The impact of microbial symbionts on host plant utilization by herbivorous insects

Molecular Ecology

Volumn 23, Issue 6, 2014, Pages 1473-1496

  Hansen, Allison K ^a   Moran, Nancy A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Buchnera; coevolution; gut microbiota; insect nutrition; insect plant microbe interaction; intracellular symbiont

Indexed keywords

APHIDIDAE; HEXAPODA;

AMINO ACID;

ANIMAL; ARTICLE; BACTERIAL GENOME; BUCHNERA; COEVOLUTION; DIGESTIVE SYSTEM; GENETICS; HERBIVORY; HOST RANGE; INSECT; INSECT NUTRITION; INSECT-PLANT-MICROBE INTERACTION; INTESTINE FLORA; INTRACELLULAR SYMBIONT; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SYMBIOSIS;

BUCHNERA; COEVOLUTION; GUT MICROBIOTA; INSECT NUTRITION; INSECT-PLANT-MICROBE INTERACTION; INTRACELLULAR SYMBIONT;

AMINO ACIDS; ANIMALS; BUCHNERA; DIGESTIVE SYSTEM; GENOME, BACTERIAL; HERBIVORY; HOST SPECIFICITY; INSECTS; SYMBIOSIS;

EID: 84896338635     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12421     Document Type: Article

References (222)

1. Acuña R, Padilla BE, Flõrez-Ramos CP, et al,. (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proceedings of the National Academy of Sciences, USA, 109, 4197-4202.
2. Adams AS, Aylward FO, Adams SM, et al,. (2013) Mountain pine beetles colonizing historical and naïve host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Applied and Environmental Microbiology, 61, 759-768.
3. Akman Gündüz E, Douglas AE, (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. Proceedings of the Royal Society B: Biological Sciences, 276, 987-991.
4. Altincicek B, Kovacs JL, Gerardo NM, (2012) Horizontally transferred fungal carotenoid genes in the two-spotted spider mite Tetranychus urticae. Biology Letters, 8, 253-257.
5. Andersen PC, Brodbeck BV, Mizell RF, (1989) Metabolism of amino acids, organic acids and sugars extracted from the xylem fluid of four host plants by adult Homalodisca coagulata. Entomologia Experimentalis et Applicata, 503, 149-159.
6. Andersen PC, Brodbeck BV, Mizell RF III, (1992) Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. Journal of Insect Physiology, 38, 611-622.
7. Andert J, Marten A, Brandl R, Brune A, (2010) Inter- and intraspecific comparison of the bacterial assemblages in the hindgut of humivorous scarab beetle larvae (Pachnoda spp.). FEMS Microbiology Ecology, 74, 439-449.
8. Andrews RE, Spence KD, (1980) Action of douglas fir tussock moth larvae and their microflora on dietary terpenes. Applied and Environmental Microbiology, 40, 959-963.
9. Aylward FO, Burnum KE, Scott JJ, et al,. (2012a) Metagenomic and metaproteomic insights into bacterial communities in leaf-cutter ant fungus gardens. The ISME Journal, 6, 1688-1701.
10. Aylward FO, Currie CR, Suen G, (2012b) The evolutionary innovation of nutritional symbioses in leaf-cutter ants. Insects, 3, 41-61.
11. Barbosa P, Krischik VA, Jones CG, (1991) Microbial Mediation of Plant-Herbivore Interactions. Wiley-Interscience, New York, NY.
12. Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE, (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS One, 5, e11339.
13. Baumann P, (2005) Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology, 59, 155-189.
14. Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW, (2004) Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters, 8, 70-79.
15. Berenbaum MR, (1988) Allelochemicals in insect-microbe-plant Interactions; agents provocateurs in the coevolutionary arms race. In: Novel Aspects of Insect-Plant Interactions (eds, Barbosa P, Letourneau DK,), pp. 97-123. Wiley-Interscience, New York, NY.
16. Bernays EA, Chapman RF, (1994) Host Plant Selection by Phytophagous Insects (Contemporary Topics in Entomology). Springer, New York, NY.
17. Bissett J, Borkent A, (1988) Coevolution of Fungi with Plants and Animals. Academic Press, New York, NY.
18. Bourgis F, Roje S, Nuccio ML, et al,. (1999) S-methylmethionine plays a major role in phloem sulfur transport and is synthesized by a novel type of methyltransferase. The Plant Cell, 11, 1485-1497.
19. Braendle C, Miura T, Bickel R, et al,. (2003) Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLoS Biology, 1, E21.
20. Bressan A, Terlizzi F, Credi R, (2012) Independent origins of vectored plant pathogenic bacteria from arthropod-associated Arsenophonus endosymbionts. Microbial Ecology, 63, 628-638.
21. Brodbeck BV, Mizell RF III, French WJ, Andersen PC, Aldrich JH, (1990) Amino acids as determinants of host preference for the xylem feeding leafhopper, Homalodisca coagulata (Homoptera: Cicadellidae). Oecologia, 83, 338-345.
22. Broderick NA, Raffa KF, Goodman RM, Handelsman J, (2004) Census of the bacterial community of the gypsy moth larval midgut by using culturing and culture-independent methods. Applied and Environmental Microbiology, 70, 293-300.
