Limited endosymbiont variation in diuraphis noxia (Hemiptera: Aphididae) biotypes from the United States and South Africa

Journal of Economic Entomology

Volumn 103, Issue 3, 2010, Pages 887-897

  Swanevelder, Z H ^a   Surridge, A K J ^a   Venter, E ^b   Botha, A M ^c  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b UNIVERSITY OF JOHANNESBURG   (South Africa)

^c STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

Biotypes; Diuraphis noxia; Endosymbiont variation

Indexed keywords

ANIMAL; ARTICLE; BUCHNERA; CHEMISTRY; DNA SEQUENCE; FEMALE; GENE DOSAGE; GENETICS; HEMIPTERA; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLASMID; SOUTH AFRICA; SYMBIOSIS; UNITED STATES;

ANIMALS; BASE SEQUENCE; BUCHNERA; FEMALE; GENE DOSAGE; HEMIPTERA; MOLECULAR SEQUENCE DATA; PLASMIDS; SEQUENCE ANALYSIS, DNA; SOUTH AFRICA; SYMBIOSIS; UNITED STATES;

APHIDIDAE; BACTERIA (MICROORGANISMS); BUCHNERA APHIDICOLA; DIURAPHIS; DIURAPHIS NOXIA; HEMIPTERA; HEXAPODA;

EID: 77953061987     PISSN: 00220493     EISSN: None     Source Type: Journal    
DOI: 10.1603/EC09257     Document Type: Article

References (90)

