Multitrophic interaction in the rhizosphere of maize: Root feeding of western corn rootworm larvae alters the microbial community composition

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Dematheis, Flavia ^a   Zimmerling, Ute ^a   Flocco, Cecilia ^a   Kurtz, Benedikt ^b   Vidal, Stefan ^b   Kropf, Siegfried ^c   Smalla, Kornelia ^a  

^a INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER; PHENOL DERIVATIVE;

16S RRNA GENE; ACINETOBACTER CALCOACETICUS; ARTHROPOD LARVA; ARTICLE; COLEOPTERA; COMMUNITY STRUCTURE; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; FUNGAL COMMUNITY; MAIZE; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT EXUDATION; POLYMERASE CHAIN REACTION; RHIZOSPHERE; RNA GENE; WESTERN CORN ROOTWORM;

ACINETOBACTER CALCOACETICUS; ANIMALS; BEETLES; LARVA; PLANT ROOTS; RHIZOSPHERE; RNA, RIBOSOMAL, 16S; SOIL MICROBIOLOGY; ZEA MAYS;

ACINETOBACTER CALCOACETICUS; BACTERIA (MICROORGANISMS); DIABROTICA VIRGIFERA VIRGIFERA; FUNGI; ZEA MAYS;

EID: 84861309379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037288     Document Type: Article

References (55)