23. Broderick NA, Robinson CJ, McMahon MD, et al,. (2009) Contributions of gut bacteria to Bacillus thuringiensis-induced mortality vary across a range of Lepidoptera. BMC Biology, 7, 11.
24. Buchner P, (1965) Endosymbiosis of Animals with Plant Microorganisms. Interscience Publishers/John Wiley, New York, NY.
25. Buchner P, Takahashi H, Hawkesford MJ, (2004) Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. Journal of Experimental Botany, 55, 1765-1773.
26. Caillaud MC, Via S, (2000) Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. The American Naturalist, 156, 606-621.
27. Caillaud MC, Via S, (2012) Quantitative genetics of feeding behavior in two ecological races of the pea aphid, Acyrthosiphon pisum. Heredity, 108, 211-218.
28. Calderõn-Cortés N, Quesada M, Watanabe H, Cano-Camacho H, Oyama K, (2012) Endogenous plant cell wall digestion: a key mechanism in insect evolution. Annual Review of Ecology, Evolution, and Systematics, 43, 45-71.
29. Caspi-Fluger A, Inbar M, Mozes-Daube N, et al,. (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proceedings of the Royal Society B: Biological Sciences, 279, 1791-1796.
30. Casteel CL, Hansen AK, Walling LL, Paine TD, (2012) Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter psyllaurous. PLoS One, 7, e35191.
31. Charles H, Calevro F, Viñuelas J, Fayard J-M, Rahbé Y, (2006) Codon usage bias and tRNA over-expression in Buchnera aphidicola after aromatic amino acid nutritional stress on its host Acyrthosiphon pisum. Nucleic Acids Research, 34, 4583-4592.
32. Clark EL, Karley AJ, Hubbard SF, (2010) Insect endosymbionts: manipulators of insect herbivore trophic interactions? Protoplasma, 244, 25-51.
33. Cobbs C, Heath J, Stireman JO, Abbot P, (2013) Carotenoids in unexpected places: Gall midges, lateral gene transfer and carotenoid biosynthesis in animals. Molecular Phylogenetics and Evolution, 68, 221-228.
34. Colman DR, Toolson EC, Takacs-Vesbach CD, (2012) Do diet and taxonomy influence insect gut bacterial communities? Molecular Ecology, 21, 5124-5137.
35. Conord C, Despres L, Vallier A, et al,. (2008) Long-term evolutionary stability of bacterial endosymbiosis in Curculionoidea: additional evidence of symbiont replacement in the Dryophthoridae family. Molecular Biology and Evolution, 25, 859-868.
36. Craig JP, Bekal S, Hudson M, et al,. (2008) Analysis of a horizontally transferred pathway involved in vitamin B6 biosynthesis from the soybean cyst nematode Heterodera glycines. Molecular Biology and Evolution, 25, 2085-2098.
37. Cryan JR, Urban JM, (2012) Higher-level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic? Systematic Entomology, 37, 7-21.
38. Danchin EGJ, Rosso M-N, Vieira P, et al,. (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proceedings of the National Academy of Sciences, USA, 107, 17651-17656.
39. De Fine Licht HH, Schiott M, Mueller UG, Boomsa JJ, (2010) Evolutionary transitions in enzyme activity of ant fungus gardens. Evolution, 64, 2055-2069.
40. De Fine Licht HH, Schiøtt M, Rogowska-Wrzesinska A, et al,. (2013) Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proceedings of the National Academy of Sciences, USA, 110, 583-587.
41. Degnan PH, Ochman H, Moran NA, (2011) Sequence conservation and functional constraint on intergenic spacers in reduced genomes of the obligate symbiont Buchnera. PLoS Genetics, 7, e1002252.
42. D'Ettorre P, Mora P, Dibangou V, Rouland C, Errard C, (2002) The role of the symbiotic fungus in the digestive metabolism of two species of fungus-growing ants. Journal of Comparative Physiology B, Biochemical, Systemic, and Environmental Physiology, 172, 169-176.
43. DiGuistini S, Wang Y, Liao NY, et al,. (2011) Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen. Proceedings of the National Academy of Sciences, USA, 108, 2504-2509.
44. Dillon R, Charnley K, (2002) Mutualism between the desert locust Schistocerca gregaria and its gut microbiota. Research in Microbiology, 153, 503-509.
45. Douglas AE, (1988) Sulphate utilization in an aphid symbiosis. Insect Biochemistry, 18, 599-605.
46. Douglas AE, (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology, 43, 17-37.
47. Douglas AE, Dixon AFG, (1987) The mycetocyte symbiosis of aphids: variation with age and morph in virginoparae of Megoura viciae and Acyrthosiphon pisum. Journal of Insect Physiology, 33, 109-113.
48. Douglas AE, Prosser WA, (1992) Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. Journal of Insect Physiology, 38, 565-568.
49. Douglas AE, Bouvaine S, Russell RR, (2011) How the insect immune system interacts with an obligate symbiotic bacterium. Proceedings of the Royal Society B: Biological Sciences, 278, 333-338.
