Skip to main content
SpringerLink
Log in

Genetic control of root exudation

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

The literature on genetics of root exudation and on genotypic differences in qualitative and quantitative composition of root exudates in crop and native plant species was critically assessed. Differences in exudation have been reported for genotypes that differ in tolerance to nutrient deficiencies, ion toxicities, and pathogen attack. The exudation profile of a limited number of genotypes (frequently only two genotypes with the contrasting response to the environmental stress) have been reported to date. Little is known about the variability in larger samples of the germplasm or about actual genetics behind differential qualitative and quantitative composition of root exudates. Changing the exudation profile of a given genotype may be achieved by manipulating the biosynthetic capacity and by increasing the capacity of the plasma membrane to transport the specific compound out into the rhizosphere. Overexpression of the bacterial citrate synthase gene in the cytoplasm of tobacco plants resulted in exudation of large quantities of citrate into the rhizosphere and partial alleviation of the aluminium (Al) toxicity stress. A similar strategy of transforming plants with citrate synthase gene is being tried as a way of improving plant capacity to extract phosphorus (P) from soils with notoriously low P availability.

More research into the genetic basis of qualitative and quantitative differences in root exudation is warranted. Understanding the genetic control of root exudation, followed by manipulation of qualitative and quantitative composition of root exudates, will result in better adaptation of plants to environmental conditions and a greater yield of crops.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allan DL and Vance 1999 Altered metabolism and gene expression in cluster roots of phosphorus-deficient white lupin. In Abstracts of the 16th International Botanical Congress. Aug. 1-7, 1999. pp. 191. St. Louis, Missouri, USA.

  • Ascencio J 1997 Root secreted acid phosphatase kinetics as a physiological marker for phosphorus deficiency. J. Plant Nutr. 20, 9-26.

    Google Scholar 

  • Asmar F 1997 Variation in activity of root extracellular phytase between genotypes of barley. Plant Soil 195, 61-64.

    Google Scholar 

  • Asmar F, Gahoonia T S and Nielsen N E 1995 Barley genotypes differ in activity of soluble extracellular phosphatase and depletion of organic phosphorus in the rhizosphere soil. Plant Soil 172, 117-122.

    Google Scholar 

  • Azaizeh H A, Marschner H, Römheld V and Wittenmayer L 1995 Effects of a vesicular-arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil-grown maize plants. Mycorrhiza 5, 5321-5327.

    Google Scholar 

  • Barbour W M, Hattermann D R and Stacey G 1991 Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Appl. Environ. Microbiol. 57, 2635-2639.

    Google Scholar 

  • Basu U, Godbold D and Taylor G J 1994 Aluminum resistance in Triticum aestivum associated with enhanced exudation of malate. J. Plant Physiol. 144, 747-753.

    Google Scholar 

  • Basu U, Good A G, Aung T, Slaski J J, Basu A, Briggs K G and Taylor G J 1999 A 23-kDa, root exudate polypeptide co-segregates with aluminum resistance in Triticum aestivum. Physiol. Plant. 106, 53-61.

    Google Scholar 

  • Boeuf-Tremblay V, Plantureux S and Guckert A 1995 Influence of mechanical impedance on root exudation of maize seedlings at two development stages. Plant Soil 172, 279-287.

    Google Scholar 

  • Bolanos-Vasquez M C and Werner D 1997 Effects of Rhizobium tropici, R. etli and R. leguminosarum bv. phaseoli on nod gene-inducing flavonoids in root exudates of Phaseolus vulgaris. Mol.Plant-Microbe Interact. 10, 330-346.

    Google Scholar 

  • Braum S M 1995 Mobilization of phosphorus and other mineral nutrients by citrate in the rhizosphere of Lupinus albus L. Ph.D. thesis, University of Wisconsin, Madison, Wisconsin, USA.

    Google Scholar 

  • Cakmak I, Derici R, Torun B, Tolay I, Braun H I and Schlegel R 1997 Role of rye chromosomes in improvement of zinc efficiency in wheat and triticale. Plant Soil 196, 249-253.

    Google Scholar 

  • Cakmak I, Gülüt K Y, Marschner H and Graham R D 1994 Effect of zinc and iron deficiency on phytosiderophore release in wheat genotypes differing in zinc efficiency. J. Plant Nutr. 17, 1-17.

