
- Strauss AS, Wang D, Stock M, Gretscher RR, Groth M, Boland W, et al. Tissue-Specific Transcript Pro- filing for ABC Transporters in the Sequestering Larvae of the Phytophagous Leaf Beetle Chrysomela populi. PLoS One. 2014; 9(6):e98637. https://doi.org/10.1371/journal.pone.0098637 PMID: 24887102
- McGettigan J, McLennan RK, Broderick KE, Kean L, Allan AK, Cabrero P, et al. Insect renal tubules constitute a cell-autonomous immune system that protects the organism against bacterial infection. Insect Biochem Mol Biol. 2005; 35(7):741-54. https://doi.org/10.1016/j.ibmb.2005.02.017 PMID: 15894191
- Dow JA, Davies SA. The Malpighian tubule: rapid insights from post-genomic biology. J Insect Physiol. 2006; 52(4):365-78. https://doi.org/10.1016/j.jinsphys.2005.10.007 PMID: 16310213
- Yang J, McCart C, Woods DJ, Terhzaz S, Greenwood KG, ffrench-Constant RH, et al. A Drosophila systems approach to xenobiotic metabolism. Physiological genomics. 2007; 30(3):223-31. https://doi. org/10.1152/physiolgenomics.00018.2007 PMID: 17488889
- Mamidala P, Wijeratne AJ, Wijeratne S, Kornacker K, Sudhamalla B, Rivera-Vega LJ, et al. RNA-Seq and molecular docking reveal multi-level pesticide resistance in the bed bug. BMC genomics. 2012; 13:6. https://doi.org/10.1186/1471-2164-13-6 PMID: 22226239
- Dow JA. Insights into the Malpighian tubule from functional genomics. J Exp Biol. 2009; 212(Pt 3):435- 45. https://doi.org/10.1242/jeb.024224 PMID: 19151219
- Nijhout HF. Excretory Role of the Midgut in Larvae of the Tobacco Hornworm, Manduca sexta (L.). J Exp Biol. 1975; 62:221-30. PMID: 1151277
- Palm N-B. Storage and excretion of vital dyes in insects: With special regard to trypan blue. Arkiv fo ¨r Zoologi. Stockholm: Almqvist u. Wiksell; 1952. p. 195-272.
- Shelomi M, Sitepu IR, Boundy-Mills KL, Kimsey LS. Review of the Gross Anatomy and Microbiology of the Phasmatodea Digestive Tract. Journal of Orthoptera Research. 2015; 24(1):29-40.
- Bradler S. Der Phasmatodea Tree of Life: U ¨berraschendes und Ungekla ¨rtes in der Stabschrecken-Evo- lution. Entomologie heute. 2015; 27:1-23.
- Shelomi M, Kimsey LS. Vital staining of the stick insect digestive system identifies appendices of the midgut as novel system of excretion. Journal of Morphology. 2014; 275(6):623-33. https://doi.org/10\. 1002/jmor.20243 PMID: 24338977
- Monteiro EC, Tamaki FK, Terra WR, Ribeiro AF. The digestive system of the "stick bug" Cladomorphus phyllinus (Phasmida, Phasmatidae): A morphological, physiological and biochemical analysis. Arthro- pod structure & development. 2014; 43(2):123-34.
- Bordas L. Conside ´rations ge ´ne ´rales sur l'appareil digestif des "Phasmidae". Bulletin du Museum d'His- toire Naturelle (Paris). 1897; 2:378-9.
- Heymons R. Ueber die Organisation und Entwickelung von Bacillus rossii Fabr. Sitzungsberichte der Ko ¨niglich Preussischen Akademie der Wissenschaften zu Berlin. 1897; 16:363-73.
- Ramsay JA. The Excretory System of the Stick Insect Dixippus morosus (Orthoptera, Phasmidae). Journal of Experimental Biology. 1955; 32:183-99.
- Aneshansley D, Marler C, Beyenbach K. Transepithelial voltage measurements in isolated Malpighian tubules of Aedes aegypti. J Insect Physiol. 1989; 35(1):41-52.
- Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome research. 1999; 9(9):868- 77. PMID: 10508846
- Conesa A, Gotz S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. Interna- tional journal of plant genomics. 2008; 2008:619832. https://doi.org/10.1155/2008/619832 PMID: 18483572
- Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, et al. KEGG for linking genomes to life and the environment. Nucleic acids research. 2008; 36(Database issue):D480-D4. https://doi.org/10\. 1093/nar/gkm882 PMID: 18077471
- Wheeler TJ, Eddy SR. nhmmer: DNA homology search with profile HMMs. Bioinformatics. 2013; 29 (19):2487-9. https://doi.org/10.1093/bioinformatics/btt403 PMID: 23842809
- Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, et al. The Pfam protein families database. Nucleic acids research. 2004; 32(Database issue):D138-D41. https://doi.org/10.1093/nar/ gkh121 PMID: 14681378
- Schmitz G, Langmann T. Structure, function and regulation of the ABC1 gene product. Current opinion in lipidology. 2001; 12(2):129-40. PMID: 11264984
- Vaughan AM, Oram JF. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. Journal of lipid research. 2006; 47(11):2433-43. https://doi.org/10\. 1194/jlr.M600218-JLR200 PMID: 16902247
- Toyoda Y, Hagiya Y, Adachi T, Hoshijima K, Kuo MT, Ishikawa T. MRP class of human ATP binding cassette (ABC) transporters: historical background and new research directions. Xenobiotica. 2008; 38 (7-8):833-62. https://doi.org/10.1080/00498250701883514 PMID: 18668432
- Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA. Fat metabolism in insects. Annual review of nutrition. 2001; 21:23-46. https://doi.org/10.1146/annurev.nutr.21.1.23 PMID: 11375428
- Arrese EL, Canavoso LE, Jouni ZE, Pennington JE, Tsuchida K, Wells MA. Lipid storage and mobiliza- tion in insects: current status and future directions. Insect Biochem Mol Biol. 2001; 31(1):7-17. PMID: 11102830
- Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, et al. A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Developmental Biology. 2006; 300(1):335-48. http://dx.doi.org/10.1016/j.ydbio.2006.07.047\. PMID: 16987510
- Shelomi M, Jasper WC, Atallah J, Kimsey LS, Johnson BR. Differential expression of endogenous plant cell wall degrading enzyme genes in the stick insect (Phasmatodea) midgut. BMC Genomics. 2014; 15:917. https://doi.org/10.1186/1471-2164-15-917 PMID: 25331961
- Pantel J. Le calcium, forme de rêserve dans la femelle des Phasmides; ses formes d'e ´limination dans les deux sexes. Comptes Rendus Acad Sci Paris. 1919; 168:242-4.
