Abstract
This paper reviews strategies for manipulating plants and their root-associated microorganisms to improve plant health and productivity. Some strategies directly target plant processes that impact on growth, while others are based on our knowledge of interactions among the components of the rhizosphere (roots, microorganisms and soil). For instance, plants can be engineered to modify the rhizosphere pH or to release compounds that improve nutrient availability, protect against biotic and abiotic stresses, or encourage the proliferation of beneficial microorganisms. Rhizobacteria that promote plant growth have been engineered to interfere with the synthesis of stress-induced hormones such as ethylene, which retards root growth, and to produce antibiotics and lytic enzymes active against soilborne root pathogens. Rhizosphere engineering also can involve the selection by plants of beneficial microbial populations. For example, some crop species or cultivars select for and support populations of antibiotic-producing strains that play a major role in soils naturally suppressive to soil-borne fungal pathogens. The fitness of root-associated bacterial communities also can be enhanced by soil amendment, a process that has allowed the selection of bacterial consortia that can interfere with bacterial pathogens. Plants also can be engineered specifically to influence their associated bacteria, as exemplified by quorum quenching strategies that suppress the virulence of pathogens of the genus Pectobacterium. New molecular tools and powerful biotechnological advances will continue to provide a more complete knowledge of the complex chemical and biological interactions that occur in the rhizosphere, ensuring that strategies to engineer the rhizosphere are safe, beneficial to productivity, and substantially improve the sustainability of agricultural systems.
Abbreviations
- ACC:
-
1-aminocyclopropane-1-carboxylate
- ALMT:
-
Al3+-activated malate transporter
- DAPG:
-
2,4-diacetylphloroglucinol
- EST:
-
expressed sequence tags
- Ggt :
-
Gaeumannomyces graminis var. tritici
- MATE:
-
multidrug and toxic compound extrusion
- NAHL:
-
N-acyl homoserine lactone
- PCA:
-
phenazine-1-carboxylic acid
- PGPR:
-
plant growth-promoting rhizobacteria
- QS:
-
quorum-sensing
- QTL:
-
quantitative trait locus(i)
- TAD:
-
take-all decline
References
Allende-Molar R (2006) Role of 2, 4-diacetylphloroglucinol-producing Pseudomonas fluorescens in suppression of take-all and Pythium root rots of wheat. Department of Plant Pathology. Washington State University, Pullman, WA USA
Alsanius BW, Hultberg M, Englund JE (2002) Effect of lacZY-marking of the 2, 4-diaceyl-phloroglucinol producing Pseudomonas fluorescens strain 5–2/4 on its physiological performance and root colonization ability. Microbial Res 157:39–45
Anoop VM, Basu U, McCammon MT, McAlister-Henn L, Taylor GJ (2003) Modulation of citrate metabolism alters aluminum tolerance in yeast and transgenic canola overexpressing a mitochondrial citrate synthase. Plant Physiol 132:2205–2217
Asano N, Oseki K, Tomioka E, Kizu H, Matsui K (1994) N-containing sugars from Morus alba and their glycosidase inhibitory activities. Carbohydr Res 259:243–255
Asano N, Kato A, Kizu H, Matsui K, Watson AA, Nash RJ (1996) Calystegine B4, a novel trehalase inhibitor from Scopolia japonica. Carbohydr Res 293:195–204
Atkinson TG, Neal JL Jr, Larson RI (1975) Genetic control of the rhizosphere microflora of wheat. In: Bruehl GW (ed) Biology and Control of Soil-Borne Plant Pathogens. Am Phytopathol Soc, Saint-Paul, pp 116–122
Baker KF, Cook RJ (1974) Biological control of plant pathogens. Am Phytopathol Soc, Saint Paul, MN, p 433
Bankhead SB, Landa BB, Lutton E, Weller DM, Gardener BBM (2004a) Minimal changes in rhizobacterial population structure following root colonization by wild type and transgenic biocontrol strains. FEMS Microbiol Ecol 49:307–318
Bankhead SB, Schroeder K, Son MY, Thomashow LS, Weller DM (2004) Population dynamics and movement of transgenic Pseudomonas fluorescens in the rhizosphere of field-grown wheat. In: Hartmann A, Schmid M, Wenzel W, Hinsinger Ph (eds) Rhizosphere 2004: Perspectives and Challenges. A Tribute to Lorenz Hiltner. GSF Forschungszentrum, p 165
