اثر اسیدهای آلی ریشه در قابلیت جذب عناصر غذایی در ریزوسفر

نوع مقاله : مقاله پژوهشی

نویسندگان

1 استادیار پژوهش مؤسسه تحقیقات خاک و آب

2 استاد دانشگاه تربیت مدرس

3 استاد خاکشناسی و محیط زیست دانشگاه ولز انگلستان

چکیده

بسیاری از خاکهای ایران در مناطق کشاورزی دارای طبیعت و خصوصیت آهکی و واکنش قلیایی هستند. در بسیاری از مناطق کشور کربنات کلسیم تقریباً 40 درصد از وزن خاکها را تشکیل می‌دهد. pH خاکهای آهکی عمدتاً توسط مقادیر کربنات کلسیم موجود در پروفیل خاک کنترل شده و اغلب بین 5/8-5/7 در نوسان می‌باشد. واکنش کربنات کلسیم در خاکهای آهکی منجر به افزایش pH خاک می شود خصوصاً در مناطقی که میزان بارندگی کم می‌باشد. این واکنشها در افق سطحی خاکهای آهکی حلالیت و جذب بسیاری از عناصر را مانند P، Zn، Mn، Cu و Fe محدوده نموده بعلاوه در رشد گیاه و ریشه هم اختلال ایجاد می کند و در نهایت باعث کاهش عملکرد می‌گردد مگر اینکه مقادیر زیادی کودهای شیمیایی مصرف شود. بنابراین حلالیت و قابلیت جذب اندک عناصر غذایی در خاکهای آهکی توجه بسیاری از دانشمندان علم تغذیه را با توجه به هزینه‌ بالای کودهای شیمیایی، محیط زیست و سلامت جامعه به خود معطوف نموده است. مطالعات بسیاری نشان داده است که در خاکهای آهکی اسیدهای آلی حاصل از ترشحات ریشه گیاه می توانند به عنوان عامل موثر بر استخراج بخش قابل توجهی از عناصر غذایی مورد نیاز گیاه عمل نمایند و راندمان مصرف کود و آب را در این خاکها بهبود ببخشند. هدف اصلی از تهیه این مقاله معرفی اسیدهای آلی و جلب دیدگاههای جامعه علمی کشور به ویژه متخصصین علم تغذیه گیاه و حاصلخیزی خاک به نقش اسیدهای آلی مانند سیترات و اگزالات (که از ترکیبات آلی با وزن مولکولی کم می‌باشند و از ریشه گیاه در ریزوسفر ترشح می‌شوند) در افزایش حلالیت و قابل جذب نمودن عناصر غذایی کم محلول مانند فسفر، آهن، روی و انجام فعالیتهای پژوهشی متخصصین تغذیه گیاهی در این زمینه می‌باشد. در این مقاله تحقیقات انجام گرفته در گذشته و حال در مورد رفتار اسیدهای آلی در گیاه و خاک به صورت خلاصه مورد بررسی قرار گرفته است تا اهمیت و نقش آنها در ریزوسفر ارزیابی شود. ریزوسفر منطقه‌ای از خاک است که بلافاصله ریشه گیاه را احاطه کرده و در اثر فعالیت‌های ریشه و ویژگیهای اکولوژیکی آن تغییر می‌یابد. در این منطقه حساس گیاهان‌ به محیطشان واکنش نشان می‌دهند. در شرایطی که گیاه دارای رشد و نمو معمول می‌باشد، مقدار فراوانی از مواد معدنی و آلی بین ریشه و خاک مبادله می‌گردد که به طور اجتناب‌ناپذیری منجر به تغییراتی در خصوصیات فیزیکی و شیمیایی ریزوسفر می‌شود. گیاهان همچنین در واکنش به محیط و تنش‌های مشخص محیطی قادر هستند در ریزوسفرتغییراتی ایجاد نمایند. اسیدهای آلی معمولاً از این منطقه بدست می‌آیند و ترشح آنها از ریشه‌های گیاه به کمبود عناصر غذایی و تنش‌‌های محیطی ارتباط پیدا می‌کند. اسیدهای آلی مانند سیترات (citrate)، اگزالات (oxalate) و مالات (malate) در بسیاری از فرآیندهای ریشه شرکت می‌کنند که این فرآیندها شامل استخراج عناصر غذایی، سمیت‌زدایی فلزی، هوازدگی مینرالی و جذب پاتوژن‌ها می‌باشد. البته تا زمانی که مکانیسم رهاسازی اسیدهای آلی و سرنوشت این ترکیبات در خاک کاملاً درک نشود، ارزیابی کامل نقش اسیدهای آلی در فرآیندهای یاد شده مقدور نخواهد بود. بنابراین بررسی حاضر شامل اطلاعاتی در زمینه غلظت و تجمع اسیدهای آلی در گیاهان، واکنش خاک، جذب (sorption) و تجزیه میکروبی (biodegradation) می‌باشد. بطور خلاصه، رهاسازی اسیدهای آلی از ریشه‌ها در پاسخ به تعدادی از تنش‌های محیطی مانند کمبود فسفر و کمبود آهن مشخص شده است که البته نوع گونه گیاهی در این واکنش‌ها نقش مهمتری دارند. از طرفی در این بررسی جذب (sorption) اسیدهای آلی توسط مینرالهای خاک و نیز تجزیه میکروبی آنها نقش بسیار اساسی در کارآیی اسیدهای آلی در فرآیندهای ریزوسفر دارند.