1. Abbot, P., and N. A. Moran. 2002. Extremely low levels of genetic polymorphism in endosymbionts (Buchnera) of aphids (Pemphigus). Mol. Ecol. 11: 2649-2660.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389- 3402.
4. Baker, D. A., H. D. Loxdale, and O. R. Edwards. 2003. Genetic variation and founder effects in the parasitoid wasp, Diaeretiella rapae (MÕintosh) (Hymenoptera: Bra-conidae: Aphidiidae), affecting its potential as a biological control agent. Mol. Ecol. 12: 3303-3311.
5. Baumann, L., P. Baumann, N. A. Moran, J. Sandstrom, and M. L. Thao. 1999. Genetic characterization of plasmids containing genes encoding enzymes of leucine biosynthesis in endosymbionts (Buchnera) of aphids. J. Mol. Evol. 48: 77-85.
6. Baumann, P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu. Rev. Microbiol. 59: 55-89.
7. Baumann, P., C.-Y. Lai, L. Baumann, D. Rouhbakhsh, N. A. Moran, and A. M. Clark. 1995. Genetics, physiology and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. Annu. Rev. Microbiol. 49: 55-94.
8. Blackman, R. L., and V. F. Eastop. 2000. Aphids on the worldÕs crops. an identiFIcation and information guide. Wiley, London, United Kingdom.
9. Burd, J. D., D. R. Porter, G. J. Puterka, S. D. Haley, and F. B. Peairs. 2006. Biotypic variation among North American Russian wheat aphid (Homoptera: Aphididae) populations. J. Econ. Entomol. 99: 1862-1866.
10. Chen, D.-Q., B. C. Campbell, and A. H. Purcell. 1996. Anew Rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr. Microbiol. 33: 123- 128.
11. Chen, D.-Q., C. B. Montllor, and A. H. Purcell. 2000. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol. Exp. Appl. 95: 315-323.
12. Chiel, E., Y. Gottlieb, E. Zchori-Fein, N. Mozes-Daube, N. Katzir, M. Inbar, and M. Ghanim. 2007. Biotype-dependent secondary symbiont communities is sympatric populations of Bemisia tabaci. Bull. Entomol. Res. 97: 407-413.
13. Cole, J. R., B. Chai, R. J. Farris, Q. Wang, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, A. M. Bandela, E. Cardenas, G. M. Garrity, and J. M. Tiedje. 2006. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 35: D169-D172.
14. Darby, A. C., L. M. Birkle, S. L. Turner, and A. E. Douglas. 2001. An aphid-borne bacterium allied to the secondary symbionts of whiteßy. FEMS Microbiol. Ecol. 36: 43-50.
15. Dixon, A.F.G. 1998. Aphid ecology: an optimization approach. Chapman & Hall, London, United Kingdom.
16. Don, R. H., P. T. Cox, B. J. Wainwright, K. Baker, and J. S. Mattick. 1991. ÔTouchdownÕ PCR to circumvent spurious priming during gene ampliFIcation. Nucleic Acids Res. 19: 4008.
17. Douglas, A. E. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43: 17-37.
18. Douglas, A. E., and W. A. Prosser. 1992. Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J. Insect Physiol. 38: 565-568.
19. Du Toit, F. 1989. Inheritance of resistance in two Triticum aestivum lines to Russian wheat aphid (Homoptera: Aphididae). J. Econ. Entomol. 82: 1251-1253.
20. Dunbar, H., A.C.C. Wilson, N. R. Ferguson, and N. A. Moran. 2007. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLOS Biol. 5: e96 [1006- 1015].
21. Emroy, S. A., P. Bouvet, and J. G. Belasco. 1992. A 5 α-terminal stem-loop structure can stabilize mRNA in Escherichia coli. Genes Dev. 6: 135-148.
22. Ferrari, J., C. L. Scarborough, and H.C.J. Godfray. 2007. Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia (Berl.) 153: 323-329.
23. Ferrari, J., A. C. Darby, T. J. Daniell, H.C.J. Godfray, and A. E. Douglas. 2004. Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29: 60-65.
24. Fjellbirkeland, A., V. Torsvik, and L. Ovreas. 2001. Methanotrophic diversity in an agricultural soil as evaluated by denaturing gradient gel electrophoresis proFIles of pmoA, mxaF and 16S rDNA sequences. Antonie van Leeuwenhoek 79: 209-217.
25. Fukatsu, T. 2001. Secondary intracellular symbiotic bacteria in aphids of the genus Yamatocallis (Homoptera: Aphididae: Drepanosiphinae). Appl. Environ. Microbiol. 67: 5315-5320.
26. Funk, D. J., J. J. Wernegreen, and N. A. Moran. 2001. IntraspeciFIc variation in symbiont genomes: bottlenecks and the aphid-Buchnera association. Genetics 157: 477- 489.