50. Dowd PF, Shen SK, (2011) The contribution of symbiotic yeast to toxin resistance of the cigarette beetle (Lasioderma serricorne). Entomologia Experimentalis et Applicata, 56, 241-248.
51. Downie DA, Gullan PJ, (2005) Phylogenetic congruence of mealybugs and their primary endosymbionts. Journal of Evolutionary Biology, 18, 315-324.
52. Egert M, Wagner B, Lemke T, Brune A, Friedrich MW, (2003) Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae). Applied and Environmental Microbiology, 69, 6659-6668.
53. Engel P, Martinson VG, Moran NA, (2012) Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences, USA, 109, 11002-11007.
54. Erthal M, Silva CP, Cooper RM, Samuels RI, (2009) Hydrolytic enzymes of leaf-cutting ant fungi. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 152, 54-59.
55. Farrell B, (1998) "Inordinate Fondness" explained: why are there so many beetles? Science, 281, 555-559.
56. Febvay GR, Liadouze I, Guillaud J, Bonnot G, (1995) Analysis of energetic amino acid metabolism in Acyrthosiphon pisum: a multidimensional approach to amino acid metabolism in aphids. Archives of Insect Biochemistry and Physiology, 29, 45-69.
57. Feldhaar H, (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecological Entomology, 36, 533-543.
58. Felton GW, Tumlinson JH, (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Current Opinion in Plant Biology, 11, 457-463.
59. Fermaud M, Le Menn R, (1989) Association of Botrytis cinerea with grape berry moth larvae. Phytopathology, 79, 651-656.
60. Fermaud M, Le Menn R, (1992) Transmission of Botrytis cinerea to grapes by grape berry moth larvae. Phytopathology, 82, 1393-1398.
61. Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE, (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecological Entomology, 29, 60-65.
62. Ferrari J, Scarborough CL, Godfray HCJ, (2007) Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia, 153, 323-329.
63. Ferrari J, Via S, Godfray HCJ, (2008) Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution, 62, 2508-2524.
64. Ferrari J, West JA, Via S, Godfray HCJ, (2012) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution, 66, 375-390.
65. Frago E, Dicke M, Godfray HCJ, (2012) Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology and Evolution, 27, 705-711.
66. Fukatsu T, Hosokawa T, (2002) Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. Applied and Environmental Microbiology, 68, 389-396.
67. Futuyma DJ, Agrawal AA, (2009) Evolutionary history and species interactions. Proceedings of the National Academy of Sciences, USA, 106, 18043-18044.
68. Giron D, Kaiser W, Imbault N, Casas J, (2007) Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biology Letters, 3, 340-343.
69. Gomes De Siqueira C, Bacci M, Pagnocca F, Bueno O, Hebling M, (1998) Metabolism of plant polysaccharides by Leucoagaricus gongylophorus, the symbiotic fungus of the leaf-cutting ant Atta sexdens L. Applied and Environmental Microbiology, 64, 4820-4822.
70. Gosalbes MJ, Lamelas A, Moya A, Latorre A, (2008) The striking case of tryptophan provision in the cedar aphid Cinara cedri. Journal of Bacteriology, 190, 6026-6029.
71. Grbic̈ M, Van Leeuwen T, Clark RM, et al,. (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479, 487-492.
72. Grünwald S, Pilhofer M, Höll W, (2010) Microbial associations in gut systems of wood- and bark-inhabiting longhorned beetles [Coleoptera: Cerambycidae]. Systematic and Applied Microbiology, 33, 25-34.
73. Halbert SE, Manjunath KL, (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. The Florida Entomologist, 3, 330-353.
74. van Ham RCHJ, Kamerbeek J, Palacios C, et al,. (2003) Reductive genome evolution in Buchnera aphidicola. Proceedings of the National Academy of Sciences, USA, 100, 581-586.
75. Hansen AK, Moran NA, (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proceedings of the National Academy of Sciences, USA, 108, 2849-2854.
76. Hansen AK, Trumble JT, Stouthamer R, Paine TD, (2008) A new Huanglongbing Species, "Candidatus Liberibacter psyllaurous", found to infect tomato and potato, is vectored by the psyllid Bactericera cockerelli (Sulc). Applied and Environmental Microbiology, 74, 5862-5865.
77. Hansen AK, Vorburger C, Moran NA, (2012) Genomic basis of endosymbiont-conferred protection against an insect parasitoid. Genome Research, 22, 106-114.
78. Hawthorne DJ, Via S, (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature, 412, 904-907.
79. Heath JJ, Stireman JO III, (2010) Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea. Entomologia Experimentalis et Applicata, 137, 36-49.
80. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, (2008) Wolbachia and virus protection in insects. Science, 322, 702.
81. Hehemann J-H, Kelly AG, Pudlo NA, Martens EC, Boraston AB, (2012) Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proceedings of the National Academy of Sciences, USA, 109, 19786-19791.
82. Hölldobler B, Wilson EO, (2010) The Leafcutter Ants: Civilization by Instinct. W. W. Norton, New York, NY.
83. Hongoh Y, Sharma VK, Prakash T, et al,. (2008) Genome of an endosymbiont coupling N2 fixation to cellulolysis within protist cells in termite gut. Science, 322, 1108-1109.