کلیدواژه‌ها

عنوان مقاله [English]

Rhizosphere Organic Acids and Nutrient Availability

نویسندگان [English]

  • Z. Khademi 1
  • M. J. Malakouti 2
  • D. L. Jones 3
1 Assistant Professor, Soil and Water Research Institute
2 Professor, Tarbiat Modarres University
3 Professor, Wales University, UK
چکیده [English]

The principle objective of this review article is to present to plant nutrition specialists some interesting aspects of the role of organic acids in improving the availability of nutrient elements in calcareous soils in order to promote more research in this area. The rhizosphere is the zone of soil immediately surrounding plant roots that is modified by root activity. In this critical zone, plants respond to their environment. As a consequence of normal growth and development, a large range of organic and inorganic substances are exchanged between the root and soil, which inevitably leads to changes in the biochemical and physical properties of the rhizosphere. Plants also modify their rhizosphere in response to certain environmental signals and stresses. Organic anions are commonly detected in this region, and their exudation form plant roots have now been associated with nutrient deficiencies and inorganic ion stresses. Organic acids such as citrate, oxalate and malate are active in many of the roots natural processes including nutrient absorption, reducing metal toxicity, mineral weathering and pathogens attraction. A full assessment of their role in these processes, however, cannot be determined unless the exact mechanisms of plant organic acid release and fate of these compounds in the soil are more fully understood. This review therefore, includes information on organic acid levels in plants, soil reactions (soil solution concentration, sorption) and microbial considerations (mineralization). In summary, the release of organic acids from roots can operate by multiple mechanisms in response to a number of well-defined environmental stresses (e.g., P and Fe stress). These responses, however, are high stress and plant-species specific. In addition, this review indicates that the sorption of organic acids to the mineral phase and mineralization by the soils microbial biomass are critical to determining the effectiveness of organic acids in most rhizophere processes.

کلیدواژه‌ها [English]