27. Gil, R., B. Sabater-Munoz, V. Perez-Brocal, F. J. Silva, and A. Latorre. 2006. Plasmids in the aphid endosymbiont Buchnera aphidicola with the smallest genomes. A puzzling evolutionary story. Gene 370: 17-25.
28. Gottlieb, Y., M. Ghanim, E. Chiel, D. Gerling, V. Portnoy, S. Steinberg, G. Tzuri, A. R. Horowitz, E. Belausov, N. Mozes-Daube, et al. 2006. IdentiFIcation and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl. Environ. Microbiol. 72: 3646-3652.
29. Haley, S. D., F. B. Peairs, C. B. Walker, J. B. Rudolph, and T. L. Randolph. 2004. Occurrence of a new Russian wheat aphid biotype in Colorado. Crop Sci. 44: 1589- 1592.
30. Haynes, S., A. C. Darby, T. J. Daniell, G. Webster, F.J.F. van Veen, H.C.J. Gofdfray, J. I. Prosser, and A. E. Douglas. 2003. Diversity of bacteria associated with natural aphid populations. Appl. Environ. Microbiol. 69: 7216-7223.
31. Jyoti, J. L., and J. P. Michaud. 2005. Comparative biology of a novel strain of Russian wheat aphid (Homoptera: Aphididae) on three wheat cultivars. J. Econ. Entomol. 98: 1032-1039.
32. Jyoti, J. L., J. A. Qureshi, J. P. Michaud, and T. J. Martin. 2006. Virulence of two Russian wheat aphid biotypes to eight wheat cultivars at two temperatures. Crop Sci. 46: 774- 780.
33. Koga, R., T. Tsuchida, and T. Fukatsu. 2003. Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. Lond. 270: 2543-2550.
34. Lai, C.-Y., L. Baumann, and P. Baumann. 1994. AmpliFIcation of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc. Natl. Acad. Sci. U.S.A. 91: 3819-3823.
35. Lai, C.-Y., P. Baumann, and N. A. Moran. 1996. The endosymbiont (Buchnera sp.) of the aphid Diuraphis noxia contains plasmids consisting of trpEG and tandem repeats of trpEG pseudogenes. Appl. Environ. Microbiol. 62: 332- 339.
36. Lapitan, N.L.V., Y.-C. Li, R.S.G. Walters, Y. Peng, F. B. Peairs, and A.-M. Botha. 2007. Limited nuclear and mitochondrial DNA variation among Russian wheat aphid (Diuraphis noxia) biotypes from the United States and Africa, American Entomological Society, San Diego, December 9-12, American Entomological Society, San Diego, CA.
37. Leonardo, T. E. 2004. Removal of a specialization-associated symbiont does not affect aphid Fitness. Ecol. Lett. 7: 461-468.
38. Lu, G., and E. N. Moriyama. 2004. Vector NTI, a balanced all-in-one sequence analysis suite. Brief. Bioinform. 5: 378-388.
39. Markham, N. R., and M. Zuker. 2005. DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res. 33: 577-581.
40. Mittler, T. E. 1971. Dietary amino acid requirements of the aphid Myzus persicae affected by antibiotic uptake. J. Nutr. 101: 1023-1028.
41. Montllor, C. B., A. Maxmen, and A. H. Purcell. 2002. Facultative bacterial endosymbionts beneFIt pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27: 189-195.
42. Moran, N. A., H. E. Dunbar, and J. L. Wilcox. 2005. Regulation of transcription in a reduced bacterial genome: nutrient-provisioning genes of the obligate symbiont Buchnera aphidicola. J. Bacteriol. 187: 4229-4237.
43. Moran, N. A., G. R. Plague, J. P. Sandstrom, and J. L. Wilcox. 2003. A genomic perspective on nutrient provisioning by bacterial symbionts of insects. Proc. Natl. Acad. Sci. U.S.A. 100: 14543-14548.
44. Moreno, C. X., F. Fred Moy, T. J. Daniels, H. P. Godfrey, and F. C. Cabello. 2006. Molecular analysis of microbial communities identiFIed in different developmental stages of Ixodes scapularis ticks from Westchester and Dutchess counties, New York. Environ. Microbiol. 8: 761-772.
45. Munson, M. A., P. Baumann, and M. G. Kinsey. 1991. Buchnera gen. nov. and Buchnera aphidicola sp. nov., a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. Int. J. Syst. Bacteriol. 41: 566-568.
46. Muyzer, G., and K. Smalla. 1998. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek 73: 127-141.
47. Muyzer, G., E. C. De Waal, and A. G. Uitterlinden. 1993. ProFIling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-ampliFIed genes coding for 16S rRNA. Appl. Environ. Microbiol. 59: 695-700.
48. Myers, R. M., S. G. Fisher, L.L.S., and T. Maniatis. 1985. Nearly all single base substitutions in DNA fragments joined to a GC-clamp can be detected by denaturing gradient gel electrophoresis. Nucleic Acids Res. 13: 3131- 3145.