84. Hosokawa T, Kikuchi Y, Nikoh N, Shimada M, Fukatsu T, (2006) Strict host-symbiont cospeciation and reductive genome evolution in insect gut bacteria. PLoS Biology, 4, e337.
85. Hosokawa T, Kikuchi Y, Nikoh N, Fukatsu T, (2012) Polyphyly of gut symbionts in stinkbugs of the family Cydnidae. Applied and Environmental Microbiology, 78, 4758-4761.
86. Howard JJ, (1988) Leafcutting and diet selection: relative influence of leaf chemistry and physical features. Ecology, 69, 250-260.
87. Hubbell SP, Wiemer DF, Adejare A, (1983) An antifungal terpenoid defends a neotropical tree (Hymenaea) against attack by fungus-growing ants (Atta). Oecologia, 60, 321-327.
88. Hubbell SP, Howard JJ, Wiemer DF, (1984) Chemical leaf repellency to an attine ant: seasonal distribution among potential host plant species. Ecology, 65, 1067-1076.
89. Jaenike J, Brekke TD, (2011) Defensive endosymbionts: a cryptic trophic level in community ecology. Ecology Letters, 14, 150-155.
90. Janson EM, Stireman JO, Singer MS, Abbot P, (2008) Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution, 62, 997-1012.
91. Janson EM, Grebenok RJ, Behmer ST, Abbot P, (2009) Same host-plant, different sterols: variation in sterol metabolism in an insect herbivore community. Journal of Chemical Ecology, 35, 1309-1319.
92. Janson EM, Peeden ER, Stireman JO III, Abbot P, (2010) Symbiont-mediated phenotypic variation without co-evolution in an insect-fungus association. Journal of Evolutionary Biology, 23, 2212-2228.
93. Jaquiéry J, Stoeckel S, Nouhaud P, et al,. (2012) Genome scans reveal candidate regions involved in the adaptation to host plant in the pea aphid complex. Molecular Ecology, 21, 5251-5264.
94. Joy JB, (2013) Symbiosis catalyses niche expansion and diversification. Proceedings of the Royal Society B: Biological Sciences, 280, 2212-2228.
95. Kaiser W, Huguet E, Casas J, Commin C, Giron D, (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proceedings of the Royal Society B: Biological Sciences, 277, 2311-2319.
96. Kelley LA, Sternberg MJE, (2009) Protein structure prediction on the web: a case study using the Phyre server. Nature Protocols, 4, 363-371.
97. Kikuchi Y, Meng X-Y, Fukatsu T, (2005) Gut symbiotic bacteria of the genus Burkholderia in the broad-headed bugs Riptortus clavatus and Leptocorisa chinensis (Heteroptera: Alydidae). Applied and Environmental Microbiology, 71, 4035-4043.
98. Kikuchi Y, Hosokawa T, Fukatsu T, (2010) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. The ISME Journal, 5, 446-460.
99. Kikuchi Y, Hosokawa T, Fukatsu T, (2011) Specific developmental window for establishment of an insect-microbe gut symbiosis. Applied and Environmental Microbiology, 77, 4075-4081.
100. Kikuchi Y, Hayatsu M, Hosokawa T, et al,. (2012) Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences, USA, 109, 8618-8622.
101. Kirsch R, Wielsch N, Vogel H, et al,. (2012) Combining proteomics and transcriptome sequencing to identify active plant-cell-wall-degrading enzymes in a leaf beetle. BMC Genomics, 13, 587.
102. Kluth S, Kruess A, Tscharntke T, (2002) Insects as vectors of plant pathogens: mutualistic and antagonistic interactions. Oecologia, 133, 193-199.
103. Kölsch G, Pedersen BV, (2010) Can the tight co-speciation between reed beetles (Col., Chrysomelidae, Donaciinae) and their bacterial endosymbionts, which provide cocoon material, clarify the deeper phylogeny of the hosts? Molecular Phylogenetics and Evolution, 54, 810-821.
104. Kono M, Koga R, Shimada M, Fukatsu T, (2008) Infection dynamics of coexisting Beta- and Gammaproteobacteria in the nested endosymbiotic system of mealybugs. Applied and Environmental Microbiology, 74, 4175-4184.
105. Kooij PW, Schiott M, Boomsma JJ, De Fine Licht HH, (2011) Rapid shifts in Atta cephalotes fungus-garden enzyme activity after a change in fungal substrate (Attini, Formicidae). Insectes Sociaux, 58, 145-151.
106. Kwong WK, Moran NA, (2012) Cultivation and characterization of the gut symbionts of honey bees and bumble bees: Snodgrassella alvi gen. nov., sp nov, a member of the Neisseriaceae family of the Betaproteobacteria; and Gilliamella apicola gen. nov., sp nov, a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the Enterobacteriales order of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, 63, 2008-2018.
