Termites have many unique evolutionary adaptations associated with their eusocial lifestyles. Recent omics research has created a wealth of new information in numerous areas of termite biology (e.g., caste polyphenism, lignocellulose digestion, and microbial symbiosis) with wide-ranging applications in diverse biotechnological niches. Termite biotechnology falls into two categories: () termite-targeted biotechnology for pest management purposes, and () termite-modeled biotechnology for use in various industrial applications. The first category includes several candidate termiticidal modes of action such as RNA interference, digestive inhibition, pathogen enhancement, antimicrobials, endocrine disruption, and primer pheromone mimicry. In the second category, termite digestomes are deep resources for host and symbiont lignocellulases and other enzymes with applications in a variety of biomass, industrial, and processing applications. Moving forward, one of the most important approaches for accelerating advances in both termite-targeted and termite-modeled biotechnology will be to consider host and symbiont together as a single functional unit.


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Literature Cited

  1. Anderson WF, Akin DE. 1.  2008. Structural and chemical properties of grass lignocelluloses related to conversion for biofuels. J. Ind. Microbiol. Biotechnol. 35:355–66 [Google Scholar]
  2. Baum JA, Bogaert T, Clinton W, Heck GR, Feldmann P. 2.  et al. 2007. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 25:1322–26 [Google Scholar]
  3. Bellés X, Martín D, Piulachs MD. 3.  2005. The mevalonate pathway and the synthesis of juvenile hormone in insects. Annu. Rev. Entomol. 50:181–99 [Google Scholar]
  4. Bignell DE. 4.  2011. Morphology, physiology, biochemistry and functional design of the termite gut: an evolutionary wonderland. See Ref. 5 375–412
  5. Bignell DE, Roisin Y, Lo N. 5.  2011. Biology of Termites: A Modern Synthesis Dordrecht, Netherlands: Springer [Google Scholar]
  6. Boucias DG, Stokes C, Storey G, Pendland JC. 6.  1996. The effects of imidacloprid on the termite Reticulitermes flavipes and its interaction with the mycopathogen Beauveria bassiana. Pflanzenschutz-Nachr. Bayer 49:103–44 [Google Scholar]
  7. Brennan Y, Callen WN, Christoffersen L, Dupree P, Goubet F. 7.  et al. 2004. Unusual microbial xylanases from insect guts. Appl. Environ. Microbiol. 70:3609–17 [Google Scholar]
  8. Breznak JA, Brune A. 8.  1994. Role of microorganisms in the digestion of lignocellulose by termites. Annu. Rev. Entomol. 39:453–87 [Google Scholar]
  9. Brugerolle G, Radek R. 9.  2006. Symbiotic protozoa of termites. Soil Biology HVA Konig 243–69 Berlin: Springer-Verlag [Google Scholar]
  10. Brune A, Emerson D, Breznak JA. 10.  1995. Termite gut microflora as an oxygen sink: microelectrode determinations of oxygen and pH gradients in guts of lower and higher termites. Appl. Env. Microbiol. 61:2681–87 [Google Scholar]
  11. Brune A, Miambi E, Breznak JA. 11.  1995. Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Appl. Environ. Microbiol. 61:2688–95 [Google Scholar]
  12. Brune A, Ohkuma M. 12.  2011. Role of the termite gut microbiota in symbiotic digestion. See Ref. 5, pp 439–75
  13. Bulmer MS, Bachelet I, Raman R, Rosengaus RB, Sasisekharan R. 13.  2009. Targeting an antimicrobial effector function in insect immunity as a pest control strategy. Proc. Natl. Acad. Sci. USA 106:12652–57 [Google Scholar]
  14. Bulmer MS, Crozier RH. 14.  2006. Variation in positive selection in termite GNBPs and Relish. Mol. Biol. Evol. 23:317–26 [Google Scholar]
  15. Bulmer MS, Lay F, Hamilton C. 15.  2010. Adaptive evolution in subterranean termite antifungal peptides. Insect Mol. Biol. 19:669–74 [Google Scholar]
  16. Cairo JP, Oliveira LC, Uchima CA, Alvarez TM, Citadini AP. 16.  et al. 2013. Deciphering the synergism of endogenous glycoside hydrolase families 1 and 9 from Coptotermes gestroi. Insect Biochem. Mol. Biol. 43:970–81 [Google Scholar]