    Google Scholar 

  • Cakmak I, Öztürk L, Karanlik S, Marschner H and Ekiz H 1996a Zinc-efficient wild grasses enhance release of phytosiderophores under zinc deficiency. J. Plant Nutr. 19, 551-563.

    Google Scholar 

  • Cakmak I, Sari N, Marschner H, Ekiz H, Kalayci M, Yilmaz A and Braun H J 1996b Phytosiderophore release in bread and durum wheat genotypes differing in zinc efficiency. Plant Soil 180, 183-189.

    Google Scholar 

  • Cakmak I, Torun B, Erenoglu B, Öztürk L, Marschner H, Kalayci M, Ekiz H and Yilmaz A 1998 Morphological and physiological differences in the response of cereals to zinc deficiency. Euphytica 100, 340-357.

    Google Scholar 

  • Caradus J R 1995 Genetic control of phosphorus uptake and phosphorus status in plants. In Genetic Manipulation of Crop Plants to Enhance Integrated Nutrient Management in Cropping Systems. 1. Phosphorus. Eds C Johansen, K K Lee, K K Sharma, G V Subbarao and E A Kueneman. pp. 55-74. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, Andhra Pradesh, India.

    Google Scholar 

  • Cianzio S R 1999 Breeding crops for improved nutrient efficiency: soybean and wheat as case studies. In Mineral Nutrition of Crops: Fundamental Mechanisms and Implications. Ed. Z Rengel. pp. 267-287. The Haworth Press, New York, USA.

    Google Scholar 

  • Cieslinski G, van Rees K C J, Szmigielska A M and Huang P M 1997 Low molecular weight organic acids released from roots of durum wheat and flax into sterile nutrient solutions. J. Plant Nutr. 20, 753-764.

    Google Scholar 

  • Cowling R M and Lamont B B 1998 On the nature of Gondwana species flocks: Diversity of Proteaceae in Mediterranean Southwestern Australia and South Africa. Aust. J. Bot. 46, 335-355.

    Google Scholar 

  • Christiansen-Weniger C, Groneman A F and van Veen J A 1992 Associative N2 fixation and root exudation of organic acids from wheat cultivars of different aluminium tolerance. Plant Soil 139, 167-174.

    Google Scholar 

  • Crowley D E and Rengel Z 1999 Biology and chemistry of rhizosphere influencing nutrient availability. In Mineral Nutrition of Crops: Fundamental Mechanisms and Implications. Ed. Z Rengel. pp. 1-40. The Haworth Press, New York, USA

    Google Scholar 

  • de la Fuente J M, Ramirez-Rodriguez V, Cabrera-Ponce J L and Henera-Estrella L 1997 Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276, 1566-1568.

    Google Scholar 

  • Delhaize E 1995 Genetic control and manipulation of root exudates. In Genetic Manipulation of Crop Plants to Enhance Integrated Nutrient Management in Cropping Systems. 1. Phosphorus. EdsC Johansen, K K Lee, K K Sharma, G V Subbarao and B A Kueneman. pp. 145-152. International Crops Research Institute for the Semi-Arid Tropics, Patancheru, Andhra Pradesh, India.

    Google Scholar 

  • Delhaize E, Ryan P R and Randall P J 1993 Aluminum tolerance in wheat (Triticum aestivum L.). II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiol. 103, 695-702.

    Google Scholar 

  • de Pater B S and Schilperoort R A 1992 Structure and expression of a root-specific rice gene. Plant Mol. Biol. 18, 161-164.

    Google Scholar 

  • Dinkelaker B, Hengeler C and Marschner H 1995 Distribution and function of proteoid roots and other root clusters. Bot. Acta 108, 181-200.

    Google Scholar 

  • Dinkelaker B, Hengeler C, Neumann G, Eltrop L and Marschner H 1997 Root exudates and mobilization of nutrients. In Trees-contributions to Modern Tree Physiology. Eds H Rennenberg, W Eschrich and H Ziegler. pp. 441-452. Backhuys Publishers, Leiden, The Netherlands.