107. Labandeira CC, Sepkoski JJ, (1993) Insect diversity in the fossil record. Science, 261, 310-315.
108. Lamelas A, Gosalbes MJ, Moya A, Latorre A, (2011) New clues about the evolutionary history of metabolic losses in bacterial endosymbionts, provided by the genome of Buchnera aphidicola from the aphid Cinara tujafilina. Applied and Environmental Microbiology, 77, 4446-4454.
109. Leonardo TE, (2004) Removal of a specialization-associated symbiont does not affect aphid fitness. Ecology Letters, 7, 461-468.
110. Leonardo TE, Muiru GT, (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proceedings of the Royal Society B: Biological Sciences, 270, S209-S212.
111. Li Z-W, Shen Y-H, Xiang Z-H, Zhang Z, (2011) Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects. BMC Evolutionary Biology, 11, 356.
112. Macdonald SJ, Thomas GH, Douglas AE, (2011) Genetic and metabolic determinants of nutritional phenotype in an insect-bacterial symbiosis. Molecular Ecology, 20, 2073-2084.
113. Macdonald SJ, Lin GG, Russell CW, Thomas GH, Douglas AE, (2012) The central role of the host cell in symbiotic nitrogen metabolism. Proceedings of the Royal Society B: Biological Sciences, 279, 2965-2973.
114. Martinson VG, Moy J, Moran NA, (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology, 78, 2830-2840.
115. Matsuura Y, Kikuchi Y, Hosokawa T, et al,. (2012) Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. The ISME Journal, 6, 397-409.
116. Mattson WJ Jr, (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics, 11, 119-161.
117. May RM, (1988) How many species are there on Earth? Science, 241, 1441-1449.
118. McClean APD, Oberholzer PCJ, (1965) Citrus psylla, a vector of the greening disease of Sweet Orange. South African Journal of Agricultural Science, 8, 297-298.
119. McCutcheon JP, Moran NA, (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proceedings of the National Academy of Sciences, USA, 104, 19392-19397.
120. McCutcheon JP, Moran NA, (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 million years of evolution. Genome Biology and Evolution, 2, 708-718.
121. McCutcheon JP, Moran NA, (2012) Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology, 10, 13-26.
122. McCutcheon JP, von Dohlen CD, (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Current Biology, 21, 1366-1372.
123. McCutcheon JP, McDonald BR, Moran NA, (2009) Convergent evolution of metabolic roles in bacterial co-symbionts of insects. Proceedings of the National Academy of Sciences, USA, 106, 15394-15399.
124. McFall-Ngai M, Hadfield MG, Bosch TCG, et al,. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences, USA, 110, 3229-3236.
125. McLean AHC, van Asch M, Ferrari J, Godfray HCJ, (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B: Biological Sciences, 278, 760-766.
126. Mitter C, Farrell B, Wiegmann B, (1988) The phylogenetic study of adaptive zones: has phytophagy promoted insect diversification? The American Naturalist, 132, 107-128.
127. Mittler TE, (1971) Dietary amino acid requirements of the aphid Myzus persicae affected by antibiotic uptake. The Journal of Nutrition, 101, 1023-1028.
128. Moller IE, De Fine Licht HH, Harholt J, Willats WGT, Boomsma JJ, (2011) The dynamics of plant cell-wall polysaccharide decomposition in leaf-cutting ant fungus gardens. PLoS One, 6, e17506.
129. Mondy N, Corio-Costet M-F, (2000) The response of the grape berry moth (Lobesia botrana) to a dietary phytopathogenic fungus (Botrytis cinerea): the significance of fungus sterols. Journal of Insect Physiology, 46, 1557-1564.
130. Mondy N, Charrier B, Fermaud M, Pracros P, Corio-Costet M-F, (1998) Mutualism between a phytopathogenic fungus (Botrytis cinerea) and a vineyard pest (Lobesia botrana). Positive effects on insect development and oviposition behaviour. Comptes Rendus de l'Académie des Sciences-Series III-Sciences de la Vie, 321, 665-671.
131. Montllor CB, Maxmen A, Purcell AH, (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.
132. Morales-Jiménez J, Zúñiga G, Villa-Tanaca L, Hernández-Rodríguez C, (2009) Bacterial community and nitrogen fixation in the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae: Scolytinae). Microbial Ecology, 58, 879-891.
133. Morales-Jiménez J, Zúñiga G, Ramírez-Saad HC, Hernández-Rodríguez C, (2012) Gut-associated bacteria throughout the life cycle of the bark beetle Dendroctonus rhizophagus Thomas and Bright (Curculionidae: Scolytinae) and their cellulolytic activities. Microbial Ecology, 64, 268-278.
134. Morales-Jiménez J, Vera-Ponce de Leõn A, García-Domínguez A, et al,. (2013) Nitrogen-fixing and uricolytic bacteria associated with the gut of Dendroctonus rhizophagus and Dendroctonus valens (Curculionidae: Scolytinae). Microbial Ecology, 66, 200-210.
135. Moran NA, (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proceedings of the National Academy of Sciences, USA, 104 (Suppl 1), 8627-8633.
136. Moran NA, Jarvik T, (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science, 328, 624-627.
137. Moran NA, Plague GR, Sandström JP, Wilcox JL, (2003) A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proceedings of the National Academy of Sciences, USA, 100 (Suppl 2), 14543-14548.