  17. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B. 17.  2009. The Carbohydrate-Active EnZymes database: CAZy; an expert resource for glycogenomics. Nucleic Acids Res. 37:D233 [Google Scholar]
  18. Chandrasekharaiah M, Thulasi A, Bagath M, Kumar DP, Santosh SS. 18.  et al. 2011. Molecular cloning, expression and characterization of a novel feruloyl esterase enzyme from the symbionts of termite (Coptotermes formosanus) gut. BMB Rep. 44:52–57 [Google Scholar]
  19. Chouvenc T, Su NY, Grace JK. 19.  2011. Fifty years of attempted biological control of termites—analysis of a failure. Biol. Control 59:69–82 [Google Scholar]
  20. Cleveland LR. 20.  1923. Symbiosis between termites and their intestinal protozoa. Proc. Natl. Acad. Sci. USA 9:424–28 [Google Scholar]
  21. Cleveland LR. 21.  1924. The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar. Biol. Bull. 46:177–225 [Google Scholar]
  22. Cleveland LR. 22.  1928. Further observations and experiments on the symbiosis between termites and their intestinal protozoa. Biol. Bull. 54:231–37 [Google Scholar]
  23. Cornette R, Gotoh H, Koshikawa S, Miura T. 23.  2008. Juvenile hormone titers and caste differentiation in the damp-wood termite Hodotermopsis sjostedti. J. Insect Physiol. 54:922–30 [Google Scholar]
  24. Cornette R, Koshikawa S, Hojo M, Matsumoto T, Miura T. 24.  2006. Caste-specific cytochrome P450 in the damp-wood termite Hodotermopsis sjostedti. Insect Mol. Biol. 15:235–44 [Google Scholar]
  25. Coy MR, Salem TZ, Denton JS, Kovaleva ES, Liu Z. 25.  et al. 2010. Phenol-oxidizing laccases from the termite gut. Insect Biochem. Mol. Biol. 40:723–32 [Google Scholar]
  26. Eger JE Jr, Lees MD, Neese PA, Atkinson TH, Thoms EM. 26.  et al. 2012. Elimination of subterranean termite colonies using a refined cellulose bait matrix containing noviflumuron when monitored and replenished quarterly. J. Econ. Entomol. 105:533–39 [Google Scholar]
  27. Elliott KL, Hehman GL, Stay B. 27.  2009. Isolation of the gene for the precursor of Phe-Gly-Leu-amide allatostatins in the termite Reticulitermes flavipes. Peptides 30:855–60 [Google Scholar]
  28. Eutick ML, Veivers P, O'Brien RW, Slaytor M. 28.  1978. Dependence of the higher termite, Nasutitermes exitiosus and the lower termite, Coptotermes lacteus on their gut flora. J. Insect Physiol. 24:363–68 [Google Scholar]
  29. Gao Q, Tancredi SE, Thompson GJ. 29.  2012. Identification of mycosis-related genes in the eastern subterranean termite by suppression subtractive hybridization. Arch. Insect Biochem. Physiol. 80:63–76 [Google Scholar]
  30. Geib SM, Filley TR, Hatcher PG, Hoover K, Carlson JE. 30.  et al. 2008. Lignin degradation in wood-feeding insects. Proc. Natl. Acad. Sci. USA 105:12932–37 [Google Scholar]
  31. Hamilton C, Bulmer MS. 31.  2012. Molecular antifungal defenses in subterranean termites: RNA interference reveals in vivo roles of termicins and GNBPs against a naturally encountered pathogen. Dev. Comp. Immunol. 36:372–77 [Google Scholar]
  32. Hamilton C, Lay F, Bulmer MS. 32.  2011. Subterranean termite prophylactic secretions and external antifungal defenses. J. Insect. Physiol. 57:259–1266 [Google Scholar]
  33. Hamm RL, DeMark JJ, Chin-Heady E, Tolley MP. 33.  2013. Consumption of a durable termite bait matrix by subterranean termites and resulting insecticidal activity. Pest Manag. Sci. 69:507–11 [Google Scholar]
  34. Han Q, Liu N, Robinson H, Cao L, Qian C. 34.  et al. 2013. Biochemical characterization and crystal structure of a GH10 xylanase from termite gut bacteria reveal a novel structural feature and significance of its bacterial Ig-like domain. Biotechnol. Bioeng. 110:3093–103 [Google Scholar]
  35. Hanus R, Vrkoslav V, Hrdý I, Cvacka J, Sobotník J. 35.  2010. Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. Proc. Biol. Sci. 277:995–1002 [Google Scholar]