Barnard AM, Bowden SD, Burr T, Coulthurst SJ, Monson RE, Salmond GP (2007) Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos Trans R Soc Lond B Biol Sci 362:1165–1183
Bergsma-Vlami M, Prins ME, Raaijmakers JM (2005) Influence of plant species on population dynamics, genotypic diversity and antibiotic production in the rhizosphere by indigenous Pseudomonas spp. FEMS Microbiol Ecol 52:59–69
Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Adv Agron 66:1–102
Chin-A-Woeng TF, van den Broek D, de Voer G, van der Drift KM, Tuinman S, Thomas-Oates JE, Lugtenberg BJ, Bloemberg GV (2001) Phenazine-1-carboxamide production in the biocontrol strain Pseudomonas chlororaphis PCL1391 is regulated by multiple factors secreted into the growth medium. Mol Plant Microbe Interact 14:969–979
Cirou A, Diallo S, Kurt C, Latour X, Faure D (2007) Growth promotion of quorum-quenching bacteria in the rhizosphere of Solanum tuberosum. Environ Microbiol 9:1511–1522
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Colbert SF, Hendson M, Ferri M, Schroth MN (1993a) Enhanced growth and activity of a biocontrol bacterium genetically engineered to utilize salicylate. Appl Environ Microbiol 59:2071–2076
Colbert SF, Schroth MN, Weinhold AR, Hendson M (1993b) Enhancement of population densities of Pseudomonas putida ppg7 in agricultural ecosystems by selective feeding with the carbon source salicylate. Appl Environ Microbiol 59:2064–2070
Colores GM, Macur RE, Ward DM, Inskeep WP (2000) Molecular analysis of surfactant-driven microbial population shifts in hydrocarbon-contaminated soil. Appl Environ Microbiol 66:2959–2964
Cook RJ (2003) Take-all of wheat. Physiol Mol Plant Path 62:73–86
Craig N (2002) Tn7. In: Craig N, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. ASM, Washington, DC, pp 423–456
D’Angelo-Picard C, Faure D, Carlier A, Uroz S, Raffoux A, Fray R, Dessaux Y (2004) Bacterial populations in the rhizosphere of tobacco plants producing the quorum-sensing signals hexanoyl-homoserine lactone and 3-oxo-hexanoyl-homoserine lactone. FEMS Microbiol Ecol 51:19–29
D’Angelo-Picard C, Faure D, Penot I, Dessaux Y (2005) Diversity of N-acyl homoserine lactone-producing and -degrading bacteria in soil and tobacco rhizosphere. Environ Microbiol 7:1796–1808
de la Fuente JM, Ramírez-Rodríguez V, Cabrera-Ponce JL, Herrera-Estrella L (1997) Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276:1566–1568
de la Fuente-Martinez JM, Herrera-Estrella L (1999) Advances in the understanding of aluminum toxicity and the development of aluminum-tolerant transgenic plants. Adv Agron 66:103–120
De La Fuente L, Landa BB, Weller DM (2006) Host crop affects rhizosphere colonization and competitiveness of 2, 4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 96:751–762
De Leij FAAM, Thomas CE, Bailey MJ, Whipps JM, Lynch JM (1998) Effect of insertion site and metabolic load on the environmental fitness of a genetically modified Pseudomonas fluorescens isolate. Appl Environ Microbiol 64:2634–2638
de Sousa CNA (1998) Classification of Brazilian wheat cultivars for aluminium toxicity in acid soil. Plant Breed 117:217–221
de Souza JT, Weller DM, Raaijmakers JM (2003) Frequency, diversity, and activity of 2, 4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in Dutch take-all decline soils. Phytopathology 93:4–63
Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium tolerance and mineral nutrition. FEBS Lett 581:2255–2262
Delhaize E, Hebb DM, Ryan PR (2001) Expression of a Pseudomonas aeruginosa citrate synthase gene in tobacco is not associated with either enhanced citrate accumulation or efflux. Plant Physiol 125:2059–2067
Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA 101:15249–15254
Delhaize E, Ryan PR, Hocking PJ, Richardson AE (2003) Effects of altered citrate synthase and isocitrate dehydrogenase expression on internal citrate concentrations of tobacco (Nicotiana tabacum L.). Plant Soil 248V:137–144
Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702
