Decomposer animals induce differential expression of defence and auxin-responsive genes in plants

Soil Biology and Biochemistry

Volumn 43, Issue 6, 2011, Pages 1130-1138

  Endlweber, Kerstin ^a   Krome, Kristin ^a   Welzl, Gerhard ^b   Schäffner, Anton Rudolf ^b   Scheu, Stefan ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Arabidopsis thaliana; Auxin; Collembola; Microarray; Protaphorura fimata; Soil fauna

Indexed keywords

ARABIDOPSIS THALIANA; AUXIN; COLLEMBOLA; PROTAPHORURA FIMATA; SOIL FAUNA;

GENE EXPRESSION; NUTRIENTS; SOILS;

ANIMALS;

ARTHROPOD; DECOMPOSITION; DICOTYLEDON; GENE EXPRESSION; GROWTH RATE; HERBIVORE; HORMONE; MOBILIZATION; MORPHOLOGY; NUTRIENT UPTAKE; PHENOTYPIC PLASTICITY; ROOT; SOIL MICROORGANISM;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; COLLEMBOLA; PROTAPHORURA FIMATA;

EID: 79954607709     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2010.11.013     Document Type: Article

References (62)

1. Bardgett R.D., Chan K.F. Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biology & Biochemistry 1999, 31:1007-1014.
2. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 1995, 57:289-300.
3. Bezemer T.M., Wagenaar R., van Dam N.M., Wäckers F.L. Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos 2003, 101:555-562.
4. Bezemer T.M., Wagenaar R., van Dam M., van der Putten W.H., Wackers F.L. Above- and below-ground terpenoid aldehyde induction in cotton Gossypium herbaceum, following root and leaf injury. Journal of Chemical Ecology 2004, 30:53-67.
5. Blilou I., Ocampo J.A., Garcia-Garrido J.M. Induction of Ltp (lipid transfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. Journal of Experimental Botany 2000, 51:1969-1977.
6. Blouin M., Barot S., Lavelle P. Earthworms (Millsonia anomala, Megascolecidae) do not increase rice growth through enhanced nitrogen mineralization. Soil Biology & Biochemistry 2005, 38:2063-2068.
7. Bonkowski M., Scheu S. Biotic interactions in the rhizosphere: effects on plant growth and herbivore development. Insects and Ecosystem Functioning 2004, 71-91. Springer, Heidelberg. W.W. Weisser, E. Sieman (Eds.).
8. Bonkowski M. Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 2004, 162:617-631.
9. Chamberlain P.M., McNamara N.P., Chaplow J., Stott A.W., Black H.I.J. Translocation of surface litter carbon into soil by Collembola. Soil Biology & Biochemistry 2006, 38:2655-2664.
10. Cole L., Dromph K.M., Boaglio V., Bardgett R.D. Effect of density and species richness of soil mesofauna on nutrient mineralisation and plant growth. Biology and Fertility of Soils 2004, 39:337-343.
11. Curl E.A., Truelove B. The Rhizosphere 1986, Springer, New York.
12. Degenkolbe T., Hannah M.A., Freund S., Hincha D.K., Heyer A.G., Köhl K.I. A quality-controlled microarray method for gene expression profiling. Analytical Biochemistry 2005, 346:217-224.
13. Dromph K.M. Collembolans as vectors of entomopathogenic fungi. Pedobiologia 2003, 47:245-256.
14. Endlweber K., Scheu S. Effects of Collembola on root properties of two competing ruderal plant species. Soil Biology & Biochemistry 2006, 38:2025-2031.
15. Endlweber K., Scheu S. Interactions between mycorrhizal fungi and Collembola: effects on root structure of competing plant species. Biology and Fertility of Soils 2007, 43:741-749.
16. Endlweber K., Ruess L., Scheu S. Collembola switch diet in presence of plant roots thereby functioning as herbivores. Soil Biology & Biochemistry 2009, 41:1151-1154.
17. Erb M., Ton J., Degenhardt J., Turlings T.C.J. Interactions between arthropod induced aboveground and belowground defenses in plants. Plant Physiology 2008, 146:867-874.
18. Friberg H., Lagerlof J., Ramert B. Influence of soil fauna on fungal plant pathogens in agricultural and horticultural systems. Biocontrol Science and Technology 2005, 15:641-658.
19. Frost C.J., Mescher M.C., Carlson J.E., De Moraes C.M. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiology 2008, 146:818-824.
