Alteration of cell-wall porosity is involved in osmotic stress-induced enhancement of aluminium resistance in common bean (Phaseolus vulgaris L.)

Journal of Experimental Botany

Volumn 61, Issue 12, 2010, Pages 3245-3258

  Yang, Zhong Bao ^a   Eticha, Dejene ^a   Rao, Idupulapati Madhusudana ^b   Horst, Walter Johannes ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b INTERNATIONAL CENTER FOR TROPICAL AGRICULTURE CIAT   (Colombia)

Author keywords

Aluminium; Apoplast; Drought stress; Intercellular space; Organic acids; Polyethylene glycol; Root elongation

Indexed keywords

ALUMINUM; CITRIC ACID; PECTIN; WATER;

ARTICLE; BEAN; CELL WALL; DROUGHT; DRUG EFFECT; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; MERISTEM; METABOLISM; OSMOSIS; PHYSIOLOGICAL STRESS; PLANT ROOT; POROSITY; DRUG EFFECTS; PHASEOLUS; TOXICITY;

ALUMINUM; CELL WALL; CITRATES; DROUGHTS; GENOTYPE; MERISTEM; OSMOSIS; PECTINS; PHASEOLUS; PLANT ROOTS; POROSITY; STRESS, PHYSIOLOGICAL; WATER;

PHASEOLUS VULGARIS;

EID: 77954791237     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq146     Document Type: Article

References (77)