- Moscona A. Studies of the Egg of Bacillus libanicus (Orthoptera, Phasmidae). I. The Egg Envelopes. Quarterly Journal of Microscopical Science. 1950; 91(2):183-93. PMID: 24538992
- Savage AA. The development of the Malpighian tubules of Carausius morosus (Orthoptera). Quarterly Journal of Microscopical Science. 1962; 103(4):417-37.
- Eguchi M. Alkaline phosphatase isozymes in insects and comparison with mammalian enzyme. Com- parative biochemistry and physiology Part B, Biochemistry & molecular biology. 1995; 111(2):151-62.
- Yi SX, Adams TS. Age-and diapause-related acid and alkaline phosphatase activities in the intestine and malpighian tubules of the Colorado potato beetle, Leptinotarsa decemlineata (Say). Arch Insect Biochem Physiol. 2001; 46(3):152-63. https://doi.org/10.1002/arch.1025 PMID: 11276072
- O'Donnell MJ. Too much of a good thing: how insects cope with excess ions or toxins in the diet. J Exp Biol. 2009; 212(Pt 3):363-72. https://doi.org/10.1242/jeb.023739 PMID: 19151211
- Ursic-Bedoya R, Buchhop J, Joy JB, Durvasula R, Lowenberger C. Prolixicin: a novel antimicrobial pep- tide isolated from Rhodnius prolixus with differential activity against bacteria and Trypanosoma cruzi. Insect Mol Biol. 2011; 20(6):775-86. https://doi.org/10.1111/j.1365-2583.2011.01107.x PMID: 21906194
- Allan AK, Du J, Davies SA, Dow JA. Genome-wide survey of V-ATPase genes in Drosophila reveals a conserved renal phenotype for lethal alleles. Physiological genomics. 2005; 22(2):128-38. https://doi. org/10.1152/physiolgenomics.00233.2004 PMID: 15855386
- Beyenbach KW, Skaer H, Dow JA. The developmental, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol. 2010; 55:351-74. https://doi.org/10.1146/annurev-ento-112408-085512 PMID: 19961332
- Shapiro JP, Law JH, Wells MA. Lipid transport in insects. Annu Rev Entomol. 1988; 33(1):297-318.
- de Sine ´ty R. Recherches sur la biologie et l'anatomie des Phasmes. La Cellule. 1901; 19:117-278.
- Cermelli S, Guo Y, Gross SP, Welte MA. The lipid-droplet proteome reveals that droplets are a protein- storage depot. Curr Biol. 2006; 16(18):1783-95. https://doi.org/10.1016/j.cub.2006.07.062 PMID: 16979555
- Hughes I, Binkley J, Hurle B, Green ED, Sidow A, Ornitz DM. Identification of the Otopetrin Domain, a conserved domain in vertebrate otopetrins and invertebrate otopetrin-like family members. BMC Evol Biol. 2008; 8:41. https://doi.org/10.1186/1471-2148-8-41 PMID: 18254951
- Sharpe ML, Dearden PK, Gimenez G, Krause KL. Comparative RNA seq analysis of the New Zealand glowworm Arachnocampa luminosa reveals bioluminescence-related genes. BMC genomics. 2015; 16 (1):825.
- Zhu J, Busche JM, Zhang X. Identification of juvenile hormone target genes in the adult female mosqui- toes. Insect Biochem Mol Biol. 2010; 40:23-9. https://doi.org/10.1016/j.ibmb.2009.12.004 PMID: 20018242
- Wang GX, Cho KW, Uhm M, Hu CR, Li S, Cozacov Z, et al. Otopetrin 1 protects mice from obesity- associated metabolic dysfunction through attenuating adipose tissue inflammation. Diabetes. 2014; 63 (4):1340-52. https://doi.org/10.2337/db13-1139 PMID: 24379350
- Wu C, Crowhurst RN, Dennis AB, Twort VG, Liu S, Newcomb RD, et al. De novo Transcriptome Analy- sis of the Common New Zealand Stick Insect Clitarchus hookeri (Phasmatodea) Reveals Genes involved in Olfaction, Digestion and Sexual Reproduction. PLoS ONE. 2016, 11(6): e0157783. https:// doi.org/10.1371/journal.pone.0157783 PMID: 27336743
- Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expres- sion analysis of RNA-seq experiments with TopHat and Cufflinks. Nature protocols. 2012; 7(3):562-78. https://doi.org/10.1038/nprot.2012.016 PMID: 22383036
- Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research. 2004; 32(5):1792-7. https://doi.org/10.1093/nar/gkh340 PMID: 15034147
- Zhao S, Guo Y, Sheng Q, Shyr Y. Heatmap3: an improved heatmap package with more powerful and convenient features. BMC bioinformatics. 2014; 15(Suppl 10):P16.