20. Fuller V.L., Lilley C.J., Atkinson H.J., Urwin P.E. Differential gene expression in Arabidopsis following infection by plant-parasitic nematodes Meloidogyne incognita and Heterodera schachtii. Molecular Plant Pathology 2007, 8:595-609.
21. Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review Phytopathology 2005, 43:205-227.
22. Glombitza S., Dubuis P.H., Thulke O., Welzl G., Bovet L., Gotz M., Affenzeller M., Geist B., Hehn A., Asnaghi C., Ernst D., Seidlitz H.K., Gundlach H., Mayer K.F., Martinoia E., Werck-Reichhart D., Mauch F., Schäffner A.R. Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Molecular Biology 2004, 54:817-835.
23. Goda H., Sasaki E., Akiyama K., Maruyama-Nakashita A., Nakabayashi K., Li W., Ogawa M., Yamauchi Y., Preston J., Aoki K., Kiba T., Takatsuto S., Fujioka S., Asami T., Nakano T., Kato H., Mizuno T., Sakakibara H., Yamaguchi S., Nambara E., Kamiya Y., Takahashi H., Hirai M.Y., Sakurai T., Shinozaki K., Saito K., Yoshida S., Shimada Y. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant Journal 2008, 55:526-542.
24. Gormsen D., Olsson P.A., Hedlund K. The influence of collembolans and earthworms on AM fungal mycelium. Applied Soil Ecology 2004, 27:211-220.
25. Gutjahr C., Paszkowski U. Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Molecular Plant Microbe Interactions 2009, 22:763-772.
26. Harris K.K., Boerner R.E.J. Effects of belowground grazing by Collembola on growth, mycorrhizal infection, and P-uptake of Geranium-robertianum. Plant and Soil 1990, 129:203-210.
27. Heil M., Baldwin I.T. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends in Plant Science 2002, 7:61-67.
28. Jammes F., Lecomte P., de Almeida-Engler J., Bitton F., Martin-Magniette M.-L., Renou J.P., Abad P., Favery B. Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant Journal 2005, 44:447-458.
29. Kilian J., Whitehead D., Horak J., Wanke D., Weinl S., Batistic O., D'Angelo C., Bornberg-Bauer E., Kudla J., Harter K. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant Journal 2007, 50:347-363.
30. Kreuzer K., Bonkowski M., Langel R., Scheu S. Decomposer animals (Lumbricidae, Collembola) and organic matter distribution affect the performance of Lolium perenne (Poaceae) and Trifolium repens (Fabaceae). Soil Biology & Biochemistry 2004, 36:2005-2011.
31. Krome K., Rosenberg K., Bonkowski M., Scheu S. Grazing of protozoa on rhizosphere bacteria alters growth and reproduction of Arabidopsis thaliana. Soil Biology & Biochemistry 2009, 41:1866-1873.
32. Lohmann M., Scheu S., Müller C. Decomposers and root feeders interactively affect plant defence in Sinapis alba. Oecologia 2009, 160:289-298.
33. Lussenhop J., Bassirirad H. Collembola. Effects on plant mass and nitrogen acquisition by ash seedlings (Fraxinus pennsylvanica). Soil Biology & Biochemistry 2005, 37:645-650.
34. Megias A.G., Müller C. Root herbivores and detritivores shape above-ground multitrophic assemblage through plant-mediated effects. Journal of Animal Ecology 2010, 79:923-931.
35. Mikkelsen M.D., Hansen C.H., Wittstock U., Halkier B.A. Cytochrome P450cyp79b2 from Arabidopsis catalyzes the conversion of tryptophane to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. Journal of Biological Chemistry 2000, 275:33712-33717.
36. Partsch S., Milcu A., Scheu S. Decomposers (Lumbricidae, Collembola) affect plant performance in model grasslands of different diversity. Ecology 2006, 87:2548-2558.
37. Péret B., Bert de Rybel B., Casimiro I., Benkova E., Swarup R., Laplaze L., Beeckmam T., Bennett M.J. Arabidopsis lateral root development: an emerging story. Trends in Plant Science 2009, 14:399-408.
38. Perilli S., Moubayidin L., Sabatini S. The molecular basis of cytokinin function. Current Opinion in Plant Biology 2010, 13:21-26.
39. Phillips D.A., Ferris H., Cook D.R., Strong D.R. Molecular control points in rhizosphere food webs. Ecology 2003, 84:816-826.
40. Pieterse C.M.J., Van Wees S.C.M., Ton J., Van Pelt J.A., Van Loon L.C. Signalling in Rhizobacteria-induced systemic resistance in Arabidopsis thaliana. Plant Biology 2002, 4:535-544.