  • Organic acids
  • Rhizosphrer
  • Root exudates
  • Nutrient elements

مراجع

  1. Banik, S., Dey, B. K., (1983). Alluvial soil microorganisms capable of utilizing in soluble aluminum phosphate as a sole source of phosphorus. Zentralbatt fur Mikrobiologie 138, 437-442.
  2. Baziramakenga, R. Simard, R. R., and Leroux, G. D. (1995). Determination of organic acids in soil extraets by ion chromatography. Soil Biol. Biochen. 27:349-356.
  3. Bolan, N. S., Naidu, R., Mahimairaja, S., Baskaran, S., (1994). Influence of low- molecular wieght organic- acids on the solubilization of phosphates. Biology and Fertility of Soils 18, 311-319.
  4. Bolan, N. S., R. Naidu, S. Mahimairaja, and S. Baskaran. (1994). Influence of
    low-molecular-weight organic-acids on the solubilization of phosphates. Biol. Fert. Soils 18: 311-319.
  5. Bowers, J. H., Nameth, S. T., Riedel, R. M. and Rowe, R. C. (1996). Infection and colonization of potato roots by Vericillium dahliae as affected by Pratylenchus penetrans and crenatus. Phytopathol. 86: 614 - 621.
  6. Braum S. M., Helmke, P. A. (1995). White lupin utilizes soil phosphorus that is unavailable to soybean. Plant and Soil, 176:95-100.
  7. Cakmak, and H. Marschner. (1988). Increase in membrane-permeability and exudation in roots of zinc deficient plants. J. Plant Physiol., 132: 356-361.
  8. Chairidchai, P., Ritchie, G. S. P., (1993). Zinc adsorption by sterilized and non sterilized soil in the presence of citrate and catechol. Communications in Soil Science and Plant Analysis 24, 261-275.
  9. Chang, K. J., and Roberts, J. K. M. (1991). Cytoplasmic malate levels in maize
    root-tips during K+ ion uptake determined by 13C-NMR spectroscopy. Biochim. Biophys. Acta. 1092: 29-34.
  10. Chang, K. J., and Roberts, J. K. M., (1989). Observation of cytoplasmic of cytoplasmic and vacuolar malate in maize root-tips by 13C-NMR spectroscopy. Plant Physiol. 89: 97-203.
  11. Cline, G. R., P. E. Powell, P. J. Szaniszlo, C. P. P. Reid. (1982). Comparison of the abilities of hydroxamic, synthetic, and other natural organic acids to chelate iron and other ions in nutrient solution. Soil Sci. Soc. Am. J., 46: 1158-1164.
  12. Darrah, P. R., (1991a). Measuring the diffusion- coefficient of rhizosphere exudates in 2. The diffusion of compounds. J. Soil Sei. 42:421-434.
  13. Darrah, P. R., (1994b). Measuring the diffusion- coefficient of rhizosphere exudates in soil1. The diffusion of non-sorbing compounds. J. Soil Sei. 42: 413-420.
  14. Delhaize, E. P. R. Ryan, P. J. Randall. (1993). Aluminum tolerance in wheat (Triticum aestivum ) 2. Aluminum stimulated excretion of malic acid from root apices. Plant Physiol., 103: 695-702.
  15. Devos, C.R., Lubberding H. J., and Bienfait, H. F., (1986). Rhizosphere acid-infcation as a response to iron-deficiency in bean plants. Plant Physiol. 81:842-846.
  16. Dinkelaker, B. Hengeler, C. and Marschner, H. (1989). Citrit-acid excretion and precipitation of calcium citrate in the rhizosphere of whitc lupin
    (Lupums albus ) Plant Cell Environ. 12:285-292.
  17. Dinkelaker, B., Hengele, C., Marschner, H., (1995). Distribution and function of proteoid roots and other root cluster. Bot Acta 108, 183-200.
  18. Dinkelaker, B., Marschner, H., (1992). In vivo demonstration of acid phosphatase activity in the rhizosohere of soil- grown plants. Plant and Soil 144, 199-205.
  19. Dutton M. V., and Evans C. S. (1996). Oxalate production by fungi-its role in pathogenicity and ecology in the soil enviroment. J. Microbiol. 42: 881-895.
  20. Elkhatib, E. A., (1990). Simultaneous determination of low molecular-weight organic-acids in soil solution by ion chromatography. Z. Plfanzenernahr. Bodenk. 153:201-205.
  21. Evans, A., (1991). Influence of low- molecular- weight organic- acids on zinc distribution within micronutrient pools and zinc uptake by wheat. Journal of Plant Nutrition 14, 1307-1318.
