Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains

Plant and Soil

Volumn 374, Issue 1-2, 2014, Pages 689-700

  Zhang, Nan ^a,b   Wang, Dandan ^a,b   Liu, Yunpeng ^a,b   Li, Shuqing ^a,b   Shen, Qirong ^a,b   Zhang, Ruifu ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b AGRO ENVIRONMENTAL PROTECTION INSTITUTE   (China)

Author keywords

Biofilm formation; Chemotaxis; Colonization; Organic acids; PGPR; Root exudates

Indexed keywords

AGRICULTURAL PRODUCTION; BIOFILM; CITRIC ACID; COLONIZATION; GENETIC ANALYSIS; GROWTH RESPONSE; HOST PLANT; MICROBIAL ACTIVITY; ORGANIC ACID; RHIZOSPHERE; ROOT SYSTEM;

EID: 84890890543     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-013-1915-6     Document Type: Article

References (50)

1. Adler J (1973) A method for measuring chemotaxis and use of the method to determine optimum conditions for chemotaxis by Escherichia coli. J Gen Microbiol 74: 77-91.
2. Andersen PC, Brodbeck BV, Oden S, Shriner A, Leite B (2007) Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiol Lett 274: 10-217.
3. Bacilio-Jimenez M, Aguilar-Flores S, Ventura-Zapata E, Perez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249: 271-277.
4. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32: 666-681.
5. Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20: 642-650.
6. Badri DV, Chaparro JM, Zhang RF, Shen QR, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288: 4502-4512.
7. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9: 26-32.
8. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
9. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. PNAS 98: 11621-11626.
10. 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.
11. Broz AK, Manter DK, Vivanco JM (2007) Soil fungal abundance and diversity: another victim of the invasive plant Centaurea maculosa. ISME J 1: 763-765.
12. Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, Shen Q (2011) Bacillus subtilis SQR 9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils 47: 495-506.
13. Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo J, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85: 418-430.
14. Compant S, Duffy B, Nowak J, Clement C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71: 4951-4959.
15. Compant S, Clement C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42: 669-678.
16. de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mol R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15: 1173-1180.
17. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72: 313-327.
18. Fan B, Chen X, Budiharjo A, Bleiss W, Vater J, Borriss R (2011) Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein. J Biotechnol 151: 303-311.
19. Fan B, Borriss R, Bleiss W, Wu X (2012) Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants in different patterns. J Microbiol 50: 38-44.
20. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37: 395-412.
21. Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42: 1199-1209.
22. Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321: 235-257.
23. Jakoby M, Wang H, Reidt W, Weisshaar B, Bauer P (2004) FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577: 528-534.
24. Jones DL (1998) Organic acids in the rhizosphere - a critical review. Plant Soil 205: 25-44.
25. Kloepper JW, Schroth MN (1978) Plant growth-promoting rhizobacteria on radishes. In: Station de pathologie vegetale et phyto-bacteriologie (ed) Proceedings of the 4th International Conference on Plant Pathogenic Bacteria. Gilbert-Clarey, Tours.
26. Li S, Zhang N, Zhang Z, Luo J, Shen B, Zhang R, Shen Q (2013) Antagonist Bacillus subtilis HJ5 controls Verticillium wilt of cotton by root colonization and biofilm formation. Biol Fertil Soils 49: 295-303.
27. Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol 47: 374-379.
28. Liu X, Parales RE (2008) Chemotaxis of Escherichia coli to pyrimidines: a new role for the signal transducer tap. J Bacteriol 190: 972-979.
29. Lugtenberg BJJ, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541-556.
30. Marschner P, Crowley D, Yang CH (2004) Development of specific rhizosphere bacterial communities in relation to plant species, nutrition and soil type. Plant Soil 261: 199-208.
31. Micallef SA, Channer S, Shiaris MP, Colon-Carmona A (2009) Plant age and genotype impact the progression of bacterial community succession in the Arabidopsis rhizosphere. Plant Signal Behav 4: 777-780.
32. Morgan JA, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56: 1729-1739.
33. Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLOS ONE 7: e35498.
34. Phillips DA, Fox TC, King MD, Bhuvaneswari TV, Teuber LR (2004) Microbial products trigger amino acid exudation from plant roots. Plant Physiol 136: 2887-2894.
35. Qiu M, Zhang R, Xue C, Zhang S, Li S, Zhang N, Shen Q (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils 48: 807-816.
36. Rudrappa T, Czymmek KJ, Pare PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148: 1547-1556.
37. Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol Ecol 45: 219-227.
38. Soto MJ, Sanjuan J, Olivares J (2006) Rhizobia and plant-pathogenic bacteria: common infection weapons. Microbiol 152: 3167-3174.
39. Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator. J Bacteriol 185: 1951-1957.
40. Stepanovic S, Dakic I, Opavski N, Jezek P, Ranin L (2003) Influence of the growth medium composition on biofilm formation by Staphylococcus sciuri. Ann Microbiol 53: 63-74.
41. Sun S, Wang J, Zhu L, Liao D, Gu M, Ren L, Kapulnik Y, Xu G (2012) An active factor from tomato root exudates plays an important role in efficient establishment of mycorrhizal symbiosis. PLOS ONE 7: e43385.
42. Timmusk S, Grantcharova N, Wagner EG (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71: 7292-7300.
43. Walker TS, Bais HP, Deziel E, Schweizer HP, Rahme LG, Fall R, Vivanco JM (2004) Pseudomonas aeruginosa- plant root interactions, pathogenicity, biofilm formation, and root exudation. Plant Physiol 134: 320-331.
44. Weng J, Wang Y, Li J, Shen Q, Zhang R (2012) Enhanced root colonization and biocontrol activity of B. amyloliquefaciens SQR-9 by abrB gene desruption. Appl Microbiol Biotechnol. doi: 10. 1007/s00253-012-4572-4.
45. Wieland G, Neumann R, Backhaus H (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67: 5849-5854.
46. Xu H (2011) D-Amino acid mitigated membrane biofouling and promoted biofilm. J Membr Sci 376: 266-274.
47. Xu Z, Shao J, Li B, Yan X, Shen Q, Zhang R (2013) Contribution of bacillomycin D in Bacillus amyloliquefaciens SQR9 to antifungal activity and biofilm formation. Appl Environ Microbiol 79: 808-815.
48. Yaryura PM, Leon M, Correa OS, Kerber NL, Pucheu NL, Garcia AF (2008) Assessment of the role of chemotaxis and biofilm formation as requirements for colonization of roots and seeds of soybean plants by Bacillus amyloliquefaciens BNM339. Curr Microbiol 56: 625-632.
49. Zhang N, Wu K, He X, Li S, Zhang Z, Shen B, Yang X, Zhang R, Huang Q, Shen Q (2011) A new bioorganic fertilizer can effectively control banana wilt by strong colonization with Bacillus subtilis N11. Plant Soil 344: 87-97.
50. Zohora US, Rahman MS, Ano T (2009) Biofilm formation and lipopeptide antibiotic iturin A production in different peptone media. J Environ Sci Supplement: S24-S27.