    Google Scholar 

  • Erenoglu B, Cakmak I, Marschner H, Römheld V, Eker S, Daghan H, Kalayci M and Ekiz H 1996 Phytosiderophore release does not relate well with Zn efficiency in different bread wheat genotypes. J. Plant Nutr. 19, 1569-1580.

    Google Scholar 

  • Fan T W-M, Lane A N, Pedler J, Crowley D and Higashi R M 1997 Comprehensive analysis of organic ligands in whole root exudates using nuclear magnetic resonance and gas chromatograph-mass spectrometry. Anal. Biochem. 251, 57-68.

    Google Scholar 

  • Gagnon H and Ibrahim R K 1998 Aldonic acids: a novel family of nod gene inducers of Mesorhizobium loti, Rhizobium lupini, and Sinorhizobium meliloti. Mol. Plant-Microbe Interact. 11, 988-998.

    Google Scholar 

  • Gardner W K, Barber D A and Parberry K G 1983 The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70, 107-124.

    Google Scholar 

  • Graham R D and Rengel Z 1993 Genotypic variation in zinc uptake and utilization. In Zinc in Soils and Plants. Ed. A D Robson. pp. 107-118. Kluwer Academic Publishers, Dordrecht, The Netherlands.

    Google Scholar 

  • Graham R D, Ascher J S, Ellis P A E and Shepherd K W 1987 Transfer to wheat of the copper efficiency factor carried on rye chromosome arm 5RL. Plant Soil 99, 107-114.

    Google Scholar 

  • Graham R D, Ascher J S and Hynes S C 1992 Selecting zinc-efficient cereal genotypes for soils and low zinc status. Plant Soil 146, 241-250.

    Google Scholar 

  • Grierson P F 1992 Organic acids in the rhizosphere of Banksia integrifolia L. Plant Soil 144, 259-265.

    Google Scholar 

  • Guyon P, Petit A, Tempe J and Dessaux Y 1993 Transformed plants producing opines specifically promote growth of opine-degrading agrobacteria. Mol. Plant-Microbe Interact. 6, 92-98.

    Google Scholar 

  • Hansen N C and Jolley V D 1995 Phytosiderophore release as a criterion for genotypic evaluation of iron efficiency in oat. J. Plant Nutr. 18, 455-465.

    Google Scholar 

  • Hansen N C, Jolley V D, Berg W A, Hodges M E and Krenzer E G 1996 Phytosiderophore release related to susceptibility of wheat to iron deficiency. Crop Sci. 36, 1473-1476.

    Google Scholar 

  • Hansen N C, Jolley V D and Brown J C 1995 Clipping foliage differentially affects phytosiderophore release by two wheat cultivars. Agron. J. 87, 1060-1063.

    Google Scholar 

  • Helal H M 1990 Varietal differences in root phosphatase activity as related to utilisation of organic phosphates. Plant Soil 123, 161-163.

    Google Scholar 

  • Hernandez G, Ramirez M, Suarez R and Fuentes S I 1995 Root exuded nod-gene inducing signals limit the nodulation capacity of different alfalfa varieties with Rhizobium meliloti. Plant Cell Reports 14, 626-629.

    Google Scholar 

  • Higuchi K, Nishizawa N K, Römheld V, Marschner H and Mori S 1996 Absence of nicotianamine synthase activity in the tomato mutant 'chloronerva'. J. Plant Nutr. 19, 1235-1239.

    Google Scholar 

  • Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa N-K and Mori S 1999 Cloning of nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol. 119, 471-479.

    Google Scholar 

  • Hoffland E, van den Boogaurd R, Nelemans J and Findenegg G 1992 Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol. 122, 675-680.

    Google Scholar 

  • Hopkins B G, Whitney D A, Lamond R E and Jolley V D 1998 Phytosiderophore release by sorghum, wheat, and corn under zinc deficiency. J. Plant Nutr. 21, 2623-2637.

    Google Scholar 

  • Hungria M and Phillips D A 1993 Effects of a seed color mutation on rhizobial nod-gene-inducing flavonoids and nodulation in common bean. Mol. Plant-Microbe Interact. 6, 418-422.