  22. Fan, T. W. M., N. Lane, J. Pedler, D. Crowley, and R. M. Higashi. (1997). Comprehensive analysis of organic ligands in whole root exudates using nuclear magnetic resonance and gas chromatography mass spectrometry. Anal. Biochem., 251: 57-68.
  23. Fohse, D., Jungk, A., (1983). Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant and soil 74, 359-368.
  24. Fox, T. C., J. E. Shaff, M. A. Grusak,, W.A. Norvell, Y. Chen, R. L. Chaney. (1996). Direct measurement of Fe59-labeled Fe2+ influx in roots of pea using a chelator buffer system to control free Fe2+ in solution. Plant Physiol. 111: 93-100.
  25. Gardner K., Parbery D. G., Barber D. A. (1981). Proteoid root morphology and function in Lupinus albus. Plant and Soil, 60:143-47.
  26. Gerke, J., (1994). Kinetics of soil phosphate desorption as affected by citric acid. Zeitschrift fur Pflanzenernahrung and Bodenkunde 157, 17-22.
  27. Greke, J. (1992). Phosphate, aluminum and iron in the soil solution of three different soils in relation to varying concentrations of citric acid. Z. Phanzenernahr. Bodenk. 155: 339-343.
  28. Greke, J. (1994). Kinetcs of soil phosphate desorption as affected by citric acid Z. Pflanzenernahr. Bodenk. 157:17-22.
  29. Grierson, P. F. (1992). Organic-acid in the rhizosphere of Banksiaintegrifolia Plant Soil. 144:256-265.
  30. Guerinot, M. L., and Yi, Y. (1994). Iron: nutritious, noxions, and not readily available. Plant Physiol. 104-815-820.
  31. Hoffland, E. Van Den Boogaard, R., Nelemans J. Findenegg, G. (1992). Biosynthesis and root exudation of citric and malic acids in phosphate-starved rape plants. New Phytol. 122:675-680.
  32. Hoffland, E., (1992). Quantitatove evaluation of the role of organic-acid exudation in the mobilization of rock phosphate by rape. Plant and Soil, 140: 279-289.
  33. Hoffland, E., Findenegg, G. R., Nelemans, J. A., (1989). Solubilization of rock phosphate by rape. II. Local root exudation of organic acid as a response to P starvation. Plant and Soil 113, 161-165.
  34. Hoffland, E., Findenegg. G. R., and Nelemans J. A. (1989). Solubilization of rock phosphate by rape. 2. Local root exudation of organic acid as a response to P starvation. Plant and Soil, 113: 161-165.
  35. Hoffland, E., Vanden Boogaard, R., Nelemans, J., Findenegg, G., (1992). Biosynthesis and root exduation of citric and malic acids in phosphate- starved rape plants. New Phytologist 122, 675-680.
  36. Hue, N. V., Craddock, G. R., Adams, F. (1986). Effect of organic acids on aluminum toxicity in subsoils. Soil Sci. Am. J. 50:28-34.
  37. Imas, P., B. BarYosef, U. Kafkafi, and R. Ganmore-Neumann. (1997a). Phosphate induced carboxylate and proton release by tomato roots. Plant and Soil, 191: 35-39.
  38. Imas, P., B. BarYosef, U., and Ganmore-Neumann. (1997b). Release of carboxylic anions and protons by tomato roots in response to ammonium nitrate ratio and pH in nutrient solution. Plant and Soil, 191: 27-34.
  39. Johnson J. F., Vance C. P., Allen, D. L. (1996). Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol. 112:31-41.
  40. Johnson, D. L. and Brassington D. S. (1998). Sorption of organic acids in acid soils and its implications in the rhizosphere. Eur. J. Soil Sci. 49:447-455.
  41. Johnson, J. F., D. L. Allan, C. P. Vance, and G. Weiblen. (1996a). Root carbon dioxide fixation by phosphorus-deficient Lupinus albus: Contribution to organic-acid exudation by proteoid roots. Plant Physiol., 112: 19-30.
  42. Jones, D. L. and P. R. Darrah. (1996). Re-sorption of organic-compounds by roots of Zea mays and its consequences in the rhizosphere. 3. Characteristics of sugar influx and efflux. Plant and Soil, 178: 153-160.
  43. Jones, D. L., and Darrah P. R. (1994a). Amino-acid influx at the soil-root interface of Zea mays and its implications in the rhizosphere. Plant and Soil, 163: 1-12.