  36. Hattori A, Sugime Y, Sasa C, Miyakawa H, Ishikawa Y. 36.  et al. 2013. Soldier morphogenesis in the damp-wood termite is regulated by the insulin signaling pathway. J. Exp. Zool. B 320:295–306 [Google Scholar]
  37. Hayashi Y, Lo N, Miyata H, Kitade O. 37.  2007. Sex-linked genetic influence on caste determination in a termite. Science 318:985–87 [Google Scholar]
  38. Hayashi Y, Shigenobu S, Watanabe D, Toga K, Saiki R. 38.  et al. 2013. Construction and characterization of normalized cDNA libraries by 454 pyrosequencing and estimation of DNA methylation levels in three distantly related termite species. PLOS ONE 8:e76678 [Google Scholar]
  39. Himuro C, Yokoi T, Matsuura K. 39.  2011. Queen-specific volatile in a higher termite Nasutitermes takasagoensis. J. Insect Physiol. 57:962–65 [Google Scholar]
  40. Hirayama K, Watanabe H, Tokuda G, Kitamoto K, Arioka M. 40.  2010. Purification and characterization of termite endogenous β-1,4-endoglucanases produced in Aspergillus oryzae. Biosci. Biotechnol. Biochem. 74:1680–86 [Google Scholar]
  41. Hongoh Y. 41.  2011. Toward the functional analysis of uncultivable, symbiotic microorganisms in the termite gut. Cell. Mol. Life Sci. 68:1311–25 [Google Scholar]
  42. Howard RW, Haverty MI. 42.  1979. Comparison of feeding substrates for evaluating effects of insect growth regulators on subterranean termites. J. Ga. Entomol. Soc. 14:3–7 [Google Scholar]
  43. Howard RW, Haverty MI. 43.  1979. Termites and juvenile hormone analogs: a review of methodology and observed effects. Sociobiology 4:269–78 [Google Scholar]
  44. Hrdý I. 44.  1985. The role of juvenile hormone and juvenoids in soldier formation in Rhinotermitidae. Caste Differentiation in Social Insects JAL Watson, BM Okot-Kotber, C Noirot 245–49 Oxford, NY: Pergamon [Google Scholar]
  45. Hrdý I, Kuldová J, Hanus R, Wimmer Z. 45.  2006. Juvenile hormone III, hydroprene and a juvenogen as soldier caste differentiation regulators in three Reticulitermes species: potential of juvenile hormone analogues in termite control. Pest Manag. Sci. 62:848–54 [Google Scholar]
  46. Hrdý I, Kuldová J, Wimmer Z. 46.  2004. Juvenogens as potential agents in termite control: laboratory screening. Pest Manag. Sci. 60:1035–42 [Google Scholar]
  47. Hungate RE. 47.  1938. Studies on the nutrition of Zootermopsis II: the relative importance of the termite and the protozoa in wood digestion. Ecology 19:1–25 [Google Scholar]
  48. Hussain A, Li YF, Cheng Y, Liu Y, Chen CC, Wen SY. 48.  2013. Immune-related transcriptome of Coptotermes formosanus Shiraki workers: the defense mechanism. PLOS ONE 8:e69543 [Google Scholar]
  49. Husseneder C, Grace JK. 49.  2005. Genetically engineered termite gut bacteria (Enterobacter cloacae) deliver and spread foreign genes in termite colonies. Appl. Microbiol. Biotechnol. 68:360–67 [Google Scholar]
  50. Husseneder C, Grace JK, Oishi DE. 50.  2005. Use of genetically engineered Escherichia coli to monitor ingestion, loss, and transfer of bacteria in termites. Curr. Microbiol. 50:119–23 [Google Scholar]
  51. Husseneder C, Sethi A, Foil L, Delatte J. 51.  2010. Testing protozoacidal activity of ligand-lytic peptides against termite gut protozoa in vitro (protozoa culture) and in vivo (microinjection into termite hindgut). J. Vis. Exp. 46:2190 doi:10.3791/2190 [Google Scholar]
  52. Huvenne H, Smagghe G. 52.  2010. Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review. J. Insect Physiol. 56:227–35 [Google Scholar]
  53. Inoue T, Moriya S, Ohkuma M, Kudo T. 53.  2005. Molecular cloning and characterization of a cellulase gene from a symbiotic protist of the lower termite, Coptotermes formosanus. Gene 349:67–75 [Google Scholar]
  54. Itakura S, Murayama S, Kamata Y, Tanaka H, Enoki A. 54.  2009. RNA interference in symbiotic protists of the termite Coptotermes formosanus through ingestion of siRNA by the host termite. Sociobiology 54:77–87 [Google Scholar]