Dessaux Y, Petit A, Farrand SK, Murphy PM (1998) Opines and opine-like molecules in plant-Rhizobiaceae interactions. In: Kondorosi A, Spaink H, Hooykaas P (eds) The Rhizobiaceae. Kluwer Academic, Dordrecht, pp 173–197
Devliegher W, Arif M, Verstraete W (1995) Survival and plant growth promotion of detergent-adapted Pseudomonas fluorescens ANP15 and Pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol 61:3865–3871
Di Gregorio S, Barbafieri M, Lampis S, Sanangelantoni AM, Tassi E, Vallini G (2006) Combined application of Triton X-100 and Sinorhizobium sp. Pb002 inoculum for the improvement of lead phytoextraction by Brassica juncea in EDTA amended soil. Chemosphere 63:293–299
Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108:183–200
Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97:3526–3531
Dong YH, Wang LH, Xu JL, Zhang HB, Zhang XF, Zhang LH (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813–817
Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759
Downing K, Thomson JA (2000) Introduction of the Serratia marcescens chiA gene into an endophytic Pseudomonas fluorescens for the biocontrol of phytopathogenic fungi. Can J Microbiol 46:363–369
Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol 144:197–205
Eckardt NA (2001) Move it on out with MATEs. Plant Cell 13:1477–1480
Faure D, Dessaux Y (2007) Novel biocontrol strategies directed at Pectobacterium carotovorum. Eur J Plant Pathol 119:353–365
Fox PM, Borthakur D (2001) Selection of several classes of mimosine-degradation-defective Tn3Hogus-insertion mutants of Rhizobium sp. strain TAL1145 on the basis of mimosine-inducible GUS activity. Can J Microbiol 47:488–494
Fray RG (2002) Altering plant-microbe interaction through artificially manipulating bacterial quorum sensing. Ann Bot (Lond) 89:245–253
Fray RG, Throup JP, Daykin M, Wallace A, Williams P, Stewart GS, Grierson D (1999) Plants genetically modified to produce N-acylhomoserine lactones communicate with bacteria. Nat Biotechnol 17:1017–1020
Freeman J, Ward E (2004) Gaeumannomyces graminis, the take-all fungus and its relatives. Mol Plant Pathol 5:235–252
Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091
Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214
Gévaudant F, Duby G, von Stedingk E, Zhao RM, Morsomme P, Boutry M (2007) Expression of a constitutively activated plasma membrane H+-ATPase alters plant development and increases salt tolerance. Plant Physiol 144:1763–1776
Glandorf DCM, Verheggen P, Jansen T, Jorritsma JW, Smit E, Leeflang P, Wernars K, Thomashow LS, Laureijs E, Thomas-Oates JE, Bakker PAHM, Van Loon LC (2001) Effect of genetically modified Pseudomonas putida WCS358r on the fungal rhizosphere microflora of fieldgrown wheat. Appl Environ Microbiol 67:3371–3378
Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339
Gordon DM, Ryder MH, Heinrich K, Murphy PJ (1996) An experimental test of the rhizopine concept in Rhizobium meliloti. Appl Environ Microbiol 62:3991–3996
Hammond AC (1995) Leucaena toxicosis and its control in ruminants. J Anim Sci 73:1487–1492
Heckman JR, Clarke BB, Murphy JA (2003) Optimizing manganese fertilization for the suppression of take-all patch disease on creeping bentgrass. Crop Science 43:1395–1398
Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review. Plant Soil 248:43–59
Hoekenga OA, Maron LG, Cançado GMA, Piñeros MA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto M, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminium tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738–9743
Hornby D (1983) Suppressive soils. Ann Rev Phytopathol 21:65–85
Hornby D (1998) Take-all of cereals: a regional perspective. CAB International, Wallingford
Huang ZY, Bonsall RF, Mavrodi DV, Weller DM, Thomashow LS (2004) Transformation of Pseudomonas fluorescens with genes for biosynthesis of phenazine-1-carboxylic acid improves biocontrol of rhizoctonia root rot and in situ antibiotic production. FEMS Microbiol. Ecol. 49:243–251
Ji P, Wilson M (2003) Enhancement of population size of a biological control agent and efficacy in control of bacterial speck of tomato through salicylate and ammonium sulfate amendments. Appl Environ Microbiol 69:1290–1294
Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant-Microbe Interact 19:250–256
Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817
Koby S, Schickler H, Chet I, Oppenheim AB (1994) The chitinase encoding Tn7-based chiA gene endows Pseudomonas fluorescens with the capacity to control plant-pathogens in soil. Gene 147:81–83
Koyama H, Kawamura A, Kihara T, Hara T, Takita E, Shibata D (2000) Overexpression of mitochondrial citrate synthase in Arabidopsis thaliana improved growth on a phosphorus-limited soil. Plant Cell Physiol 41:1030–1037
Koyama H, Takita E, Kawamura A, Hara T, Shibata D (1999) Over expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium. Plant Cell Physiol 40:482–488
Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–1180
Kwak YS, Bakker PAHM, Glandorf DM, Rice JT, Paulitz TC, Weller DM (2009) Diversity, virulence and 2,4-diacetylphloroglucinol sensitivity of Gaeumannomyces graminis var. tritici isolates from Washington State. Phytopathol (in press)
Landa BB, Mavrodi OV, Raaijmakers JM, Gardener BBM, Thomashow LS, Weller DM (2002) Differential ability of genotypes of 2, 4-diacetylphloroglucinol-producing Pseudomonas fluorescens strains to colonize the roots of pea plants. Appl Environ Microbiol 68:3226–3237
Landa BB, Mavrodi OV, Schroeder KL, Allende-Molar R, Weller DM (2006) Enrichment and genotypic diversity of phlD-containing fluorescent Pseudomonas spp. in two soils after a century of wheat and flax monoculture. FEMS Microbiol Ecol 55:351–368
Leadbetter JR, Greenberg EP (2000) Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J Bacteriol 182:6921–6926
Leeflang P, Smit E, Glandorf DCM, van Hannen EJ, Wernars K (2002) Effects of Pseudomonas putida WCS358r and its genetically modified phenazine producing derivative on the Fusarium population in a field experiment, as determined by 18S rDNA analysis. Soil Biol Biochem 34:1021–1025
Lemanceau P, Corberand T, Gardan L, Latour X, Laguerre G, Boeufgras J, Alabouvette C (1995) Effect of two plant species, flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Appl Environ Microbiol 61:1004–1012
Li JS, Yang HB, Peer WA, Richter G, Blakeslee J, Bandyopadhyay A, Titapiwantakun B, Undurraga S, Khodakovskaya M, Richards EL, Krizek B, Murphy AS, Gilroy S, Gaxiola R (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125
Ligaba A, Katsuhara M, Ryan PR, Shibasaka M, Matsumoto H (2006) The BnALMT1 and BnALMT2 genes from Brassica napus L. encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol 142:1294–1303
Ligon JM, Hill DS, Hammer PE, Torkewitz NR, Hofmann D, Kempf HJ, van Pee KH (2000) Natural products with antifungal activity from Pseudomonas biocontrol bacteria. Pest Manag Sci 56:688–695
López-Bucio J, Martínez de la Vega O, Guevara-García A, Herrera-Estrella L (2000a) Enhanced phosphorus uptake in transgenic tobacco plants that overproduce citrate. Nature Biotech 18:450–453
López-Bucio J, Nieto-Jacobo MF, Ramirez-Rodriguez V, Herrera-Estrella L (2000b) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1–13
Lugtenberg BJJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39:461–490
Lynch JM (2002) Resilience of the rhizosphere to anthropogenic disturbance. Biodegradation 13:21–27
Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
Maddula VS, Zhang Z, Pierson EA, Pierson LS 3rd (2006) Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30–84. Microb Ecol 52:289–301
Mae A, Montesano M, Koiv V, Palva ET (2001) Transgenic plants producing the bacterial pheromone N-acyl-homoserine lactone exhibit enhanced resistance to the bacterial phytopathogen Erwinia carotovora. Mol Plant–Microbe Interact 14:1035–1042
Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161
Mansouri H, Petit A, Dessaux Y (2002) Engineered rhizosphere: the trophic bias generated by opine-producing plants is independent of the opine-type, the soil origin and the plant species. Appl Environ Microbiol 68:2562–2566
Mazzola M, Cook RJ, Pierson LS, Thomashow LS, Weller DM (1992) Contribution of phenazine antibiotic biosynthesis to the ecological competence of fluorescent pseudomonads in soil habitats. Appl Environ Microbiol 58:2616–2624