49. Nakabachi, A., S. Shigenobu, N. Sakazume, T. Shiraki, Y. Hayashizaki, P. Carninci, H. Ishikawa, T. Kudo, and T. Fukatsu. 2005. Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium, Buchnera. Proc. Natl. Acad. Sci. U.S.A. 102: 5477-5482.
50. Ni, X., S. S. Quisenberry, J. Markwell, T. Heng-Moss, L. Higley, F. Baxendale, G. Sarath, and R. Klucas. 2001. In vitro enzymatic chlorophyll catabolism in wheat elicited by cereal aphid feeding. Entomol. Exp. Appl. 101: 159- 166.
51. Oliver, K. M., J. A. Russell, N. A. Moran, and M. S. Hunter. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc. Natl. Acad. Sci. U.S.A. 100: 1803-1807.
52. Plague, G. R., C. Dale, and N. A. Moran. 2003. Low and homogeneous copy number of plasmid-borne symbiont genes affecting host nutrition in Buchnera aphidicola of the aphid Uroleucon ambrosiae. Mol. Ecol. 12: 1095-1100.
53. Porter, D. R., and J. A. Webster. 2000. Russian wheat aphidinduced protein alterations in spring wheat. Euphytica 111: 199-203.
54. Puterka, G. J., J. D. Burd, and R. L. Burton. 1992. Biotypic variation in a worldwide collection of Russian wheat aphid (Homoptera: Aphididae). J. Econ. Entomol. 85: 1497-1506.
55. Puterka, G. J., W. C. Black, W. M. Steiner, and R. L. Burtpn. 1993. Genetic variation and phylogenetic relationships among worldwide collections of the Russian wheat aphid, Diuraphis noxia (Mordvilko), inferred from allozyme and RAPD-PCR markers. Heredity 70: 604-618.
56. Reeson, A. F., T. Jankovic, M. L. Kasper, S. Rogers, and A. D. Austin. 2003. Application of 16S rDNA-DGGE to examine the microbial ecology associated with a social wasp Vespula germanica. Insect Mol. Biol. 12: 85-91.
57. Romero, D., and R. Palacios. 1997. Gene ampliFIcation and genome plasticity in prokaryotes. Annu. Rev. Genet. 31: 91-111.
58. Rozen, S., and H. J. Skaletsky. 2000. Primer3 on the WWW for general users and for biologist programmers, pp. 365- 386. In S. Krawetz and S. Misener [eds.], Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ.
59. Russell, J. A., and N. A. Moran. 2005. Horizontal transfer of bacterial symbionts: heritability and Fitness effects in a novel aphid host. Appl. Environ. Microbiol. 71: 7987-7994.
60. Russell, J. A., A. Latorre, B. Sabater-Munoz, A. Moya, and N. A. Moran. 2003. Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol. Ecol. 12: 1061-1075.
61. Sandstrom, J., and N. A. Moran. 1999. How nutritionally imbalanced is phloem sap for aphids? Entomol. Exp. Appl. 91: 203-210.
62. Sandstrom, J., A. Telang, and N. A. Moran. 2000. Nutritional enhancement of host plants by aphids-a comparison of three aphid species on grasses. J. Insect Physiol. 46: 33-40.
63. Sandstrom, J. P., J. A. Russell, J. P. White, and N. A. Moran. 2001. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10: 217-228.
64. Scarborough, C. L., J. Ferrari, and H.C.J. Godfray. 2005. Aphid protected from pathogen by endosymbiont. Science (Wash., D.C.) 310: 1781.
65. Sheffield, V. C., D. R. Cox, L. S. Lerman, and R. M. Myers. 1989. Attachment of a 40-base-pair GC-rich sequence (GC-clamp) to genomicDNAfragments by the polymerase chain reaction results in improved detection of singlebase changes. Proc. Natl. Acad. Sci. U.S.A. 86: 232-236.
66. Shigenobu, S., H. Watanabe, M. Hattori, Y. Sakaki, and H. Ishikawa. 2000. Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. Nature (Lond.) 407: 81-86.
67. Shufran, K. A., L. R. Kirkman, and G. J. Puterka. 2007. Absence of mitochondrial DNA sequence variation in Russian wheat aphid (Hemiptera: Aphididae) populations consistent with a single introduction into United States. J. Kans. Entomol. Soc. 80: 319-326.
68. Silva, F. J., R.C.H. J. van Ham, B. Sabater, and A. Latorre. 1998. Structure and evolution of the leucine plasmids carried by the endosymbiont (Buchnera aphidicola) from aphids of the family Aphididae. FEMS Microbiol. Lett. 168: 43-49.
69. Smith, C. M. 2009. Global phylogenetics of an invasive species: evidence for multiple invasions into North America. In Joint Meeting of the Southwestern Branch of the Entomological Society of America and Western Extension/ Education Research Activity (WERA066), February 2009, Stillwater, OK.