  55. Itakura S, Tatsuuma S, Teranishi T, Hashizume K, Kaneda M, Tanaka H. 55.  2012. RNA interference in the termite Reticulitermes speratus: a comparison of the effects of single siRNAs and a long dsRNA on the silencing of the hexamerin gene. Jpn. J. Environ. Entomol. Zool. 23:151–56 [Google Scholar]
  56. Johnson E. 56.  2009. Goodbye to carbon neutral: getting biomass footprints right. Environ. Impact Assess. Rev. 29:165–68 [Google Scholar]
  57. Ke J, Laskar DD, Chen S. 57.  2013. Tetramethylammonium hydroxide (TMAH) thermochemolysis for probing in situ softwood lignin modification in each gut segment of the termite. J. Agric. Food Chem. 61:1299–308 [Google Scholar]
  58. Ke J, Laskar DD, Singh D, Chen S. 58.  2011. In situ lignocellulosic unlocking mechanism for carbohydrate hydrolysis in termites: crucial lignin modification. Biotechnol. Biofuels 4:17 [Google Scholar]
  59. Korb J, Weil T, Hoffmann K, Foster KR, Rehli M. 59.  2009. A gene necessary for reproductive suppression in termites. Science 324:758 [Google Scholar]
  60. Koshikawa S, Cornette R, Matsumoto T, Miura T. 60.  2010. The homolog of Ciboulot in the termite (Hodotermopsis sjostedti): a multimeric β-thymosin involved in soldier-specific morphogenesis. BMC Dev. Biol. 10:63 [Google Scholar]
  61. Lange JP. 61.  2007. Lignocellulose conversion: an introduction to chemistry, process and economics. Biofuels Bioprod. Biorefin. 1:39–48 [Google Scholar]
  62. Lefeuve P, Bordereau C. 62.  1984. Soldier formation regulated by a primer pheromone from the soldier frontal gland in a higher termite, Nasutitermes lujae. Proc. Natl. Acad. Sci. USA 81:7665–68 [Google Scholar]
  63. Lin L, Qin G, Wei Y, Du L, Pang Z, Huang R. 63.  2009. [Saturation mutagenesis of three amino acid positions consisting of the active site of an endoglucanase from termite Coptotermes formosanus.]. Sheng Wu Gong Cheng Xue Bao 25:927–31 [Google Scholar]
  64. Liu Y, Henderson G, Mao L, Laine RA. 64.  2005. Effects of temperature and nutrition on juvenile hormone titers of Coptotermes formosanus. Ann. Entomol. Soc. Am. 98:732–37 [Google Scholar]
  65. Liu Y, Henderson G, Mao L, Laine RA. 65.  2005. Seasonal variation of juvenile hormone titers of the Formosan subterranean termite, Coptotermes formosanus. Environ. Entomol. 34:557–62 [Google Scholar]
  66. Lo N, Tokuda G, Watanabe H. 66.  2011. Evolution and function of endogenous termite cellulases. See Ref. 5 51–67
  67. Matsuura K. 67.  2001. Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92:20–26 [Google Scholar]
  68. Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L. 68.  2010. Identification of a pheromone regulating caste differentiation in termites. Proc. Natl. Acad. Sci. USA 107:12963–68 [Google Scholar]
  69. Matsuura K, Vargo EL, Kawatsu K, Labadie PE, Nakano H. 69.  et al. 2009. Queen succession through asexual reproduction in termites. Science 323:1687 [Google Scholar]
  70. Mauldin JK, Rich NM. 70.  1980. Effect of chlortetracycline and other antibiotics on protozoan numbers in the eastern subterranean termite. J. Econ. Entomol. 73:123–28 [Google Scholar]
  71. Misra JN, Vijayaraghavan PK. 71.  1956. Ethyl malonate—an inhibitor of termite cellulase. Curr. Sci. 25:229–30 [Google Scholar]
  72. Miura T, Scharf ME. 72.  2011. Molecular mechanisms underlying caste differentiation in termites. See Ref. 5 211–53
  73. Nakashima KI, Watanabe H, Saitoh H, Tokuda G, Azuma JI. 73.  2002. Dual cellulose digesting system of the wood feeding termite, Coptotermes formosanus. Insect Biochem. Mol. Biol. 32:777–84 [Google Scholar]
  74. Nambu Y, Tanaka H, Enoki A, Itakura S. 74.  2010. RNA interference in the termite Reticulitermes speratus: silencing of the hexamerin gene using a single 21 nucleotide small interfering RNA-promoted differentiation of nymph to nymphoid. Sociobiology 55:527–46 [Google Scholar]