1. Gray ME, Sappington TW, Miller NJ, Moeser J, Bohn MO, (2009) Adaptation and invasiveness of western corn rootworm: intensifying research on a worsening pest. Annu Rev Entomol 54: 303-321.
2. Szalai M, Papp Komáromi J, Bažok R, Igrc Barčić J, Kiss J, et al. (2011) Generational growth rate estimates of Diabrotica virgifera virgifera populations (Coleoptera: Chrysomelidae). J Pest Sci 84: 133-142.
3. Ciosi M, Miller NJ, Kim KS, Giordano R, Estoup A, et al. (2008) Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity. Mol Ecol 17: 3614-3627.
4. EPPO (2011) European and Mediterranean Plant Protection Organization website. Available: http://www.eppo.org/QUARANTINE/Diabrotica_virgifera/diabrotica_virgifera. Accessed 2012 Apr 6.
5. Wesseler J, Fall EH, (2010) Potential damage costs of Diabrotica virgifera virgifera infestation in Europe: the "no control" Scenario. J Appl Entomol 134: 385-394.
6. Meinke LJ, Sappington TW, Onstad DW, Guillemaud T, Miller NJ, et al. (2009) Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics. Agric For Entomol 11: 29-46.
7. Urias-Lopez MA, Meinke LJ, Leon GH, Haile FJ, (2000) Influence of Western Corn Rootworm (Coleoptera:Chrysomelidae) Larval Injury on Photosynthetic Rate and Vegetative Growth of Different Types of Maize. Environ Entomol 29: 861-867.
8. Spike BP, Tollefson JJ, (1991) Yield Response of Corn Subjected to Western Corn-Rootworm (Coleoptera, Chrysomelidae) Infestation and Lodging. J Econ Entomol 84: 1585-1590.
9. European Commission (2003) 2003/766/EC: Decision of 24 October 2003 on emergency measures to prevent the spread within the Community of Diabrotica virgifera LeConte. Off J Eur Union L 275: 49-50.
10. European Commission (2006) 2006/565/EC: Recommendation of 11 August 2006 on containment programmes to limit the further spread of Diabrotica virgifera LeConte in Community areas where its presence is confirmed. Off J Eur Union L 225: 30-31.11.
11. Clark PL, Vaughn TT, Meinke LJ, Molina-Ochoa J, Foster JE, (2006) Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) larval feeding behavior on transgenic maize (MON 863) and its isoline. J Econ Ent 99: 722-727.
12. Levine E, Spencer JL, Isard SA, Onstad DW, Gray ME, (2002) Adaptation of the western corn rootworm to crop rotation: evolution of a new strain in response to a management practice. Am Entomol 48: 94-107.
13. Onstad DW, Spencer JL, Guse CA, Levine E, Isard SA, (2001) Modeling evolution of behavioral resistance by an insect to crop rotation. Entomol Exp Appl 100: 195-201.
14. Parimi S, Meinke LJ, French WB, Chandler LD, Siegfried BD, (2006) Stability and persistence of aldrin and methyl-parathion resistance in western corn rootworm populations (Coleoptera: Chrysomelidae). J Econ Entomol 25: 269-274.
15. Gassmann AJ, Petzold-Maxwell JL, Keweshan RS, Dunbar MW, (2011) Field-Evolved Resistance to Bt Maize by Western Corn Rootworm. PLoS ONE 6: e22629.
16. Meihls LN, Higdon ML, Siegfried BD, Miller NJ, Sappington TW, et al. (2008) Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc Natl Acad Sci U S A 105: 19177-19182.
17. Hayat R, Ali S, Amara U, Khalid R, Ahmed I, (2010) Soil beneficial bacteria and their role in plant growth and promotion: a review. Ann Microbiol DOI 10.1007/s13213-010-0117-1.
18. Van Loon LC, Bakker P, Pieterse CMJ, (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36: 453-483.
19. Van Oosten VR, Bodenhausen N, Reymond P, Van Pelt JA, Van Loon LC, et al. (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Mol Plant Microbe Int 21: 919-930.
20. Nishida T, Katayama N, Izumi N, Ohgushi T, (2010) Arbuscular mycorrhizal fungi species-specifically affect induced plant responses to a spider mite. Popul Ecol 52: 507-515.
21. Berg G, Smalla K, (2009) Plant species and soil type cooperativelyshape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68: 1-13.
22. Denton CS, Bardgett RD, Cook R, Hobbs PJ, (1998) Low amounts of root herbivory positively influences the rhizosphere microbial community in a temperate grassland soil. Soil Biol Biochem 31: 155-165.
23. Grayston SJ, Dawson LA, Treonis AM, Murray PJ, Ross J, et al. (2001) Impact of root herbivory by insect larvae on soil microbial communities. Eur J Soil Biol 37: 277-280.
24. Dawson LA, Grayston SJ, Murray PJ, Ross J, Reid EJ, et al. (2004) Impact of Tipula paludosa larvae on plant growth and soil microbial community. Appl Soil Ecol 25: 51-61.
25. Treonis AM, Grayston SJ, Murray PJ, Dawson LA, (2004) Effects of root feeding, cranefly larvae on soil microorganisms and the composition of rhizosphere solutions collected from grassland plants. Appl Soil Ecol 28: 203-251.
26. Brimecombe MJ, De Lelj FA, Lynch JM, (2001) The Rhizosphere. The Effect of Root Exudates on Rhizosphere Microbil Populations. In: Pinton R, Varanini Z, Nannipieri P, editors. The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface pp. 95-140 Marcel Dekker, New York.
27. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco LM, (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
28. Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM, (2008) Root Exudates Regulate Soil Fungal Community Composition and Diversity. Appl Environ Microbiol 74: 738-744.