138. Moran NA, Tran P, Gerardo NM, (2005) Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Applied and Environmental Microbiology, 71, 8802-8810.
139. Moran NA, McCutcheon JP, Nakabachi A, (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42, 165-190.
140. Moran NA, Hansen AK, Powell JE, Sabree ZL, (2012) Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One, 7, e36393.
141. Mueller UG, (2012) Symbiont recruitment versus ant-symbiont co-evolution in the attine ant-microbe symbiosis. Current Opinion in Microbiology, 15, 269-277.
142. Munson MA, Baumann P, Clark MA, et al,. (1991) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. Journal of Bacteriology, 173, 6321-6324.
143. Nakabachi A, Yamashita A, Toh H, et al,. (2006) The 160-kilobase genome of the bacterial endosymbiont Carsonella. Science, 314, 267.
144. Nichols-Orians C, (1991a) Condensed tannins, attine ants, and the performance of a symbiotic fungus. Journal of Chemical Ecology, 17, 1177-1195.
145. Nichols-Orians C, (1991b) Differential effects of condensed and hydrolyzable tannin on polyphenol oxidase activity of attine symbiotic fungus. Journal of Chemical Ecology, 17, 1811-1819.
146. Nikoh N, Hosokawa T, Oshima K, Hattori M, Fukatsu T, (2011) Reductive evolution of bacterial genome in insect gut environment. Genome Biology and Evolution, 3, 702-714.
147. Nishikori K, Morioka K, Kubo T, Morioka M, (2009) Age- and morph-dependent activation of the lysosomal system and Buchnera degradation in aphid endosymbiosis. Journal of Insect Physiology, 55, 351-357.
148. Nygaard S, Zhang G, Schiøtt M, et al,. (2011) The genome of the leaf-cutting ant Acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming. Genome research, 21, 1339-1348.
149. Oliver KM, Russell JA, Moran NA, Hunter MS, (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences, USA, 100, 1803-1807.
150. Oliver KM, Moran NA, Hunter MS, (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences, USA, 102, 12795-12800.
151. Oliver KM, Degnan PH, Hunter MS, Moran NA, (2009) Bacteriophages encode factors required for protection in a symbiotic mutualism. Science, 325, 992-994.
152. Oliver KM, Degnan PH, Burke GR, Moran NA, (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 55, 247-266.
153. Paganini J, Campan-Fournier A, Da Rocha M, et al,. (2012) Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes. PLoS One, 7, e50875.
154. Paine TD, Raffa KF, Harrington TC, (1997) Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annual Review of Entomology, 42, 179-206.
155. Pauchet Y, Wilkinson P, Chauhan R, Ffrench-Constant RH, (2010) Diversity of beetle genes encoding novel plant cell wall degrading enzymes. PLoS One, 5, e15635.
156. Peccoud J, Simon J-C, McLaughlin HJ, Moran NA, (2009) Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proceedings of the National Academy of Sciences, USA, 106, 16315-16320.
157. Perez-Brocal V, Gil R, Ramos S, et al,. (2006) A small microbial genome: the end of a long symbiotic relationship? Science, 314, 312-313.
158. Pilon FM, Visôtto LE, Guedes RNC, Oliveira MGA, (2013) Proteolytic activity of gut bacteria isolated from the velvet bean caterpillar Anticarsia gemmatalis. Journal of Comparative Physiology B, Biochemical, Systemic, and Environmental Physiology Feb 8. [Epub ahead of print]. doi: 10.1007/s00360-013- 0744-5.
159. Poliakov A, Russell CW, Ponnala L, et al,. (2011) Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis. Molecular & Cellular Proteomics, 10, 110007039.
160. Prado SS, Golden M, Follett PA, Daugherty MP, Almeida RPP, (2009) Demography of gut symbiotic and aposymbiotic Nezara viridula L. (Hemiptera: Pentatomidae). Environmental Entomology, 38, 103-109.
161. Price DRG, Duncan RP, Shigenobu S, Wilson ACC, (2011) Genome expansion and differential expression of amino acid transporters at the aphid/Buchnera symbiotic interface. Molecular Biology and Evolution, 28, 3113-3126.
162. Raddadi N, Gonella E, Camerota C, et al,. (2011) "Candidatus Liberibacter europaeus" sp nov that is associated with and transmitted by the psyllid Cacopsylla pyri apparently behaves as an endophyte rather than a pathogen. Environmental Microbiology, 13, 414-426.
163. Raffa KF, Berryman AA, (1983) The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecological Monographs, 53, 27-49.
164. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N, (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environmental Microbiology, 12, 2885-2893.
165. Reid NM, Addison SL, Macdonald LJ, Lloyd-Jones G, (2011) Biodiversity of active and inactive bacteria in the gut flora of wood-feeding huhu beetle larvae (Prionoplus reticularis). Applied and Environmental Microbiology, 77, 7000-7006.
166. Reymond N, Calevro F, Viñuelas J, et al,. (2006) Different levels of transcriptional regulation due to trophic constraints in the reduced genome of Buchnera aphidicola APS. Applied and Environmental Microbiology, 72, 7760-7766.