  75. Ni J, Takehara M, Miyazawa M, Watanabe H. 75.  2007. Random exchanges of non-conserved amino acid residues among four parental termite cellulases by family shuffling improved thermostability. Protein Eng. Des. Sel. 20:535–42 [Google Scholar]
  76. Ni J, Takehara M, Watanabe H. 76.  2010. Identification of activity related amino acid mutations of a GH9 termite cellulase. Bioresour. Technol. 101:6438–43 [Google Scholar]
  77. Ni J, Tokuda G. 77.  2013. Lignocellulose-degrading enzymes from termites and their symbiotic microbiota. Biotechnol. Adv. 31:838–50 [Google Scholar]
  78. Nuss AB, Forschler BT, Crim JW, Brown MR. 78.  2008. Distribution of neuropeptide F-like immunoreactivity in the eastern subterranean termite, Reticulitermes flavipes. J. Insect Sci. 8:1–18 [Google Scholar]
  79. Nuss AB, Forschler BT, Crim JW, TeBrugge V, Pohl J, Brown MR. 79.  2010. Molecular characterization of neuropeptide F from the eastern subterranean termite Reticulitermes flavipes. Peptides 31:419–28 [Google Scholar]
  80. Ohkuma M. 80.  2003. Termite symbiotic systems: efficient bio-recycling of lignocellulose. Appl. Microbiol. Biotechnol. 61:1–9 [Google Scholar]
  81. Ohkuma M, Brune A. 81.  2011. Diversity, structure, and evolution of the termite gut microbial community. See Ref. 5 413–38
  82. Ohta M, Matsuura F, Henderson G, Laine RA. 82.  2007. Novel free ceramides as components of the soldier defense gland of the Formosan subterranean termite (Coptotermes formosanus). J. Lipid Res. 48:656–64 [Google Scholar]
  83. Okot-Kotber BM, Ujvary I, Mollaaghahaba R, Szurdoki F, Matolcsy G, Prestwich GD. 83.  1991. Physiological influence on fenoxycarb pro-insecticides and soldier head extracts of various termite species on soldier differentiation in Reticulitermes flavipes. Sociobiology 19:77–89 [Google Scholar]
  84. Parman V, Vargo EL. 84.  2010. Colony-level effects of imidacloprid in subterranean termites. J. Econ. Entomol. 103:791–98 [Google Scholar]
  85. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J. 85.  et al. 2006. The path forward for biofuels and biomaterials. Science 311:484–89 [Google Scholar]
  86. Ramakrishnan R, Suiter DR, Nakatsu CH, Humber RD, Bennett GW. 86.  1999. Imidacloprid-enhanced Reticulitermes flavipes susceptibility to the entomopathogen Metarhizium anisopliae. J. Econ. Entomol. 92:1125–32 [Google Scholar]
  87. Rashamuse K, Mabizela-Mokoena N, Sanyika TW, Mabvakure B, Brady D. 87.  2012. Accessing carboxylesterase diversity from termite hindgut symbionts through metagenomics. J. Mol. Microbiol. Biotechnol. 22:277–86 [Google Scholar]
  88. Rashamuse K, Ronneburg T, Sanyika W, Mathiba K, Mmutlane E, Brady D. 88.  2014. Metagenomic mining of feruloyl esterases from termite enteric flora. Appl. Microbiol. Biotechnol. 98:727–37 [Google Scholar]
  89. Raychoudhury R, Sen R, Cai Y, Sun Y, Lietze VU. 89.  et al. 2013. Comparative metatranscriptomic signatures of wood and paper feeding in the gut of the termite Reticulitermes flavipes. Insect Mol. Biol. 22:155–71 [Google Scholar]
  90. Rosengaus RB, Traniello JFA, Bulmer MS. 90.  2011. Ecology, behavior and evolution of disease resistance in termites. See Ref. 5 165–91
  91. Saran RK, Rust MK. 91.  2007. Toxicity, uptake, and transfer efficiency of fipronil in western subterranean termite. J. Econ. Entomol. 100:495–508 [Google Scholar]
  92. Sasagawa T, Matsui M, Kobayashi Y, Otagiri M, Moriya S. 92.  et al. 2011. High-throughput recombinant gene expression systems in Pichia pastoris using newly developed plasmid vectors. Plasmid 65:65–69 [Google Scholar]
  93. Sasaguri S, Maruyama J, Moriya S, Kudo T, Kitamoto K, Arioka M. 93.  2008. Codon optimization prevents premature polyadenylation of heterologously-expressed cellulases from termite-gut symbionts in Aspergillus oryzae. J. Gen. Appl. Microbiol. 54:343–51 [Google Scholar]
  94. Scharf ME. 94.  2008. Silent pesticides. Chem. Ind. Mag. 11:20–23 [Google Scholar]