    Google Scholar 

  • Ikeda K, Toyota K and Kimura M 1997 Effects of soil compaction on the microbial populations of melon and maize rhizoplane. Plant Soil 189, 91-96.

    Google Scholar 

  • Jach G, Gornhardt B, Mundy J, Logemann J, Pinsdorf E, Leah R, Schell J and Maas C 1995 Enhanced quantitative resistance against fungal disease by combinatorial expression of different barley antifungal proteins in transgenic tobacco. Plant J. 8, 97-109.

    Google Scholar 

  • Janczarek M, Urbanik-Sypniewska T and Skorupska A 1997 Effect of authentic flavonoids and the exudate of clover roots on growth rate and inducing ability of nod genes of Rhizobium leguminosarum bv. trifolii. Microbiol. Res. 152, 93-98.

    Google Scholar 

  • Jolley V D and Brown J C 1989 Iron inefficient and efficient oat cultivars. II. Characterization of phytosiderophore released in response to iron deficiency stress. J. Plant Nutr. 12, 923-937.

    Google Scholar 

  • Jolley V D, Cook K A, Hansen N C and Stevens W B 1996 Plant physiological responses for genotypic evaluation of iron efficiency in strategy I and strategy II plants. A review. J Plant Nutr. 19, 1241-1255.

    Google Scholar 

  • Johnson J F, Allan D L and Vance C P 1994 Phosphorus stress-induced proteoid roots show altered metabolism in Lupinus albus. Plant Physiol. 104, 657-665.

    Google Scholar 

  • Johnson J F, Vance C P and Allan D L 1996a Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol. 112, 31-41.

    Google Scholar 

  • Johnson J F, Allan D L, Vance C P and Weiblen G 1996b Root carbon dioxide fixation by phosphorus-deficient Lupinus albus. Contribution to organic acid exudation by proteoid roots. Plant Physiol. 112, 19-30.

    Google Scholar 

  • Jones D L 1998 Organic acids in the rhizosphere-a critical review. Plant Soil 205, 25-44.

    Google Scholar 

  • Jorge R A and Arruda P 1997 Aluminum-induced organic acids exudation by roots of an aluminum-tolerant tropical maize. Phytochemistry 45, 675-681.

    Google Scholar 

  • Keerthisinghe G, Hocking P J, Ryan P R and Delhaize E 1998 Effect of phosphorus supply on the formation and function of proteoid roots of white lupin (Lupinus albus L.). Plant Cell Environ. 21, 467-478.

    Google Scholar 

  • Lamont B 1982 Mechanisms for enhancing nutrient uptake in plants, with particular reference to mediterranean South Africa and Western Australia. Bot. Rev. 48, 597-689.

    Google Scholar 

  • Larsen P B, Degenhardt J, Tai C-Y, Stenzler L M, Howell S H and Kochian L V 1998 Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiol. 117, 9-18.

    Google Scholar 

  • Li M, Osaki M, Rao I M and Tadano T 1997 Secretion of phytase from the roots of several plant species under phosphorus-deficient conditions. Plant Soil 195, 161-169.

    Google Scholar 

  • Liljeroth E, Kuikman P and van Veen J A 1994 Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic matter at different soil nitrogen levels. Plant Soil 161, 233-240.

    Google Scholar 

  • Lynch J 1998 The role of nutrient-efficient crops in modern agriculture. In Nutrient Use in Crop Production, Ed. Z Rengel. pp. 241-264. The Haworth Press, New York, USA.

    Google Scholar 

  • Ma J F, Zheng S J and Matsumoto H 1997 Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol. 38, 1019-1025.

    Google Scholar 

  • Ma Z and Miyasaka S C 1998 Oxalate exudation by taro in response to Al. Plant Physiol. 118, 861-865.

    Google Scholar 

  • Mandal N C and Sinha A K 1991 Differential effects of root exudates and extracts from tomato cultivars on Fusarium oxysporum f.sp. lycopersici in relation to their disease reaction. J. Mycopathol. Res. 29, 9-16.

    Google Scholar 

  • Marschner H and Römheld V 1994 Strategies of plants for acquisition of iron. Plant Soil 165, 261-274.

    Google Scholar 

  • Maxwell C A, Hartwig U A, Joseph C M and Phillips D A 1989 A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol. 91, 842-847.