167. Richard F-J, Mora P, Errard C, Rouland C, (2005) Digestive capacities of leaf-cutting ants and the contribution of their fungal cultivar to the degradation of plant material. Journal of Comparative Physiology B, Biochemical, Systemic, and Environmental Physiology, 175, 297-303.
168. Rio RVM, Wu Y-N, Filardo G, Aksoy S, (2006) Dynamics of multiple symbiont density regulation during host development: tsetse fly and its microbial flora. Proceedings of the Royal Society B: Biological Sciences, 273, 805-814.
169. Robert-Seilaniantz A, Navarro L, Bari R, Jones JD, (2007) Pathological hormone imbalances. Current Opinion in Plant Biology, 10, 372-379.
170. Robinson CJ, Schloss P, Ramos Y, Raffa K, Handelsman J, (2010) Robustness of the bacterial community in the cabbage white butterfly larval midgut. Microbial Ecology, 59, 199-211.
171. Rohfritsch O, (2008) Plants, gall midges, and fungi: a three-component system. Entomologia Experimentalis et Applicata, 128, 208-216.
172. Ryan CA, (1990) Protease inhibitors in plants: Genes for improving defenses against insects and pathogens. Annual Review of Phytopathology, 28, 425-449.
173. Sabree ZL, Huang CY, Okusu A, Moran NA, Normark BB, (2013) The nutrient-supplying capabilities of Uzinura, an endosymbiont of armoured scale insects. Environmental Microbiology, 15, 1988-1999.
174. Sandström JP, Moran NA, (1999) How nutritionally unbalanced is phloem sap for aphids? Entomologia Experimentalis et Applicata, 91, 203-210.
175. Sandström JP, Moran NA, (2001) Amino acid budgets in three aphid species using the same host plant. Physiological Entomology, 26, 202-211.
176. Sandström J, Pettersson J, (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. Journal of Insect Physiology, 40, 947-955.
177. Scarborough CL, Ferrari J, Godfray HCJ, (2005) Aphid protected from pathogen by endosymbiont. Science, 310, 1781.
178. Schauer C, Thompson CL, Brune A, (2012) The bacterial community in the gut of the Cockroach Shelfordella lateralis reflects the close evolutionary relatedness of cockroaches and termites. Applied and Environmental Microbiology, 78, 2758-2767.
179. Schiøtt M, De Fine Licht HH, Lange L, Boomsma JJ, (2008) Towards a molecular understanding of symbiont function: identification of a fungal gene for the degradation of xylan in the fungus gardens of leaf-cutting ants. BMC Microbiology, 8, 40.
180. Schiøtt M, Rogowska-Wrzesinska A, Roepstorff P, Boomsma JJ, (2010) Leaf-cutting ant fungi produce cell wall degrading pectinase complexes reminiscent of phytopathogenic fungi. BMC Biology, 8, 156.
181. Schoonhoven LM, van Loon JJA, Dicke M, (2005) Insect-Plant Biology. Oxford University Press, Oxford, UK.
182. Schuster LN, Sommer RJ, (2012) Expressional and functional variation of horizontally acquired cellulases in the nematode Pristionchus pacificus. Gene, 506, 274-282.
183. Shen Z, (2003) Polygalacturonase from Sitophilus oryzae: possible horizontal transfer of a pectinase gene from fungi to weevils. Journal of Insect Science, 3, 24.
184. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H, (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature, 407, 81-86.
185. Silva A, Bacci M, Pagnocca FC, Bueno OC, Hebling MJA, (2006a) Starch metabolism in Leucoagaricus gongylophorus, the symbiotic fungus of leaf-cutting ants. Microbiological Research, 161, 299-303.
186. Silva A, Bacci M, Pagnocca FC, Bueno OC, Hebling MJA, (2006b) Production of polysaccharidases in different carbon sources by Leucoagaricus gongylophorus Möller (Singer), the symbiotic fungus of the leaf-cutting ant Atta sexdens Linnaeus. Current Microbiology, 53, 68-71.
187. Sittenfeld A, Uribe-Lorío L, Mora M, et al,. (2002) Does a polyphagous caterpillar have the same gut microbiota when feeding on different species of food plants? Revista de Biología Tropical, 50, 547-560.
188. Six DL, (2012) Ecological and evolutionary determinants of bark beetle-fungus symbioses. Insects, 3, 339-366.
189. Six DL, Wingfield MJ, (2011) The role of phytopathogenicity in bark beetle-fungus symbioses: a challenge to the classic paradigm. Annual Review of Entomology, 56, 255-272.
190. Slansky F, Scriber JM, (1985) Food consumption and utilization. In: Comprehensive Insect Physiology, Biochemistry and Pharmacology (eds, Kerkut GA, Gilbert LI,), Vol. 4. pp. 87-163. Pergamon Press, Oxford, UK.
191. Sloan DB, Moran NA, (2012a) Genome reduction and co-evolution between the primary and secondary bacterial symbionts of psyllids. Molecular Biology and Evolution, 29, 3781-3792.
