Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants

Plant and Soil

Volumn 328, Issue 1, 2010, Pages 191-201

  Krome, K ^a   Rosenberg, K ^a   Dickler, C ^a   Kreuzer, K ^a   Ludwig Muller J ^b   Ullrich Eberius, C ^a   Scheu, S ^a   Bonkowski, M ^a,c  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Acanthamoeba castellanii; Auxin; Cytokinin; Lateral roots; Rhizosphere bacteria; Root architecture

Indexed keywords

BACTERIVORY; ENVIRONMENTAL CONDITIONS; EXPERIMENTAL STUDY; GENOME; GROWTH RATE; HERB; HORMONE; METABOLISM; MICROBIAL COMMUNITY; PROTOZOAN; RHIZOSPHERE; ROOT ARCHITECTURE; SHOOT; SOIL MICROORGANISM;

ACANTHAMOEBA CASTELLANII; AMOEBA (GENUS); ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); LEPIDIUM SATIVUM; PROTOZOA;

EID: 77049113521     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-009-0101-3     Document Type: Article

References (67)

1. Alphei J, Bonkowski M, Scheu S (1996) Protozoa, nematoda and lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106: 111-126.
2. Barbieri P, Galli E (1993) Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic-acid production. Res Microbiol 144: 69-75.
3. Barbieri P, Zanelli T, Galli E, Zanetti G (1986) Wheat inoculation with Azospirillum brasilense Sp6 and some mutants altered in nitrogen-fixation and indole-3-acetic-acid production. FEMS Microbiol Lett 36: 87-90.
4. Bhalerao RP, Eklöf J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J 29: 325-332.
5. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
6. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162: 617-631.
7. Bonkowski M, Brandt F (2002) Do soil protozoa enhance plant growth by hormonal effects? Soil Biol Biochem 34: 1709-1715.
8. Bonkowski M, Griffiths B, Scrimgeour C (2000) Substrate heterogeneity and microfauna in soil organic 'hotspots' as determinants of nitrogen capture and growth of ryegrass. Appl Soil Ecol 14: 37-53.
9. Bonkowski M, Geoghegan IE, Birch ANE, Griffiths BS (2001) Effects of soil decomposer invertebrates (protozoa and earthworms) on an above-ground phytophagous insect (cereal aphid) mediated through changes in the host plant. Oikos 95: 441-450.
10. Campanella J, Ludwig-Müller J, Bakllamaia V, Sharma V, Cartier A (2003) ILR1 and sILR1 IAA amidohydrolase homologs differ in expression pattern and substrate specificity. Plant Growth Regul 41: 215-223.
11. Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inz D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13: 843-852.
12. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett M (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8: 165-171.
13. Celenza J, Grisafi P, Fink G (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9: 2131-2142.
14. Chen K-H, Miller AN, Patterson GW, Cohen JD (1988) A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis. Plant Physiol 86: 82-825.
15. Clarholm M (1985) Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen. Soil Biol Biochem 17: 181-187.
16. Coenen C, Lomax T (1997) Auxin-cytokinin interactions in higher plants: old problems and new tools. Trends in Plant Science 2: 351-356.
17. Cohen JD (1984) Convenient apparatus for the generation of small amounts of diazomethane. Journal of Chromatography A 303: 193-196.
18. Cohen JD, Baldi BG, Slovin JP (1986) 13C6 [benzene ring]-indole-3-acetic acid: a new internal standard for quantitative mass-spectral analysis of indole-3-acetic-acid in plants. Plant Physiol 80: 14-19.
19. D'Agostino IB, Deruère J, Kieber JJ (2000) Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol 124: 1706-1717.
20. Deruère J, Kieber JJ (2002) Molecular mechanisms of cytokinin signaling. J Plant Growth Regul 21: 32-39.
21. Dobbelaere S, Croonenborghs A, Thys A, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre J, Kapulnik Y, Brener S, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Austr J Plant Physiol 28: 871-879.
22. Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84: 827-837.
23. Frankenberger W, Arshad M (1995) Phytohormones in soils: microbial production and function. Marcel Dekker, New York, p 503.
24. Griffiths BS (1989) Enhanced nitrification in the presence of bacteriophagous protozoa. Soil Biol Biochem 21: 1045-1051.
25. Griffiths BS, Bonkowski M, Dobson G, Caul S (1999) Changes in soil microbial community structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia 43: 297-304.
26. Griffiths B, Christensen S, Bonkowski M (2007) Microfaunal interactions in the rhizosphere, how nematodes and protozoa link above- and belowground processes. In: Cardon Z, Whitbeck J (eds) The rhizosphere-an ecological perspective. Elsevier, Amsterdam, pp 57-71.
27. Henry F, Nguyen C, Paterson E, Sim A, Robin C (2005) How does nitrogen availability alter rhizodeposition in Lolium multiflorum Lam. during vegetative growth? Plant Soil 269: 181-191.
28. Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inze D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339-2351.
29. Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57: 401-411.
30. Jefferson R, Kavanagh T, Bevan M (1987) GUS fusions: ß-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6: 3901-3907.
31. Jentschke G, Bonkowski M, Godbold DL, Scheu S (1995) Soil protozoa and forest tree growth: non-nutritional effects and interaction with mycorrhizae. Biol Fertil Soils 20: 263-269.
32. Kreuzer K, Adamczyk J, Iijima M, Wagner M, Scheu S, Bonkowski M (2006) Grazing of a common species of soil protozoa (Acanthamoeba castellanii) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biol Biochem 38: 1665-1672.
33. Kuikman PJ, Jansen AG, van Veen JA (1991) 15N-nitrogen mineralization from bacteria by protozoan grazing at different soil moisture regimes. Soil Biol Biochem 23: 193-200.
34. Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions. Trends Microbiol 8: 298-300.
35. Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB, Offringa R, Graham N, Doumas P, Friml J, Bogusz D, Beeckman T, Bennett M (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19: 3889-3900.
36. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R (2006) Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol 47: 788-792.
37. Li X, Mo X, Shou H, Wu P (2006) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant Cell Physiol 47: 1112-1123.
38. Lucas M, Godin C, Jay-Allemand C, Laplaze L (2008) Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. J Exp Bot 59: 55-66.
39. Malamy JE (2005a) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67-77.
40. Malamy JE (2005b) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Eviron 28: 67-77.
41. Malamy J, Benfey P (1997a) Lateral root formation in Arabidopsis thaliana. Plant Physiol 114: 277-277.
42. Malamy J, Benfey P (1997b) Down and out in Arabidopsis: the formation of lateral roots. Trends Plant Sci 2: 390-396.
43. Mao X, Hu F, Griffiths B, Li H (2006) Bacterial-feeding nematodes enhance root growth of tomato seedlings. Soil Biol Biochem 38: 1615-1622.
44. Mao X, Hu F, Griffiths B, Chen X, Liu M, Li H (2007) Do bacterial-feeding nematodes stimulate root proliferation through hormonal effects? Soil Biol Biochem 39: 1816-1819.
45. Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37: 128-138.
46. Mulkey T, Kuzmanoff K, Evans M (1982) Promotion of growth and hydrogen ion efflux by auxin in roots of maize pretreated with ethylene biosynthesis inhibitors. Plant Physiol 70: 186-188.
47. Page FC (1976) An illustrated key to freshwater and soil amoebae. Freshwater Biological Association 34, p 11.
48. Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Europ J Soil Sci 54: 741-750.
49. Patten C, Glick B (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42: 207-220.
50. Patten C, Glick B (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68: 3795-3801.
51. Reed RC, Brady SR, Muday GK (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol 118: 1369-1378.
52. Rønn R, McCaig A, Griffiths B, Prosser J (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microbiol 68: 6094-6105.
53. Rosenberg K, Krome K, Bertaux J, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME Journal 3: 675-684.
54. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463-472.
55. Sakakibara H (2003) Nitrate-specific and cytokinin-mediated nitrogen signaling pathways in plants. J Plant Res 116: 253-257.
56. Samuelson ME, Larsson CM (1993) Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N assimilation and comparison with ammonium. Plant Sci 93: 77-84.
57. Scott T (1972) Auxins and roots. Ann Rev Plant Physiol 23: 235-258.
58. Seidel C, Walz A, Park S, Cohen JD, Ludwig-Müller J (2006) Indole-3-acetic acid protein conjugates: novel players in auxin homeostasis. Plant Biol 8: 340-345.
59. Takei K, Takahashi T, Sugiyama T, Yamaya T, Sakakibara H (2002) Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin. J Exp Bot 53: 971-977.
60. Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45: 1053-1062.
61. Ulmasov T, Murfett J, Hagen G, Guilfoyle T (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
62. Verhagen FJM, Hagemann PEJ, Woldendorp JW, Laanbroek HJ (1994) Competition for ammonium between nitrifying bacteria and plant roots in soil in pots; effects of grazing by flagellates and fertilization. Soil Biol Biochem 26: 89-96.
63. Vessey J (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255: 571-586.
64. Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Nat Am Soc 98: 10487-10492.
65. Werner T, Motyka V, Laucou V, Smets R, van Onckelen H, Schmülling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532-2550.
66. Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida Cr12-2 that overproduce indoleacetic acid. Current Microbiol 32: 67-71.
67. Zhang H, Forde B (2000) Regulation of Arabidopsis root development by nitrate availability. J Exp Bot 51: 51-59.