    Google Scholar 

  • McKhann H I, Paiva N L, Dixon R A and Hirsch A M 1997 Chalcone synthase transcripts are detected in alfalfa root hairs following inoculation with wild-type Rhizobium meliloti. Mol. Plant-Microbe Interact. 10, 50-58.

    Google Scholar 

  • Meharg A A and Killham K 1995 Loss of exudates from the roots of perennial ryegrass inoculated with a range of micro-organisms. Plant Soil 170, 345-349.

    Google Scholar 

  • Mehta S, Sharma S and Sindhan G S 1992 Analysis of root exudates of cowpea and their influence on the growth of Rhizoctonia solani. Indian J. Mycol. Plant Pathol. 22, 227-231.

    Google Scholar 

  • Milner J L, Raffel S J, Letbbridge B J and Handelsman J 1995 Culture conditions that influence accumulation of zwittermicin A by Bacillus cereus UW85. Appl. Microbiol. Biotechnol. 43, 685-691.

    Google Scholar 

  • Miyasaka S C, Buta J G, Howell R K and Foy C D 1991 Mechanism of aluminum tolerance in snapbeans. Root exudation of citric acid. Plant Physiol. 96, 737-743.

    Google Scholar 

  • Mori S 1994 Mechanisms of iron acquisition by graminaceous (strategy II) plants. In Biochemistry of Metal Micronutrients in the Rhizosphere. Eds. J A Manthey, D E Crowley and D G Luster. pp. 225-249. Lewis Publishers, Boca Raton, Florida, USA.

    Google Scholar 

  • Mori S 1997 Reevaluation of the genes induced by iron deficiency in barley roots. Soil Sci. Plant Nutr. 43, 975-980.

    Google Scholar 

  • Mori S, Nishizawa N K and Fujigaki J 1990 Identification of rye chromosome 5R as a carrier of the genes for mugineic acid synthetase and 3-hydroxymugineic acid synthetase using wheat-rye addition lines. Jpn. J. Genet. 65, 343-352.

    Google Scholar 

  • Neumann G, Massonneau A, Martinoia E and Römheld V 1999 Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208, 373-382.

    Google Scholar 

  • Ni J J, Wu P, Lou A C, Zhang Y S and Tao Q N 1996 Low phosphorus effects on the metabolism of rice seedlings. Commun. Soil Sci. Plant Anal. 27, 3073-3084.

    Google Scholar 

  • O'Connell K P, Goodman R M and Handelsman J 1996 Engineering the rhizosphere: expressing a bias. Trends Biotechnol. 14, 83-88.

    Google Scholar 

  • Ozawa K, Osaki M, Matsui H, Honma M and Tadano T 1995 Purification and properties of acid phosphatase secreted from lupin roots under phosphorus-deficiency conditions. Soil Sci. Plant Nutr. 41, 461-469.

    Google Scholar 

  • Parashar R D, Hooda I and Sindhan G S 1992 Penetration and infection of different chickpea cultivars by Rhizoctonia solani. Plant Dis. Res. 7, 60-63.

    Google Scholar 

  • Pellet D M, Grunes D L and Kochian L V 1995 Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196, 788-795.

    Google Scholar 

  • Pellet D M, Papernik L A and Kochian L V 1996 Multiple aluminum-resistance mechanisms in wheat. Roles of root apical phosphate and malate exudation. Plant Physiol. 112, 591-597.

    Google Scholar 

  • Rengel Z 1992 Role of calcium in aluminium toxicity. New Phytol. 121, 499-513.

    Google Scholar 

  • Rengel Z 1997 Root exudation and microflora populations in rhizosphere of crop genotypes differing in tolerance to micronutrient deficiency. Plant Soil 196, 255-260.

    Google Scholar 

  • Rengel Z 1999 Physiological mechanisms underlying differential nutrient efficiency of crop genotypes. In Mineral Nutrition of Crops: Mechanisms and Implications. Ed. Z Rengel. pp. 227-265. The Haworth Press, New York, USA.

    Google Scholar 

  • Rengel Z, Römheld V and Marschner H 1998 Uptake of zinc and iron by wheat genotypes differing in zinc efficiency. J. Plant Physiol. 152, 433-438.