  44. Jones, D. L., and Darrah. P. R. (1995). Influx and efflux of organic-acids across the soil-root interface of Zea mays and its implications in rhizosphere C flow. Plant and Soil, 173: 103-109.
  45. Jones, D. L., and Darrah. P. R. (1995). Influx and efflux of organic-acids across the soil-root interface of Zea mays and its implications in rhizosphere C flow. Plant Soil. 173: 103-109.
  46. Jones, D. L., Brassington DS. (1998). Sorption of organic acids in acid soils and its implications in the rhizosphere. Eur. J. Soil Sci. 49:447-55.
  47. Jones, D. L., Darrah, P. R. (1994). Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant and Soil, 166:247-57.
  48. Jones, D. L., Darrah, P. R., (1994a). Amino acid influx at the soil- root interface of Zea mays L. and its implicatons in the rhizosphere. Plant and Soil 163, 1-12.
  49. Jones, D. L., Darrah, P. R., (1994b). Role of root derived organic- acids in the mobilization of nutrients from the rhizosphere. Plant and Soil 166, 247-257.
  50. Jones, D. L., Edwards, A. C., (1993). Effect of moisture content and preparation technique on the composition of soil slution obtained by centrifugation. Communications in Soil Science and Plant Analysis 24, 171-186.
  51. Jones, D. L., Edwards, A. C., (1998). Influence of sorption on the bioligical utilization of two simple carbon substrates. Soil Biology and Biochemistry 30,
    1895-1902.
  52. Jones, D. L., Edwards, A. C., Donachie, K., Darrah, P. R., (1994). Role of proteinaceous amion acids released in root exudates in nutrient acquisition from the rhizosphere. Plant and Soil 158, 183-192.
  53. Jones, D. L., P. R. Darrah, and L. V. Kochian. (1996a). Critical-evaluation of organic-acid mediated iron dissolution in the rhizosophere and its potential role in root iron uptake. Plant and Soil, 180-57-66.
  54. Jones, D. L., P. R. Darrah, and L. V. Kochian. (1996a). Critical-evaluation of organic-acid mediated iron dissolution in the rhizosophere and its potential role in root iron uptake. Plant and Soil, 180-57-66.
  55. Jones, D. L., Shaff, J. E., and Kochian L. V. (1995). Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. 1. Inhibition of tip growth by aluminum. Planta. 197:672-680.
  56. Karltun, E. (1998). Modelling SOsurface complexation on varible charge minerals. II. Competition between SO, oxalate and fulvate. Eur. J. Soil Sci. 49:113-120.
  57. Khademi, Z., 2006. Organic acids behavior in calcareous soils. PhD thesis. University of Wales, Soil Science and Environment.
  58. Kirk, G. J. D., (2002). Modeling root- induced solubilization of nutrients. Palnt and Soil 255, 49-57.
  59. Kochian, L. V. and Jones, D. L. (1997). Aluminum toxicity and resistance in plants. In Research Issues in Aluminum Toxicity. Eds. R A Yokel and M S Golub. Taylor and Francis Publishers. Bristol. PA.
  60. Kraffezyk, , G. Trolldenier, H. Beringer. (1984). Soluble root exudates of maize: Influence of potassium supply and rhizophere microorganisms. Soil Biol. Biochem. 16: 315-322.
  61. Krzyszowska, A. J., Blaylock M. J., Vance G. F., David M., B. (1996). Ionchromatographic analysis of low molecular weight organic acids in spodsol forest solutions. Soil Sci. Soc. Am. J. 60:1565-1571.
  62. Laheurte, F. ad J. Berthelin. (1988). Effect of phosphate solubilizing bacteria on maize growth and root exudation over four levels of labile phosphorus. Plant and Soil, 105: 11-17.
  63. Landsberg, E. C. (1981). Organic acid synthesis and release of hy-drogen ions response to Fe deficiency stress of mono and dicotyledonous plant species. J. Plant Nutr. 3:579-591.
  64. Lipton, D. S., R. W. Blanchar and D. G. Blevins. (1987). Citrate, malate and succinate concentration in exudates from P-sufficient and P-stressed Medicago sativa seedlings. Plant Physiol., 85: 315-317.
  65. Lundstrom, S., Van Breemen, N. and Jongmans. A. G. (1995). Evidence for micorbial decomposition of organic acids during podzolization. Eur. J. Soil Sci., 46: 489-496.