  95. Scharf ME, Boucias DG. 95.  2010. Potential of termite-based biomass pre-treatment strategies for use in bioethanol production. Insect Sci. 17:166–74 [Google Scholar]
  96. Scharf ME, Buckspan CE, Grzymala TL, Zhou X. 96.  2007. Regulation of polyphenic caste differentiation in the termite Reticulitermes flavipes by interaction of intrinsic and extrinsic factors. J. Exp. Biol. 210:4390–98 [Google Scholar]
  97. Scharf ME, Karl ZJ, Sethi A, Boucias DG. 97.  2011. Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLOS ONE 6:e21709 [Google Scholar]
  98. Scharf ME, Karl ZJ, Sethi A, Sen R, Raychoudhury R, Boucias DG. 98.  2011. Defining host-symbiont collaboration in termite lignocellulose digestion: the view from the tip of the iceberg. Commun. Int. Biol. 4:761–63 [Google Scholar]
  99. Scharf ME, Kovaleva ES, Jadhao S, Campbell JH, Buchman GW, Boucias DG. 99.  2010. Functional and translational analyses of a beta-glucosidase gene (glycosyl hydrolase family 1) isolated from the gut of the lower termite Reticulitermes flavipes. Insect Biochem. Mol. Biol. 40:611–20 [Google Scholar]
  100. Scharf ME, Ratliff CR, Hoteling JT, Bennett GW. 100.  2003. Caste differentiation responses of two sympatric Reticulitermes termite species to juvenile hormone homologs and synthetic juvenoids in two laboratory assays. Insectes Soc. 50:346–54 [Google Scholar]
  101. Scharf ME, Tartar A. 101.  2008. Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod. Biorefin. 2:540–52 [Google Scholar]
  102. Schwinghammer MA, Zhou X, Kambhampati S, Bennett GW, Scharf ME. 102.  2011. A novel gene from the takeout family involved in termite trail-following behavior. Gene 474:12–21 [Google Scholar]
  103. Sen R, Raychoudhury R, Cai Y, Sun Y, Lietze VU, Boucias DG, Scharf ME. 103.  2013. Differential impacts of juvenile hormone, soldier head extract and alternate caste phenotypes on host and symbiont transcriptome composition in the gut of the termite Reticulitermes flavipes. BMC Genomics 14:491 [Google Scholar]
  104. Sethi A, Kovaleva ES, Slack JM, Brown S, Buchman GW, Scharf ME. 104.  2013. A GHF7 cellulase from the protist symbiont community of Reticulitermes flavipes enables more efficient lignocellulose processing by host enzymes. Arch. Insect Biochem. Physiol. 84:175–93 [Google Scholar]
  105. Sethi A, Scharf ME. 105.  2013. Biofuels: fungal, bacterial degraders of lignocellulose. Encyclopedia of Life Sciences: Microbiology Chichester: Wiley & Sons [Google Scholar]
  106. Sethi A, Slack JM, Kovaleva ES, Buchman GW, Scharf ME. 106.  2013. Lignin-associated metagene expression in a lignocellulose-digesting termite. Insect Biochem. Mol. Biol. 43:91–101 [Google Scholar]
  107. Shelton TG. 107.  2013. The influence of fipronil on Reticulitermes flavipes feeding beyond treated plots. J. Econ. Entomol. 106:2160–66 [Google Scholar]
  108. Spomer NA, Kamble ST. 108.  2006. Temperature effect on kinetics of uptake, transfer, and clearance of [14C] noviflumuron in eastern subterranean termites (Isoptera: Rhinotermitidae). J. Econ. Entomol. 99:134–40 [Google Scholar]
  109. Sreerama L, Veerabhadrappa PS. 109.  1993. Isolation and properties of carboxylesterases of the termite gut-associated fungus, Xylaria nigripes. k., and their identity from the host termite, Odontotermes horni. w., mid-gut carboxylesterases. Int. J. Biochem. 25:1637–51 [Google Scholar]
  110. Sun Q, Zhou X. 110.  2013. Corpse management in social insects. Int. J. Biol. Sci. 9:313–21 [Google Scholar]
  111. Tartar A, Wheeler MM, Zhou X, Coy MR, Boucias DG, Scharf ME. 111.  2009. Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite R. flavipes. Biotechnol. Biofuels 2:25 [Google Scholar]
  112. Tarver MR, Coy MR, Scharf ME. 112.  2012. Cyp15F1: a novel cytochrome P450 gene linked to juvenile hormone-dependent caste differentiation in the termite Reticulitermes flavipes. Arch. Insect Biochem. Physiol. 80:92–108 [Google Scholar]