    Google Scholar 

  • Römheld V 1991 The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: an ecological approach. Plant Soil 130, 127-134.

    Google Scholar 

  • Römheld V and Marschner H 1990 Genotypical differences among graminaceous species in release of phytosiderophores and uptake of iron phytosiderophores. Plant Soil 123, 147-153.

    Google Scholar 

  • Rosenblueth M, Hynes M F and Martinez-Romero E 1998 Rhizobium tropici teu genes involved in specific uptake of Phaseolus vulgaris bean-exudate compounds. Mol. Gen. Genet. 258, 587-598.

    Google Scholar 

  • Rossbach S, Kulpa D A, Rossbach U and de Bruijn F J 1994 Molecular and genetic characterization of the rhizopine catabolism (mocABRC) genes of Rhizobium meliloti L5-30. Mol. Gen. Genet. 245, 11-24.

    Google Scholar 

  • Ryan P R, Delhaize E and Randall P J 1995a Characterization of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103-110.

    Google Scholar 

  • Ryan P R, Delhaize E and Randall P J 1995b Malate efflux from root apices and tolerance to aluminium are highly correlated in wheat. Aust. J. Plant Physiol. 22, 531-536.

    Google Scholar 

  • Ryan P R, Skerrett M, Findlay G P, Delhaize E and Tyerman S D 1997 Aluminum activates an anion channel in the apical cells of wheat roots. Proc. Natl. Acad. Sci. USA 94, 6547-6552.

    Google Scholar 

  • Schlegel R, Cakmak I, Torun B, Eker S and Köleli N 1997 The effect of rye genetic information on zinc, copper, manganese and iron concentation of wheat shoots in zinc-deficient soil. Cereal Res. Commun. 25, 177-184.

    Google Scholar 

  • Schlegel R, Kynast R, Schwarzacher T, Römheld V and Walter A 1993 Mapping genes for copper efficiency in rye and the relationship between copper and iron efficiency. Plant Soil 154, 61-65.

    Google Scholar 

  • Schmidt P E, Broughton W J and Werner D 1994 Nod factors of Bradyrhizobium japonicum and Rhizobium sp. NGR234 induce flavonoid accumulation in soybean root exudate. Mol. Plant-Microbe Interact. 7, 384-390.

    Google Scholar 

  • Shaul O and Galili G 1992 Threonine overproduction in transgenic tobacco plants expressing a mutant desensitized aspartate kinase of Escherichia coli. Plant Physiol. 100, 1157-1163.

    Google Scholar 

  • Shinde N V and Deshmukh R B 1989 Effect of chickpea root exudates on Fusarium oxysporum f.sp. ciceri. Indian J. Pulses Res. 2, 90-92.

    Google Scholar 

  • Skene K R 1998 Cluster roots: some ecological considerations. J. Ecol. 86, 1060-1064.

    Google Scholar 

  • Soejima H, Sugiyama T and Ishihara K 1992 Changes in cytokinin activities and mass spectrometric analysis of cytokinins in root exudates of rice plants (Oryza sativa L.). Comparison between cultivars Nipponbare and Akenohoshi. Plant Physiol. 100, 1724-1729.

    Google Scholar 

  • Stevenson P C, Padgham D E and Haware M P 1995 Root exudates associated with the resistance of four chickpea cultivars (Cicer arietinum) to two races of Fusarium oxysporum f.sp. ciceris. Plant Pathol. 44, 686-694.

    Google Scholar 

  • Ström L 1997 Root exudation of organic acids: importance to nutrient availability and the calcifuge and calcicole behaviour of plants. Oikos 80, 459-466.

    Google Scholar 

  • Ström L, Olsson T and Tyler G 1994 Differences between calcifuge and acidifuge plants in root exudation of low-molecular organic acids. Plant Soil 167, 239-245.

    Google Scholar 

  • Subbarao G V, Ae N and Otani T 1997 Genotypic variation in iron and aluminum-phosphate solubilizing activity of pigeonpea root exudates under P deficient conditions. Soil Sci. Plant Nutr. 43, 295-305.