  66. Lunstrom, S., Van Breemen, N., Jongmans A. G. (1995). Evidence for microbial decomposition of organic acids during podzolization. Eur. J. Soil Sci. 46:489-96.
  67. Marschner, H. 1995. Mineral nutrition of higher plants. Academic Press, London.
  68. Marschner, H., (1986). Mineral nutrition of Higher Plants. Academic Press, London.
  69. Marschner, H., Römheld, V., (1996). Root induced changes in the availability of micronutrients in the rhizosphere. In Plant Roots. The hidden Half, 2 nd edn., ed. Waisel, Y., Eshel, A., Kafkafi, U., Marcel Dekk, New York, 557 pp.
  70. Marschner, H., Römheld, V., Cakmak, , (1987). Root- induced changes of nutrient availability in the rhizosphere. Journa of Plant Nutrition 10, 1175-1184.
  71. Marschner, P., Rengel, Z., (2003). Contributions of rhizosphere interactions to soil biological fertility I n: Soil Biological Fertility, A key to Sustainable Land use in Agriculture. Edited by Lynette K, Abbott and Daniel V Murphy, Kluwer Academic publishers.
  72. Mawdsley J. L., Burns R.G. (1994). Root colonization by a Flavobacterium species and the influence of percolating water. Soil Biol. Biochem. 26:861-70.
  73. Mench, M. and E. Martin. (1991). Mobilization of cadmium and other metals form two soils by root exudates of Zea mays Nicotiana tabacum L and Nicotiana rustica L. Plant and Soil, 132: 187-196.
  74. Merbach, W., Mirus, E., Knof, G., Remus, R., Ruppel, S., Russow, R., Gransee, A., Schulze, J., (1999). Release of carbon and nitrogen compounds by plant roots and their possible ecological importance. Journal of Plant Nutrition and Soil Science 162, 373-383.
  75. Micales, J. A. (1997). Location and induction of oxalate decarboxylase in the brown- rot wood decay fungus postia planceta. Int. Biodeterioration Biodegrad. 39, 125-132.
  76. Millet, M., Wortham, H., Sanusi and Mirabel, P. (1997). Low molecular weight organic acids in fogwater in an urban area: Strabourg (France). Sci. Tot. Environ. 206:57-65.
  77. Neumann, G., Massonneau, A., Martinoia, A. Römheld, V., (1999). Physiological adaptations to phosphorus deficiency during proteoid root development in white lupin. Planta 208, 373-82.
  78. Nobel, P. S. (1991). Physiochemical and Enviromental Plant Physiology. Academic Press. London.
  79. Ohwaki, Y. and Sugahara, K. (1997). Active extrusion of protons and exudation of carboxylic acid in response to iron deficiency by roots of carboxylic acids in response to iron deficiency by roots of chicpea (Cicer arietinum ). Plant and Soil, 189:49-55.
  80. Osmond, C. B. (1976). Ion absorption and carbon metabilism in cells of higher plants. In Encyclopedia of Plant Physiology, New Series, Vol. 2, Part A. Eds. U Luttge and M G Pitman. pp. 347-372. Springer-Verlag, Berlin.
  81. Osmond, C. B. and Laties, G. G. (1969). Compartmentation of malate in relation to ion absorption in beet. Plant Physiol. 44:7-14.
  82. Papernik, L. A. and Kochian, L. V. 1997. Possible involvement of Alinduced electrical signals in Al tolerance in wheat. Plant Physiol. 115:657-667.
  83. Parker, D. R., Chaney, R. L. and Norvell, W. A. (1995). Chemical equilibria models: Applications to plant research. In Chemical Equilibria and Reaction Models, Special Publication 42. Ede. R H Loeppert, A P Schwab and S Goldberg. pp. 163-200. SSSA-ASA, Madison, WI.
  84. Patel, D., Barlow, P. W., Lee, R. B. (1990). Development of vacuolor volume in the root- tips of pea. Ann. Bot. 65, 159-169.
  85. Pell, D. M., Grunes, D. L., Kochian, L. V. (1995). Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788-95.
  86. Pohlman, A. A. and J. G. McColl. (1986). Kinetics of metal dissolution from forest soils by soluble organic acids. J. Environ. Qual., 15: 86-92.
  87. Pohlman, A. A. and J. G. McColl. (1988). Soluble organies from forest litter and their role in metal dissolution. Soil Sci. Soc. Am. J. 52: 265-271.