  113. Tarver MR, Florane CB, Zhang D, Grimm C, Lax AR. 113.  2012. Methoprene and temperature effects on caste differentiation and protein composition in the Formosan subterranean termite, Coptotermes formosanus. Insect Sci. 12:18 [Google Scholar]
  114. Tarver MR, Schmelz EA, Rocca JR, Scharf ME. 114.  2009. Effects of soldier-derived terpenes on soldier caste differentiation in the termite Reticulitermes flavipes. J. Chem. Ecol. 35:256–64 [Google Scholar]
  115. Tarver MR, Schmelz EA, Scharf ME. 115.  2011. Soldier caste influences on candidate primer pheromone levels and juvenile hormone-dependent caste differentiation in workers of the termite Reticulitermes flavipes. J. Insect Physiol. 57:771–77 [Google Scholar]
  116. Tarver MR, Zhou X, Scharf ME. 116.  2010. Socio-environmental and endocrine influences on developmental and caste-regulatory gene expression in the eusocial termite Reticulitermes flavipes. BMC Mol. Biol. 11:28 [Google Scholar]
  117. Terrapon N, Li C, Robertson HM, Ji L, Meng X. 117.  et al. 2014. Molecular traces of alternative social organization in a termite genome. Nat. Commun. 5:3636 [Google Scholar]
  118. Thompson GJ, Crozier YC, Crozier RH. 118.  2003. Isolation and characterization of a termite transferrin gene up-regulated on infection. Insect Mol. Biol. 12:1–7 [Google Scholar]
  119. Todaka N, Inoue T, Saita K, Ohkuma M, Nalepa CA. 119.  et al. 2010. Phylogenetic analysis of cellulolytic enzyme genes from representative lineages of termites and a related cockroach. PLOS ONE 5:e8636 [Google Scholar]
  120. Todaka N, Lopez CM, Inoue T, Saita K, Maruyama J. 120.  et al. 2010. Heterologous expression and characterization of an endoglucanase from a symbiotic protist of the lower termite, Reticulitermes speratus. Appl. Biochem. Biotechnol. 160:1168–78 [Google Scholar]
  121. Todaka N, Moriya S, Saita K, Hondo T, Kiuchi I. 121.  et al. 2007. Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiol. Ecol. 59:592–99 [Google Scholar]
  122. Todaka N, Nakamura R, Moriya S, Ohkuma M, Kudo T. 122.  et al. 2011. Screening of optimal cellulases from symbiotic protists of termites through expression in the secretory pathway of Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 75:2260–63 [Google Scholar]
  123. Toga K, Hojo M, Miura T, Maekawa K. 123.  2009. Presoldier induction by a juvenile hormone analog in the nasute termite Nasutitermes takasagoensis. Zool. Sci. 26:382–28 [Google Scholar]
  124. Toga K, Hojo M, Miura T, Maekawa K. 124.  2012. Expression and function of a limb-patterning gene Distal-less in the soldier-specific morphogenesis in the nasute termite Nasutitermes takasagoensis. Evol. Dev. 14:286–95 [Google Scholar]
  125. Toga K, Saiki R, Maekawa K. 125.  2013. Hox gene Deformed is likely involved in mandibular regression during presoldier differentiation in the nasute termite Nasutitermes takasagoensis. J. Exp. Zool. B 320:385–92 [Google Scholar]
  126. Uchima CA, Arioka M. 126.  2012. Expression and one-step purification of recombinant proteins using an alternative episomal vector for the expression of N-tagged heterologous proteins in Pichia pastoris. Biosci. Biotechnol. Biochem. 76:368–71 [Google Scholar]
  127. Uchima CA, Tokuda G, Watanabe H, Kitamoto K, Arioka M. 127.  2011. Heterologous expression and characterization of a glucose-stimulated β-glucosidase from the termite Neotermes koshunensis in Aspergillus oryzae. Appl. Microbiol. Biotechnol. 89:1761–71 [Google Scholar]
  128. 128. US Environ. Prot. Agency 2011. Pesticides: policies concerning products containing nanoscale materials. Fed. Regist. 76:11735383–95 [Google Scholar]
  129. Vargo EL, Parman V. 129.  2012. Effect of fipronil on subterranean termite colonies in the field. J. Econ. Entomol. 105:523–32 [Google Scholar]
  130. Vasan PT, Piriya PS, Prabhu DI, Vennison SJ. 130.  2011. Cellulosic ethanol production by Zymomonas mobilis harboring an endoglucanase gene from Enterobacter cloacae. Bioresour. Technol. 102:2585–89 [Google Scholar]