192. Sloan DB, Moran NA, (2012b) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biology Letters, 8, 986-989.
193. Stoll S, Feldhaar H, Fraunholz MJ, Gross R, (2010) Bacteriocyte dynamics during development of a holometabolous insect, the carpenter ant Camponotus floridanus. BMC Microbiology, 10, 308.
194. Stout MJ, Thaler JS, Thomma BPHJ, (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annual Review of Entomology, 51, 663-689.
195. Strong DR, Lawton JH, (1984) Insects on Plants: Community Patterns and Mechanisms. Harvard University Press, Cambridge, MA.
196. Suen G, Scott JJ, Aylward FO, et al,. (2010) An insect herbivore microbiome with high plant biomass-degrading capacity. PLoS Genetics, 6, e1001129.
197. Suen G, Teiling C, Li L, et al,. (2011) The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle. PLoS Genetics, 7, e1002007.
198. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA, (2011) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proceedings of the National Academy of Sciences, USA, 108, E1254-E1263.
199. Sun BF, Xiao JH, He SM, et al,. (2013) Multiple ancient horizontal gene transfers and duplications in lepidopteran species. Insect Molecular Biology, 22, 72-87.
200. Tamas I, (2002) 50 Million years of genomic stasis in endosymbiotic bacteria. Science, 296, 2376-2379.
201. Tan Q, Zhang L, Grant J, Cooper P, Tegeder M, (2010) Increased phloem transport of S-methylmethionine positively affects sulfur and nitrogen metabolism and seed development in pea plants. Plant Physiology, 154, 1886-1896.
202. Tang X, Freitak D, Vogel H, et al,. (2012) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS One, 7, e36978.
203. Teixeira DDC, Saillard C, Eveillard S, et al,. (2005) "Candidatus Liberibacter americanus", associated with citrus huanglongbing (greening disease) in São Paulo State, Brazil. International Journal of Systematic and Evolutionary Microbiology, 55, 1857-1862.
204. Teixeira L, Ferreira A, Ashburner M, (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biology, 6, e2.
205. Thao ML, Moran NA, Abbot P, et al,. (2000a) Cospeciation of psyllids and their primary prokaryotic endosymbionts. Applied and Environmental Microbiology, 66, 2898-2905.
206. Thao ML, Clark MA, Baumann L, et al,. (2000b) Secondary endosymbionts of psyllids have been acquired multiple times. Current Microbiology, 41, 300-304.
207. Tsuchida T, Koga R, Fukatsu T, (2004) Host plant specialization governed by facultative symbiont. Science, 303, 1989.
208. Urban JM, Cryan JR, (2012) Two ancient bacterial endosymbionts have coevolved with the planthoppers (Insecta: Hemiptera: Fulgoroidea). BMC Evolutionary Biology, 12, 87.
209. Vega FE, Blackburn MB, Kurtzman CP, Dowd PF, (2003) Identification of a coffee berry borer-associated yeast: does it break down caffeine? Entomologia Experimentalis et Applicata, 107, 19-24.
210. Viñuelas J, Febvay G, Duport G, et al,. (2011) Multimodal dynamic response of the Buchnera aphidicola pLeu plasmid to variations in leucine demand of its host, the pea aphid Acyrthosiphon pisum. Molecular Microbiology, 81, 1271-1285.
211. Visôtto LE, Oliveira MGA, Guedes RNC, Ribon AOB, Good-God PIV, (2009) Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. Journal of Insect Physiology, 55, 185-191.
212. Vogel KJ, Moran NA, (2010) Sources of variation in dietary requirements in an obligate nutritional symbiosis. Proceedings of the Royal Society B: Biological Sciences, 278, 115-121.
213. Vorburger C, Gehrer L, Rodriguez P, (2010) A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. Biology Letters, 6, 109-111.
214. Walters DR, McRoberts N, Fitt BDL, (2008) Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biological Reviews, 83, 79-102.
215. Warnecke F, Luginbühl P, Ivanova N, et al,. (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature, 450, 560-565.
216. Watanabe H, Tokuda G, (2010) Cellulolytic systems in insects. Annual Review of Entomology, 55, 609-632.
217. Watanabe H, Noda H, Tokuda G, Lo N, (1998) A cellulase gene of termite origin. Nature, 394, 330-331.
218. Weintraub PG, Beanland L, (2006) Insect vectors of phytoplasmas. Annual Review of Entomology, 51, 91-111.
219. Weis AE, (1982) Use of symbiotic fungus by the gall maker Asteromyia carbonifera to inhibit attack by the parasitoid Torymus capite. Ecology, 63, 1602-1605.
220. Wilson ACC, Ashton PD, Calevro F, et al,. (2010) Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Molecular Biology, 19 (Suppl 2), 249-258.
221. Wolschin F, Hölldobler B, Gross R, Zientz E, (2004) Replication of the endosymbiotic bacterium Blochmannia floridanus is correlated with the developmental and reproductive stages of its ant host. Applied and Environmental Microbiology, 70, 4096-4102.
222. Wu D, Daugherty SC, Van Aken SE, et al,. (2006) Metabolic complementarity and genomics of the dual bacterial symbiosis of sharpshooters. PLoS Biology, 4, e188.