Mazzola M, Fujimoto DK, Thomashow LS, Cook RJ (1995) Variation in sensitivity of Gaeumannomyces graminis to antibiotics produced by fluorescent Pseudomonas spp. and effect on biological control of take-all of wheat. Appl Environ Microbiol 61:2554–2559
Mazzola M, Funnell DL, Raaijmakers JM (2004) Wheat cultivar-specific selection of 2, 4-diacetylphloroglucinol-producing fluorescent Pseudomonas species from resident soil populations. Microbiol Ecol 48:338–348
McSpadden-Gardener BB, de Bruijn FJ (1998) Detection and isolation of novel rhizopine-catabolizing bacteria from the environment. Appl Environ Microbiol 64:4944–4949
Menzies JD (1959) Occurrence and transfer of a biological factor in soil that suppresses potato scab. Phytopathology 49:648–652
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–99
Miller HJ, Henken G, van Veen JA (1989) Variation and composition of bacterial populations in the rhizosphere of maize, wheat, and grass cultivars. Can J Microbiol 35:656–660
Murphy PJ, Heycke N, Banfalvi Z, Tate ME, de Bruijn F, Kondorosi A, Tempé J, Schell J (1987) Genes for the catabolism and synthesis of an opine-like compound in Rhizobium meliloti are closely linked and on the Sym plasmid. Proc Natl Acad Sci USA 84:493–497
Murphy PJ, Trenz SP, Grzemski W, De Bruijn FJ, Schell J (1993) Rhizobium meliloti rhizopine mos locus is a mosaic structure facilitating its symbiotic regulation. J Bacteriol 175:5193–5204
Neal JL Jr, Atkinson TG, Larson RI (1970) Changes in the rhizosphere microflora of spring wheat induced by disomic substitution of a chromosome. Can J Microbiol 16:153–158
Neal JL Jr, Larson RI, Atkinson TG (1973) Changes in rhizosphere populations of selected physiological groups of bacteria related to substitution of specific pairs of chromosomes in spring wheat. Plant Soil 39:209–212
Neumann G, Römheld V (2007) The release of root exudates as affected by the root physiological status. In: Pinton R, Varanini Z, Nannipieri P (eds) The Rhizosphere: Biochemistry and organic substances at the soil-plant interface. CRC, Boca Raton, pp 23–72
Notz R, Maurhofer M, Schnider-Keel U, Duffy B, Haas D, Défago G (2001) Biotic factors affecting expression of the 2, 4-diacetylphloroglucinol biosynthesis gene phlA in Pseudomonas fluorescens biocontrol strain CHA0 in the rhizosphere. Phytopathology 91:873–81
Oger P, Petit A, Dessaux Y (1997) Transgenic plants producing opines alter their biological environment. Nature/Biotechnology 15:369–372
Oger P, Mansouri H, Dessaux Y (2000) Effect of crop rotation and soil cover on the alteration of the soil microflora generated by the culture of transgenic plants producing opines. Mol Ecol 9:881–890
Oger P, Mansouri H, Nesme X, Dessaux Y (2004) Engineering root exudation of Lotus towards the production of two novel carbon compounds leads to the selection of distinct microbial populations in the rhizosphere. Microbiol Ecol 47:96–103
Okubara PA, Bonsall RF (2008) Accumulation of Pseudomonas-derived 2, 4-diacetylphloroglucinol on wheat seedling roots is influenced by host cultivar. Biol Control 46:322–331
Omote H, Hiasa M, Matsumoto T, Otsuka M, Moriyama Y (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27:587–593
Palmgren MG (1991) Regulation of plant plasma-membrane H+-ATPase activity. Physiol Plant 83:314–323
Paulitz TC, Smiley RW, Cook RJ (2002) Insights into the prevalence and management of soilborne cereal pathogens under direct seeding in the Pacific Northwest, USA. Can J Plant Path 24:416–428
Picard C, Frascaroli E, Bosco M (2004) Frequency and biodiversity of 2, 4-diacetylphloroglucinol-producing rhizobacteria are differentially affected by the genotype of two maize inbred lines and their hybrid. FEMS Microbiol Ecol 49:207–215
Pinto R, Varanini Z, Nannipieri P (2007) The Rhizosphere: Biochemistry and organic substances at the soil-plant interface. CRC, Boca Raton
Raaijmakers JM, Weller DM (1998) Natural plant protection by 2, 4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol Plant-Microbe Interact 11:144–152