1. Ahmed AER, Labavitch JM. 1977. A simplified method for accurate determination of cell wall uronide content. Journal of Food Biochemistry 1, 361-365.
2. Baron-Epel O, Gharyal PK, Schindler M. 1988. Pectins as mediators of wall porosity in soybean cells. Planta 175, 389-395.
3. Bauchot AD, Hallett IC, Redgwell RJ, Lallu N. 1999. Cell wall properties of kiwifruit affected by low temperature breakdown. Postharvest Biology and Technology 16, 245-255.
4. Beebe S, Rao IM, Cajiao C, Grajales M. 2008. Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Science 48, 582-592.
5. Blamey FPC, Edmeades DC, Wheeler DM. 1990. Role of root cation-exchange capacity in differential aluminium tolerance of Lotus species. Journal of Plant Nutrition 13, 729-744.
6. Blumenkrantz N, Asboe-Hansen G. 1973. New method for quantitative determination of uronic acids. Analytical Biochemistry 54, 484-489.
7. Brett C, Waldron K. 1996. Physiology and biochemistry of the plant cell wall. London: Chapman and Hall.
8. Broughton WJ, Herná ndez G, Blair M, Beebe S, Gepts P, Vanderleyden J. 2003. Beans (Phaseolus spp.): model food legumes. Plant and Soil 252, 55-128.
9. Carpita N, Sabularse D, Montezinos D, Delmer DP. 1979. Determination of the pore size of cell walls of living plant cells. Science 205, 1144-1147.
10. Chesson A, Gardner PT, Wood TJ. 1997. Cell wall porosity and available surface area of wheat straw and wheat grain fractions. Journal of the Science of Food and Agriculture 75, 289-295
11. CIAT. 1992. Constraints to and opportunities for improving bean production. A planning document 1993-98 and an achieving document 1987-92. Cali, Colombia, CIAT.
12. Cosgrove DJ. 1997. Assembly and enlargement of the primary cell wall in plants. Annual Review of Cell and Developmental Biology 13, 171-201.
13. Cosgrove DJ. 2005. Growth of the plant cell wall. Nature Reviews Molecular Cell Biology 6, 850-861.
14. Cushman JC, Bohnert HJ. 2000. Genomic approaches to plant stress tolerance. Current Opinion in Plant Biology 3, 117-124.
15. de la Fuente JM, Raminrez-Rodriguez V, Cabrera-Ponce JL, Herrera-Estrella L. 1997. Aluminum tolerance in transgenic plants by alteration of citrate synthesis. Science 276, 1566-1568.
16. Delhaize E, Ryan PR. 1995. Aluminum toxicity and tolerance in plants. Plant Physiology 107, 315-321.
17. Eswaran H, Reich P, Beinroth F. 1997. Global distribution of soils with acidity. In: Moniz AC, Furlani AMC, Schaffert RE, Fageria NK, Rosolem CA, Cantarella H, eds. Plant-soil interactions at low pH. Brazil, 159-164.
18. Eticha D, Stass A, Horst WJ. 2005. Cell-wall pectin and its degree of methylation in the maize root apex: significance for genotypic differences in aluminium resistance. Plant, Cell and Environment 28, 1410-1420.
19. Eticha D, Zahn M, Bremer M, Yang Z, Rangel AF, Rao IM, Horst WJ. 2010. Transcriptomic analysis reveals differential gene expression in response to aluminium in common bean (Phaseolus vulgaris) genotypes. Annals of Botany doi: 10.1093/aob/mcq049.
20. Fan L, Neumann PM. 2004. The spatially variable inhibition by water deficit of maize root growth correlates with altered profiles of proton flux and cell wall pH. Plant Physiology 135, 2291-2300.
21. Fleischer A, O'Neill MA, Ehwald R. 1999. The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiology 121, 829-838.
22. Fry SC. 1988. The growing plant cell wall: chemical and metabolic analysis. New York, USA: Longman.
23. Goldman IL, Carter Jr TE, Patterson RP. 1989. A detrimental interaction of subsoil aluminum and drought stress on the leaf water status of soybean. Agronomy Journal 81, 461-463.
24. Graham PH, Ranalli P. 1997. Common bean (Phaseolus vulgaris L.). Field Crops Research 53, 131-146.
25. Hohl M, Schopfer P. 1991. Water relations of growing maize coleoptiles: comparison between mannitol and polyethylene glycol 6000 as external osmotica for adjusting turgor pressure. Plant Physiology 95, 716-722.
26. Horst WJ. 1995. The role of the apoplast in aluminium toxicity and resistance of higher plants: a review. Journal of Plant Nutrition and Soil Science 158, 419-428.
27. Horst WJ, Asher CJ, Cakmak J, Szulkiewicz P, Wissemeier AH. 1992. Short-term responses of soybean roots to aluminium. Journal of Plant Physiology 140, 174-178.
28. Horst WJ, Schmohl N, Kollmeier M, Baluska F, Sivaguru M. 1999. Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant and Soil 215, 163-174.
29. Horst WJ, Wang Y, Eticha D. 2010. The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Annals of Botany doi: 1093/aob/mcq053.
30. Iraki NM, Bressan RA, Hasegawa PM, Carpita NC. 1989a. Alteration of the physical and chemical structure of the primary cell wall of growth-limited plant cells adapted to osmotic stress. Plant Physiology 91, 39-47.
31. Iraki NM, Singh N, Bressan RA, Carpita NC. 1989b. Cell walls of tobacco cells and changes in composition associated with reduced growth upon adaptation to water and saline stress. Plant Physiology 91, 48-53.
32. Ishitani M, Rao I, Wenzl P, Beebe S, Tohme J. 2004. Integration of genomics approach with traditional breeding towards improving abiotic stress adaptation: drought and aluminum toxicity as case studies. Field Crops Research 90, 35-45.
33. Jacomini E, Bertani A, Mapelli S. 1988. Accumulation of polyethylene glycol 6000 and its effects on water content and carbohydrate level in water-stressed tomato plant. Canadian Journal of Botany 66, 970-973.
34. Janes BE. 1974. The effect of molecular size concentration in nutrient solution and exposure time on the amount and distribution of polyethylene glycol. Plant Physiology 54, 226-229.
35. Jarvis MC. 1992. Control of thickness of collenchyma cell walls by pectins. Planta 187, 218-220.
36. Jia W, Zhang J, Liang J. 2001. Initiation and regulation of water deficit-induced abscisic acid accumulation in maize leaves and roots: cellular volume and water relations. Journal of Experimental Botany 52, 295-300.