70. Srivastava, P. N. 1987. Nutritional physiology, pp. 99-121. In P. Harrewijn [ed.], Aphids: their biology, natural enemies and control. Elsevier, Amsterdam, The Netherlands.
71. Stary, P. 2000. On-going expansion of Russian wheat aphid, Diuraphis noxia (Kurdj.) in central Europe (Hom.: Aphididae). J. Pest Sci. 73: 75-78.
72. Stary, P., and H. Lukasova. 2002. Increase of Russian wheat aphid, Diuraphis noxia (Kurdj.) in hot and dry weather (Hom., Aphididae). J. Pest Sci. 75: 6-10.
73. Stoll, S., J. Gadau, R. Gross, and H. Feldhaar. 2007. Bacterial microbiota associated with ants of the genus Tetraponera. Biol. J. Linn. Soc. 90: 399-412.
74. Surridge, A.K.J. 2007. Denaturing gradient gel electrophoresis characterisation of microbial communities in polycyclic aromatic hydrocarbon and polychlorinated biphenyl contaminated soil, pp. 183, Microbiology. University of Pretoria, Pretoria, South Africa.
75. Tamas, I., L. Klasson, B. Canback, A. K. Naslund, A.-S. Eriksson, J. J. Wernegreen, J. P. Sandstrom, N. A. Moran, and S.G.E. Andersson. 2002. 50 Million years of genomic stasis in endosymbiotic bacteria. Science (Wash., D.C.) 296: 2376-2379.
76. Telang, A., J. Sandstrom, E. Dyreson, and N. A. Moran. 1999. Feeding damage by Diuraphis noxia results in a nutritionally enhanced phloem diet. Entomol. Exp. Appl. 91: 493-412.
77. Thao, M. L., L. Baumann, P. Baumann, and N. A. Moran. 1998. Endosymbionts (Buchnera) from the aphids Schizaphis graminum and Diuraphis noxia have different copy numbers of the plasmid containing the leucine biosynthetic genes. Curr. Microbiol. 36: 238-240.
78. Tolmay, V. L., R. C. Lindeque, and G. J. Prinsloo. 2007. Preliminary evidence of a resistance-breaking biotype of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), in South Africa. Afr. Entomol. 15: 228-230.
79. Unterman, B. M., P. Baumann, and D. L. McLean. 1989. Pea aphid symbiont relationships established by analysis of 16S rRNAs. J. Bacteriol. 171: 2970-2974.
80. van der Westhuizen, A. J., and Z. Pretorius. 1996. Protein composition of wheat apoplastic ßuid and resistance to the Russian wheat aphid. Aust. J. Plant Physiol. 23: 645- 648.
81. van Ham, R.C.H. J., A. Moya, and A. Latorre. 1997. Putative evolutionary origin of plasmids carrying the genes involved in leucine biosynthesis in Buchnera aphidicola (endosymbiont of aphids). J. Bacteriol. 179: 4768-4777.
82. van Ham, R.C.H. J., F. Gonzalez-Candelas, F. J. Silva, B. Sabater, A. Moya, and A. Latorre. 2000. Postsymbiotic plasmid acquisition and evolution of the repA1-replicon in Buchnera aphidicola. Proc. Natl. Acad. Sci. U.S.A. 97: 10855-10860.
83. van Ham, R.C.H. J., J. Kamerbeek, C. Palacios, C. Rausell, F. Abascal, U. Bastolla, J. M. Fernandez, L. Jimenez, M. Postigo, F. J. Silva, et al. 2003. Reductive genome evolution in Buchnera aphidicola. Proc. Natl. Acad. Sci. U.S.A. 100: 581-586.
84. Van Zyl, R. A., and A.-M. Botha. 2008. Eliciting proteins from Diuraphis noxia biotypes differ in size and composition, IPRI-18th Biennial Workshop, Ft. Collins, USA, February 10-13, IPRI-18th Biennial Workshop, Ft. Collins, CO.
85. Weiland, A. A., F. B. Peairs, T. L. Randolph, J. B. Rudolph, S. D. Haley, and G. J. Puterka. 2008. Biotypic diversity in Colorado Russian wheat aphid (Hemiptera: Aphididae) populations. J. Econ. Entomol. 101: 569-574.
86. Wernegreen, J. J., and N. A. Moran. 2000. Decay of mutualistic potential in aphid endosymbionts through silencing of biosynthetic loci: Buchnera of Diuraphis. Proc. R. Soc. Lond. 267: 1423-1431.
87. Wong, H. C., and S. Chang. 1986. IdentiFIcation of a positive retroregulator that stabilizes mRNAs in bacteria. Proc. Natl. Acad. Sci. U.S.A. 83: 3233-3237.
88. Wuchty, S., W. Fontana, I. L. Hofacker, and P. Schuster. 1999. Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers 49: 145-165.
89. Xayaphoummine, A., T. Bucher, and H. Isambert. 2005. Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots. Nucleic Acids Res. 33: W605-W610.
90. Zientz, E., T. Dadndekar, and R. Gross. 2004. Metabolic interdependence of obligate intracellular bacteria and their insect hosts. Microbiol. Mol. Biol. Rev. 68: 745-770.