41. Pieterse C.M., Leon-Reyes A., Van der Ent S., Van Wees S.C. Networking by small-molecule hormones in plant immunity. Nature Chemical Biololgy 2009, 5:308-316.
42. Pollmann S., Muller A., Weiler E.W. Many roads lead to " Auxin": of nitrilases, synthases, and amidases. Plant Biology 2006, 8:326-333.
43. Poultney C.S., Gutiérrez R.G., Katari M.S., Gifford M.L., Paley W.B., Coruzzi G.M., Shasha D.E. Sungear: interactive visualization and functional analysis of genomic datasets. Bioinformatics 2007, 23:259-261.
44. Rosenberg K., Bertaux J., Krome K., Hartmann A., Scheu S., Bonkowski M. Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME Journal 2009, 3:675-684.
45. Schenk P.M., Kazan K., Wilson I., Anderson J.P., Richmond T., Somerville S.C., Manners J.M. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Science of the USA 2000, 97:11655-11660.
46. Scheu S., Theenhaus A., Jones T.H. Links between the detritivore and the herbivore system: effects of earthworms and Collembola on plant growth and aphid development. Oecologia 1999, 119:541-551.
47. Scheu S. Plants and generalist predators as links between the below ground and above-ground system. Basic and Applied Ecology 2001, 2:3-13.
48. Schiefelbein J. Constructing a plant cell. The genetic control of root hair development. Plant Physiology 2000, 124:1525-1531.
49. Siemens D.H., Garner S.H., Mitchell-Olds T., Callaway R.M. Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 2002, 83:505-517.
50. Smyth G.K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology 2004, 3. Article 3. 10.2202/1544-6115.1027.
51. Sorin C., Negroni L., Balliau T., Corti H., Jacquemot M.-P., Davanture M., Sandberg G., Zivy M., Bellini C. Proteomic analysis of different mutant genotypes of Arabidopsis led to the identification of 11 proteins correlating with adventitious root development. Plant Physiology 2006, 140:349-364.
52. Stout M.J., Workman K.V., Duffey S.S. Identity, spatial distribution, and variability of induced chemical responses in tomato plants. Entomolgica Experimentalis et Applicata 1996, 79:255-271.
53. Theenhaus A., Scheu S., Schaefer M. Contramensal interactions between two Collembolan species: effects on population development and on soil processes. Functional Ecology 1999, 13:238-246.
54. Thimm T., Hoffmann A., Borkott H., Munch J.C., Tebbe C.C. The gut of the soil microarthropod Folsomia candida (Collembola) is a frequently changeable but selective habitat and a vector for microorganisms. Applied and Environmental Microbiology 1998, 64:2660-2669.
55. Thimm T., Hoffmann A., Fritz I., Tebbe C.C. Contribution of the earthworm Lumbricus rubellus (Annelida, Oligochaeta) to the establishment of plasmids in soil bacterial communities. Microbial Ecology 2001, 41:341-351.
56. Tiunov A.V., Scheu S. Arbuscular Mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi. Oecologia 2005, 142:636-642.
57. van Dam N.M., Witjes L., Svatos A. Interactions between aboveground and belowground induction of glucosinolates in two wild Brassica species. New Phytologist 2004, 161:801-810.
58. Visser S., Parkinson D., Hassal M. Fungi associated with Onychiurus subtenius (Collembola) in an aspen woodland. Canadian Journal of Botany 1987, 65:635-642.
59. Wurst S., Dugassa-Gobena D., Langel R., Bonkowski M., Scheu S. Combined effects of earthworms and vesicular-arbuscular mycorrhiza on plant and aphid performance. New Phytologist 2004, 163:169-176.
60. Wurst S., Langel R., Rodger S., Scheu S. Effects of belowground biota on primary and secondary metabolites in Brassica oleracea. Chemoecology 2006, 16:69-73.
61. Zhao Y.D., Hull A.K., Gupta N.R., Goss K.A., Alonso J., Ecker J.R., Normanly J., Chory J., Celenza J.L. Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Gene Development 2002, 16:3100-3112.
62. Zimmermann P., Hirsch-Hoffmann M., Hennig L., Gruissem W. Genevestigator. Arabidopsis microarray database and analysis toolbox. Plant Physiology 2004, 136:2621-2632.