Raaijmakers JM, Weller DM (2001) Exploiting genotypic diversity of 2, 4-diacetylphloroglucinol-producing Pseudomonas spp.: characterization of superior root-colonizing P. fluorescens strain Q8r1–96. Appl Environ Microbiol 67:2545–2554
Raaijmakers JM, Bonsall RF, Weller DM (1999) Effect of population density of Pseudomonas fluorescens on production of 2, 4-diacetylphloroglucinol in the rhizosphere of wheat. Phytopathology 89:470–475
Raaijmakers JM, Weller DM, Thomashow LS (1997) Frequency of antibiotic-producing Pseudomonas spp. in natural environments. Appl Environ Microbiol 63:881–887
Richardson AE, Hadobas PA, Hayes JE (2001) Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate. Plant J 25:641–649
Rossbach S, McSpadden B, Kulpa D, de Bruijn FJ (1994) Rhizopine synthesis and catabolism genes for the creation of "biased rhizospheres" and a marker system to detect (genetically modified) microorganisms in the soil. In: Levin M, Grim C, Angle JS (eds) Biotechnology risk assessment. University of Maryland Biotechnology Insitute, College Park, pp 223–244
Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Ann Rev Plant Physiol Plant Mol Bio l 52:527–560
Ryan PR, Delhaize E, Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196:103–111
Ryan PR, Skerrett M, Flindlay G, Delhaize E, Tyerman SD (1997) Aluminium activates an anion channel in the apical cells of wheat roots. Proc Natl Acad Sci USA 94:6547–6552
Saint CP, Wexler M, Murphy PJ, Tempé J, Tate ME, Murphy PJ (1993) Characterization of genes for synthesis and catabolism of a new rhizopine induced in nodules by Rhizobium meliloti Rm220–3: extension of the rhizopine concept. J Bacteriol 175:5205–5215
Sarniguet A, Lucas P, Lucas M (1991) Relationships between take-all, soil conduciveness to the disease, populations of fluorescent pseudomonads and nitrogen fertilizers. Plant Soil 145:17–27
Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653
Savka MA, Black RC, Binns AN, Farrand SK (1996) Translocation and exudation of tumor metabolites in crown galled plants. Mol Plant Microbe Interact. 9:310–313
Savka MA, Farrand SK (1997) Modification of rhizobacterial populations by engineering bacterium utilization of a novel plant-produced resource. Nat Biotechnol 15:363–368
Savka MA, Dessaux Y, Oger P, Rossbach S (2002) Engineering bacterial competitiveness and persistence in the phytosphere. Mol Plant Microbe Interact 15:866–874
Shapira R, Ordentlich A, Chet I, Oppenheim AB (1989) Control of plant diseases by chitinase expressed from cloned DNA in Escherichia coli. Phytopathology 79:1246–1249
Siciliano SD, Fortin N, Mihoc A, Wisse G, Labelle S, Beaumier D, Ouellette D, Roy R, Whyte LG, Banks MK, Schwab P, Lee K, Greer CW (2001) Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol 67:2469–2475
Smiley RW (1979) Wheat-rhizoplane pseudomonads as antagonists of Gaeumannomyces graminis. Soil Biol Biochem 11:371–376
Soedarjo M, Hemscheidt TK, Borthakur D (1994) Mimosine, a toxin present in leguminous trees (Leucaena spp.), induces a mimosine-degrading enzyme activity in some Rhizobium strains. Appl Environ Microbiol 60:4268–4272
Soedarjo M, Borthakur D (1996) Mimosine produced by the tree legume Leucaena provides growth advantages to some Rhizobium strains that utilize it as a source of carbon and nitrogen. Plant and Soil 186:87–92
Sundheim L, Poplawsky AR, Ellingboe AH (1988) Molecular cloning of two chitinase genes from Serratia marcescens and their expression in Pseudomonas species. Physiol Molec Plant Pathol 33:483–491
Tepfer D, Goldmann A, Pamboukdjian N, Maille M, Lepingle A, Chevalier D, Dénarié J, Rosenberg C (1988) A plasmid of Rhizobium meliloti 41 encodes catabolism of two compounds from root exudate of Calystegium sepium. J Bacteriol 170:1153–1161
Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiol 127:1836–1844
Timms-Wilson TM, Ellis RJ, Renwick A, Rhodes DJ, Mavrodi DV, Weller DM, Thomashow LS, Bailey MJ (2000) Chromosomal insertion of phenazine-1-carboxylic acid biosynthetic pathway enhances efficacy of damping-off disease control by Pseudomonas fluorescens. Mol Plant-Microbe Interact 13:1293–1300