    Google Scholar 

  • Tadano T, Ozawa K, Sakai H, Osaki M and Matsui H 1993 Secretion of acid phosphatase by the roots of crop plants under phosphorus-deficient conditions and some properties of the enzyme secreted by lupin roots. Plant Soil 155/156, 95-98.

    Google Scholar 

  • Timonin M I 1946 Microflora of the rhizosphere in relation to the manganese-deficiency disease of oats. Soil Sci. Soc. Amer. Proc. 11, 284-292.

    Google Scholar 

  • Tyler G and Ström L 1995 Differing organic acid exudation pattern explains calcifuge and acidifuge behaviour of plants. Ann. Bot. 75, 75-78.

    Google Scholar 

  • Uren N C and Reisenauer H M 1988 The role of root exudates in nutrient acquisition. Adv. Plant Nutr. 3, 79-114.

    Google Scholar 

  • von Wiren N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh R A and Hider R C 1999 Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiol. 119, 1107-1114.

    Google Scholar 

  • von Wiren N, Marschner H and Römheld V 1995 Uptake kinetics of iron-phytosiderophores in two maize genotypes differing in iron efficiency. Physiol. Plant. 93, 611-616.

    Google Scholar 

  • von Wiren N, Mori S, Marschner H and Römheld V 1994 Iron inefficiency in maize mutant ys1 (Zea mays L cv. yellow-stripe) is caused by a defect in uptake of iron phytosiderophores. Plant Physiol. 106, 71-77.

    Google Scholar 

  • Walter A, Römheld V, Marschner H and Mori S 1994 Is the release of phytosiderophores in zinc-deficient wheat plants a response to impaired iron utilization? Physiol. Plant. 92, 493-500.

    Google Scholar 

  • Wasaki J, Michiko A, Ozawa K, Omura M, Osaki M, Ito H, Natsui H and Tadano T 1997 Properties of secretory acid phosphatase from lupin roots under phosphorus-deficient conditions. Soil Sci. Plant Nutr. 43, 981-986.

    Google Scholar 

  • Waschutza S, Hofmann N, Niemann E G and Fendrik I 1992 Investigations on root exudates of Korean rice. Symbiosis 13, 181-189.

    Google Scholar 

  • Welch R M 1995 Micronutrient nutrition of plants. CRC Crit. Rev. Plant Sci. 14, 49-82.

    Google Scholar 

  • Wojtaszek P, Stobiecki M and Gulewicz K 1993 Role of nitrogen and plant growth regulators in the exudation and accumulation of isoflavonoids by roots of intact white lupin (Lupinus albus L.) plants. J. Plant Physiol. 142, 689-694.

    Google Scholar 

  • Zhang F, Römheld V and Marschner H 1989 Effect of zinc deficiency in wheat on the release of zinc and iron mobilizing root exudates. Z. Pflanzenernähr. Bodenk. 152, 205-210.

    Google Scholar 

  • Zhang F S, Ma J and Cao Y P 1997 Phosphorus deficiency enhances root exudation of low-molecular weight organic acids and utilization of sparingly soluble inorganic phosphates by radish (Raphanus sativus L.) and rape (Brassica napus L.) plants. Plant Soil 196, 261-264.

    Google Scholar 

  • Zheng S J, Ma J F and Matsumoto H 1998a Continuous secretion of organic acids is related to aluminium resistance during relatively long-term exposure to aluminium stress. Physiol. Plant. 103, 209-214.

    Google Scholar 

  • Zheng S J, Ma J F and Matsumoto H 1998b High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol. 117, 745-751.

    Google Scholar 

  • Zuanazzi J A S, Clergeot P H, Quirion J C, Husson H P, Kondorosi A and Ratet P 1998 Production of Sinorhizobium meliloti nod gene activator and repressor flavonoids from Medicago sativa roots. Mol. Plant-Microbe Interact. 11, 784-794.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Soil Science and Plant Nutrition, Faculty of Agriculture, The University of Western Australia, Nedlands, WA 6907, Australia

    Z. Rengel

Authors
  1. Z. Rengel
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rengel, Z. Genetic control of root exudation. Plant and Soil 245, 59–70 (2002). https://doi.org/10.1023/A:1020646011229

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020646011229

Search

Navigation