  131. Wang Q, Qian C, Zhang XZ, Liu N, Yan X, Zhou Z. 131.  2012. Characterization of a novel thermostable β-glucosidase from a metagenomic library of termite gut. Enzyme Microb. Technol. 51:319–24 [Google Scholar]
  132. Warnecke F, Luginbühl P, Ivanova N, Ghassemian M, Richardson TH. 132.  et al. 2007. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–65 [Google Scholar]
  133. Watanabe H, Noda H, Lo NA. 133.  1998. A cellulase gene of termite origin. Nature 394:330–31 [Google Scholar]
  134. Watanabe H, Tokuda G. 134.  2010. Cellulolytic systems in insects. Annu. Rev. Entomol. 55:609–32 [Google Scholar]
  135. Wheeler MM, Tarver MR, Coy MR, Scharf ME. 135.  2010. Characterization of four esterase genes and esterase activity from the gut of the termite Reticulitermes flavipes. Arch. Insect Biochem. Physiol. 73:30–48 [Google Scholar]
  136. Wimmer Z, Jurcek O, Jedlicka P, Hanus R, Kuldová J. 136.  et al. 2007. Insect pest management agents: hormonogen esters (juvenogens). J. Agric. Food Chem. 55:7387–93 [Google Scholar]
  137. Wimmer Z, Saman D, Kuldová J, Hrdý I, Bennettová B. 137.  2002. Fatty acid esters of juvenoid alcohols as insect hormonogen agents (juvenogens). Bioorg. Med. Chem. 10:1305–12 [Google Scholar]
  138. Yang B, Wyman CE. 138.  2008. Pretreatment: the key to unlocking low-cost cellulosic ethanol. Biofuels Bioprod. Bioref. 2:26–40 [Google Scholar]
  139. Zhang D, Allen AB, Lax AR. 139.  2012. Functional analyses of the digestive β-glucosidase of Formosan subterranean termites (Coptotermes formosanus). J. Insect Physiol. 58:205–10 [Google Scholar]
  140. Zhang D, Lax AR, Bland JM, Allen AB. 140.  2011. Characterization of a new endogenous endo-β-1,4-glucanase of Formosan subterranean termite (Coptotermes formosanus). Insect Biochem. Mol. Biol. 41:211–18 [Google Scholar]
  141. Zhang D, Lax AR, Raina AK, Bland JM. 141.  2009. Differential cellulolytic activity of native-form and C-terminal tagged-form cellulase derived from Coptotermes formosanus and expressed in E. coli. Insect Biochem. Mol. Biol. 39:516–22 [Google Scholar]
  142. Zhou X, Kovaleva ES, Wu-Scharf D, Campbell JH, Buchman GW. 142.  et al. 2010. Production and characterization of a recombinant beta-1,4-endoglucanase (glycohydrolase family 9) from the termite Reticulitermes flavipes. Arch. Insect Biochem. Physiol. 74:147–62 [Google Scholar]
  143. Zhou X, Oi FM, Scharf ME. 143.  2006. Social exploitation of hexamerin: RNAi reveals a major caste-regulatory factor in termites. Proc. Natl. Acad. Sci. USA 103:4499–504 [Google Scholar]
  144. Zhou X, Smith JA, Oi FM, Koehler PG, Bennett GW, Scharf ME. 144.  2007. Correlation of cellulase gene expression and cellulolytic activity throughout the gut of the termite R. flavipes. Gene 395:29–39 [Google Scholar]
  145. Zhou X, Tarver MR, Bennett GW, Oi FM, Scharf ME. 145.  2006. Two hexamerin genes from the termite Reticulitermes flavipes: sequence, expression, and proposed functions in caste regulation. Gene 376:47–58 [Google Scholar]
  146. Zhou X, Tarver MR, Scharf ME. 146.  2007. Hexamerin-based regulation of juvenile hormone-dependent gene expression underlies phenotypic plasticity in a social insect. Development 134:601–10 [Google Scholar]
  147. Zhou X, Wheeler MM, Oi FM, Scharf ME. 147.  2008. Inhibition of termite cellulases by carbohydrate-based cellulase inhibitors: evidence from in vitro biochemistry and in vivo feeding studies. Pestic. Biochem. Physiol. 90:31–41 [Google Scholar]
  148. Zhou X, Wheeler MM, Oi FM, Scharf ME. 148.  2008. RNA interference in the termite Reticulitermes flavipes by ingestion of double-stranded RNA. Insect Biochem. Mol. Biol. 38:805–15 [Google Scholar]
  149. Zhu BC, Henderson G, Laine RA. 149.  2005. Screening method for inhibitors against Formosan subterranean termite β-glucosidases in vivo. J. Econ. Entomol. 98:41–46 [Google Scholar]

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