Toth IK, Newton JA, Hyman LJ, Lees AK, Daydin M, Ortori C, Williams P, Fray RG (2004) Potato plants genetically modified to produce N-acylhimoserine lactones increase susceptibility to soft rot Erwiniae. Mol Plant-Microbe Interact 17:880–887
Uroz S, D’Angelo-Picard C, Carlier A, Elasri M, Sicot C, Petit A, Oger P, Faure D, Dessaux Y (2003) Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology 149:1981–1989
Vance C, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non-renewable resource. New Phytol 157:423–447
Viebahn M, Glandorf DCM, Ouwens TWM, Smit E, Leeflang P, Wernars K, Thomashow LS, Van Loon LC, Bakker PAHM (2003) Repeated introduction of genetically modified Pseudomonas putida WCS358r without intensified effects on the indigenous microflora of field-grown wheat. Appl Environ Microbiol 69:3110–3118
Wang CX, Knill E, Glick BR, Defago G (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluorescens strain CHA0 and its gacA derivative CHA96 on their growth-promoting and disease-suppressive capacities. Can J Microbiol 46:898–907
Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of Alp, the aluminium tolerance locus in barley (Hordeum vulgare L.), identifies a candidate gene controlling tolerance. Theor Appl Genet 115:265–276
Weller DM, Howie WJ, Cook RJ (1988) Relationship between in vitro inhibition of Gaeumannomyces graminis var. tritici and suppression of take-all of wheat by fluorescent pseudomonads. Phytopathology 78:1094–1100
Weller DM, Landa BB, Mavrodi OV, Schroeder KL, De La Fuente L, Blouin Bankhead S, Allende Molar R, Bonsall RF, Mavrodi DV, Thomashow LS (2007) Role of 2, 4-diacetylphloroglucinol-producing fluorescent Pseudomonas spp. in the defense of plant roots. Plant Biol 9:4–20
Weller DM, Raaijmakers JM, Gardener BBM, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Ann Rev Phytopathol 40:309–48
Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404
Williams P, Winzer K, Chan WC, Cámara M (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci. 362:1119–1134
Wilson M, Lindow SE (1995) Enhanced epiphytic coexistence of near-isogenic salicylate-catabolizing and non-salicylate-catabolizing Pseudomonas putida strains after exogenous salicylate application. Appl Environ Microbiol 61:1073–1076
Wilson M, Savka MA, Hwang I, Farrand SK, Lindow SE (1995) Altered epiphytic colonization of mannityl opine-producing transgenic tobacco plants by a mannityl opine-catabolizing strain of Pseudomonas syringae. Appl Environ Microbiol 61:2151–2158
Winding A, Binnerup SJ, Pritchard H (2004) Non-target effects of bacterial biological control agents suppressing root pathogenic fungi. FEMS Microbiol Ecol 47:129–141
Yang H, Knapp J, Koirala P, Rajagopal D, Peer WA, Silbart LK, Murphy A, Gaxiola RA (2007) Enhanced phosphorus nutrition in monocots and dicots over-expressing a phosphorus-responsive type IH+-pyrophosphatase. Plant Biotech J 5:735–745
Yokosho K, Yamaji N, Ueno D, Mitani N, Ma JF (2009) OsFRDL1 is a citrate transporter required for efficient translocation of iron in rice. Plant Physiol 149:297–305
Young JC, DeWitt ND, Sussman MR (1998) A transgene encoding a plasma membrane H+-ATPase that confers acid resistance in Arabidopsis thaliana seedlings. Genetics 149:501–507
Zhang LH, Dong YH (2004) Quorum sensing and signal interference: diverse implications. Mol Microbiol 53:1563–1571
Zhang W-H, Ryan PR, Delhaize E, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD (2008) Electrophysiological characterisation of the TaALMT1 protein in transfected tobacco (Nicotiana tabacum L.) cells. Plant J (submitted)
Zhao RM, Dielen V, Kinet JM, Boutry M (2000) Cosuppression of a plasma membrane H+-ATPase isoform impairs sucrose translocation, stomatal opening, plant growth, and male fertility. Plant Cell 12:535–546
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Philippe Lemanceau.
Rights and permissions
About this article
Cite this article
Ryan, P.R., Dessaux, Y., Thomashow, L.S. et al. Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321, 363–383 (2009). https://doi.org/10.1007/s11104-009-0001-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-009-0001-6