29. Prischmann DA, Lehman RM, Christie AA, Dashiell KE, (2008) Characterization of bacteria isolated from maize roots: Emphasis on Serratia and infestation with corn rootworms (Chrysomelidae: Diabrotica). Appl Soil Ecol 40: 417-431.
30. Broekgaarden C, Poelman EH, Steenhuis G, Voorrips RE, Dicke M, et al. (2007) Genotypic variation in genome-wide transcription profiles induced by insect feeding: Brassica oleracea-Pieris rapae interactions. Genomics 8: 239.
31. Spencer JL, Hibbard BE, Moeser J, Onstad DW, (2009) Behaviour and ecology of the western corn rootworm (Diabrotica virgifera virgifera LeConte). Agr Forest Entomol 11: 9-27.
32. European Food Safety Authority (2009) Application (Reference EFSA-GMO-CZ-2005-27) for the placing on the market of the insect-resistant and herbicide-tolerant genetically modified maize MON88017, for food and feed uses, import and processing under regulation (EC) No 1829/2003 from Monsanto. EFSA J 1075: 1-28.
33. Costa R, Falcão Salles J, Berg G, Smalla K, (2006) Cultivation independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environ Microbiol 8: 2136-2149.
34. Weinert N, Meincke R, Gottwald C, Heuer H, Gomes CMC, et al. (2009) Rhizosphere communities of genetically modified zeaxanthin-accumulating potato plants and their parent cultivar differ less than those of different potato cultivars. Appl Environ Microbiol 75: 3859-3865.
35. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH, (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel electrophoretic separation in denaturing gradients. Appl Environ Microbiol 63: 3233-3241.
36. Heuer H, Wieland G, Schönfeld J, Schönwälder A, Gomes NCM, et al. (2001) Bacterial community profiling using DGGE or TGGE analysis. In: Rouchelle P, editors. Environmental molecular microbiology: protocols and applications pp. 177-190 Horizon Scientific Press, Wymondham, UK.
37. Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A, et al. (2003) Dynamics of Fungal Communities in Bulk and Maize Rhizosphere Soil in the Tropics. Appl Environ Microbiol 69: 3758-3766.
38. Kropf S, Heuer H, Grüning M, Smalla K, (2004) Significance test for comparing complex microbial community fingerprints using pairwise similarity measures. J Microbiol Meth 57: 187-195.
39. Kandeler E, Marschner P, Tscherko D, Gahoonia TS, Nielsen NE, (2002) Microbial community composition and functional diversity in the rhizosphere of maize. Plant Soil 238: 301-312.
40. Gomes NCM, Heuer H, Schönfeld J, Costa R, Mendonça-Hagler L, et al. (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232: 167-180.
41. Baumgarte S, Tebbe CC, (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Mol Ecol 14: 2539-2551.
42. Miethling-Graff R, Dockhorn S, Tebbe CC, (2010) Release of the recombinant Cry3Bb1 protein of Bt maize MON88017 into field soil and detection of effects on the diversity of rhizosphere bacteria. Eur J Soil Biol 46: 41-48.
43. Zhan Y, Yan Y, Zhang W, Yu M, Chen M, et al. (2011) Genome Sequence of Acinetobacter calcoaceticus PHEA-1 2, Isolated from Industry Wastewater. Am Soc Microbiol. doi:10.1128/JB.00261-11.
44. Poerschmann J, Rauschen S, Langer U, Augustin J, Górecki T, (2008) Molecular level lignin patterns of genetically modified Bt-Maize MON88017 and three conventional varieties using tetramethylammonium hydroxide (TMAH)-induced thermochemolysis. J Agric Food Chem 56: 11906-11913.
45. Lanoue A, Brulat V, Henkes GJ, Koch I, Schurr U, et al. (2010) De novo biosynthesis of defense root exudates in response to Fusarium attack in barley. New Phytol 185: 577-588.
46. Robert CAM, Veyrat N, Glauser G, Marti G, Doyen GR, et al. (2012) A specialist root herbivore exploits defensive metabolites to locate nutritious tissues. Ecol Lett 14: 55-64.
47. Davis CS, Ni XZ, Quisenberry SS, Foster JE, (2000) Indetification and quantification of hydroxamic acids in maize seedling root tissue and impact on western corn rootworm (Coleoptera; Chrysomelidae) larval development. J Econ Entomol 93: 989-992.
48. Kavroulakis N, Ntougias S, Besi MI, Katsou P, Damaskinou A, et al. (2010) Antagonistic bacteria of composted agro-industrial residues exhibit antibiosis against soil-borne fungal plant pathogens and protection of tomato plants from Fusarium oxysporum f.sp. radicis-lycopersici. Plant Soil 333: 233-247.
49. Kurtz B, (2010) Interaction of maize root-associated fungi and the western corn rootworm. PhD thesis. University of Göttingen.
50. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, et al. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737.
51. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, et al. (2008) A maize (E)-b-Caryophyllene synthase implicated in indirect defense responses against herbivores Is not expressed in most american maize varieties. Plant Cell 20: 482-494.
52. Erb M, Flors V, Karlen D, de Lange E, Planchamp C, et al. (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59: 292-302.
53. Wurst S, (2010) Effects of earthworms on above- and belowground herbivores. Appl Soil Ecol 45: 123-30.
54. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M, (2010) Helping plants to deal with insects: The role of beneficial soil-borne microbes. Trend Plant Sci 15: 507-514.
55. Lanoue A, Brulat V, Schurr U, Röse USR, (2010) Induced root-secreted phenolic compounds as a belowground plant defense. Plant Signal Behav 5: 1037-1038.