  88. Römheld, V., (1991). The role of phytosicerophores in acquisition of iron and other micronutrients in graminaceous species: and ecologiacl approach. Plant and Soil 130, 127-134.
  89. Rózycki, H. (1985). Production of organic acids by bacteria isolated from soil, rhizosphere and mycorrhizosphere of pine (Pinus sylvestris). Acta Microbiol. Polon. 34:301-308.
  90. Rózycki, H. and Strzelezyk, E. (1986). Organic acids production by Streptomyces spp isolated from soil, rhizosphere and mycorrhizosphere of pine (Pinus sylvestris). Plant and Soil, 96:337-345.
  91. Ryan, P. R., Delhaize, E. Randall, P. J. (1995). Malate efflux from root apices and tolerance to aluminium are highly correlated in wheat. Aust. J. Plant Physiol. 122: 531-536.
  92. Samuels, A. L., M. Fernando, and A. D. Glass. (1992). Immunoflorescent localization of plasma membrane H+-ATPase in barley roots and effects of K nutrition. Plant Physiol., 99: 1509-1514.
  93. Schachtman DP, ­Reid RJ, ­Ayling SM. ­(1998). Phosphorus uptake by plants: from soil to cell. Plant Physiol. 116:447-53.
  94. Schwab, S. M., J. A. Menge, and R. T. Leonard. (1983). Quantitative and qualitative effects of phosphorus on extracts and exudates of sudangrass roots in relation to vesicular-arbuscular mycorrhiza formation. Plant Physiol. 73: 761-765.
  95. Shen, Y., L. Strom, J. A. Jonsson, G. Tyler. (1996). Low-molecular organic-acids in the rhizosphere soil solution of beech forest (Fagus sylvatical ) cambisols determined by ion chromatography using supported liquid membrane enrichment technique. Soil Biol. Biochem., 28: 1163-1169.
  96. Ström, L. (1997). Root exudation of organic acids: importance to nutrient availability and the califuge and calcicole behavior of plants. Oikos 80:459-466.
  97. Ström, L., (1997). Root exudation of organic acids: importance to nutrient availability and the calcifuge and calciocle behavior of plants. Oikos 80, 459-466.
  98. Ström, L., Olsson, T., Tyler, G., (1994). Differences between calcifuge and acidifuge plants in root exduation of low molecular organic acids. Plant and Soil 167, 239-45.
  99. Ström, L., T. Olsson, and G. Tyler. (1994). Differences between calcifuge and acidifuge plants in root exudation of low molecular organic-acids. Plant and Soil, 167: 239-245.
  100. Stumpf, D. K., and Burris, R. H. (1981). Organic-acid contents of soybean: Age and source of nitrigen. Plant Physiol. 68: 989-991.
  101. Tyler, G., Ström, L., (1995). Differeing organic- acid exduation pattern explain calcifuge and acidifuge behavior of plants. Annals of Botany 75, 75-78.
  102. Uren, N. C., Reiscanuer, H. M., (1988). The role of root exduates in nutrient acquisition. Advances in Plant Nutrition 3, 79-114.
  103. Van Hees, P. A. W., Andersson, A. M. T., Lundström, S. (1996). Separation of organic low-molecular-weight aluminum complexes in soil solution by liquid-chromatography. Chemosphere. 33:1951-66.
  104. Watt, M., Evans J. R. (1999). Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 Plant Physiol. 120:705-16.
  105. Welch, R. M. Norvell, W. A. Schaefer, S. C. Shaff, J. E. and Kochian, L. V. (1993). Induction of iron (III) and copper (II) reduction in pea (Pisum sativum) roots by Fe and Cu status-does the root-cell plasmalemma Fe(III)-chelate reductase perform a general role in regulating cation uptake? Plants. 190:555-561.
  106. Wiehe, W., C. Hechtbuchholz, and G. Hoflich. (1994). Electronmicroscopic investigations on root colonization of Lupinus albus and Pisum sativum with two associative plant-growth promoting rhizobacteria, Pseudomonas fluorescnes and Rhizobium leguminsarum bv Symbiosis, 17: 15-31.
  107. Yang, C. H., Crowley, D. E., (2000). Rhizosphere microbial community structure in relation to root location and plant iron nutritional status. Applied and Environmental Microbiology 66, 345-351.
پژوهش های خاک
دوره 21، شماره 2
اسفند 1396
صفحه 171-189

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