37. Kerven GL, Edwards DG, Asher CJ, Hallman PS, Kobot S. 1989. Aluminium determination in soil solution. II. Short-term colorimetric procedure for the measurement of inorganic monomeric aluminium in the presence of organic acid ligands. Australian Journal of Soil Research 27, 91-102.
38. Kochian LV, Hoekenga OA, Piñ eros MA. 2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Review of Plant Biology 55, 459-493.
39. Kuga S. 1981. Pore size distribution analysis of gel substances by size exclusion chromatography. Journal of Chromatography 206, 449-461.
40. Lawlor DW. 1970. Absorption of polyethylene glycols by plants and their effects on plant growth. New Phytologist 69, 501-504.
41. Leucci MR, Lenucci MS, Piro G, Dalessandro G. 2008. Water stress and cell wall polysaccharides in the apical root zone of wheat cultivars varying in drought tolerance. Journal of Plant Physiology 165, 1168-1180.
42. McKenna BA, Kopittke PM, Wehr JB, Blamey FP, Menzies NW. 2010. Metal ion effects on hydraulic conductivity of bacterial cellulose-pectin composites used as plant cell wall analogs. Physiologia Plantarum 138, 205-214.
43. Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A. 2008. Adaptations of higher plant cell walls to water loss: drought versus desiccation. Physiologia Plantarum 134, 237-245.
44. Mugai EN, Agong SG, Matsumoto H. 2000. Aluminium tolerance mechanisms in Phaseolus vulgaris L.: citrate synthase activity and TTC reduction are well correlated with citrate secretion. Soil Science and Plant Nutrition 46, 939-950.
45. Nightingale Jr ER. 1959. Phenomenological theory of ion solvation. Effective radii of hydrated ions. Journal of Physical Chemistry 63, 1381-1387.
46. Ogawa A, Yamauchi A. 2006. Root osmotic adjustment under osmotic stress in maize seedlings. 2. Mode of accumulation of several solutes for osmotic adjustment in the root. Plant Production Science 9, 39-46.
47. Premachandra GS, Hahn DT, Rhodes D, Joly RJ. 1995. Leaf water relations and solute accumulation in two grain sorghum lines exhibiting contrasting drought tolerance. Journal of Experimental Botany 46, 1833-1841.
48. Rangel AF, Mobin M, Rao IM, Horst WJ. 2005. Proton toxicity interferes with the screening of common bean (Phaseolus vulgaris L.) genotypes for aluminium resistance in nutrient solution. Journal of Plant Nutrition and Soil Science 168, 607-616.
49. Rangel AF, Rao IM, Braun H-P, Horst WJ. 2010. Aluminium resistance in common bean (Phaseolus vulgaris) involves induction and maintenance of citrate exudation from root apices. Physiologia Plantarum 138, 176-190.
50. Rangel AF, Rao IM, Horst WJ. 2007. Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminium resistance. Journal of Experimental Botany 58, 3895-3904.
51. Rangel AF, Rao IM, Horst WJ. 2009. Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiologia Plantarum 135, 162-173.
52. Rao IM. 2001. Role of physiology in improving crop adaptation to abiotic stresses in the tropics: the case of common bean and tropical forages. In: Pessarakli M, ed. Handbook of plant and crop physiology. New York: Marcel Dekker, 583-613.
53. Ren Z, Zheng Z, Chinnusamy V, Zhu J, Cui X, Lida K, Zhu J-K. 2010. RAS1, a quantitative trait locus for salt tolerance and ABA sensitivity in Arabidopsis. Proceedings of the National Academy of Sciences, USA 107, 5669-5674.
54. Ryan PR, DiTomaso JM, Kochian LV. 1993. Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. Journal of Experimental Botany 44, 437-446.
55. Schmohl N, Horst WJ. 2000. Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cell grown in suspension culture. Plant, Cell and Environment 23, 735-742.
56. Schmohl N, Pilling J, Fisahn J, Horst WJ. 2000. Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiologia Plantarum 109, 419-427. (Pubitemid 30637962)
57. Serraj R, Sinclair TR. 2002. Osmolyte accumulation: can it really help increase crop yield under drought conditions? Plant, Cell and Environment 25, 333-341.
58. Sharp RE. 2002. Interaction with ethylene: changing views on the role of ABA in root and shoot growth responses to water stress. Plant, Cell and Environment 25, 211-222.
59. Sharp RE, Silk WK, Hsiao TC. 1988. Growth of the maize primary root at low water potentials. I. Spatial distribution of expansive growth. Plant Physiology 87, 50-57.
60. Shen H, Ligaba A, Yamaguchi M, Osawa H, Shibata K, Yan XL, Matsumoto H. 2004. Effect of K-252a and abscisic acid on the efflux of citrate from soybean roots. Journal of Experimental Botany 55, 663-671.
61. Shen H, Yan X, Wang X, Zheng S. 2002. Exudation of citrate in common bean in response to aluminum stress. Journal of Plant Nutrition 25, 1921-1932.
62. Singh SP. 2001. Broadening the genetic base of common bean cultivars: a review. Crop Science 41, 1659-1675.
63. Sivaguru M, Horst WJ. 1998. The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize. Plant Physiology 116, 155-163.
64. Sponchiado BN, White JW, Castillo JA, Jones PG. 1989. Root growth of four common bean cultivars in relation to drought tolerance in environments with contrasting soil types. Experimental Agriculture 25, 249-257.
65. Taylor GJ, McDonald-Stephens JL, Hunter DB, Bertsch PM, Elmore D, Rengel Z, Reid RJ. 2000. Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiology 123, 987-996.
66. Thung M, Rao IM. 1999. Integrated management of abiotic stresses. In: Singh SP, ed. Common bean improvement in the twenty-first century. Dordrecht: Kluwer Academic Publishers, 331-370.
67. von Uexküll HR, Mutert E. 1995. Global extent, development and economic impact of acid soils. Plant and Soil 171, 1-15.
68. Wakabayashi K, Hoson T, Kamisaka S. 1997. Changes in amounts and molecular mass distribution of cell wall polysaccharides of wheat (Triticum aestivum L.) coleoptiles under water stress. Journal of Plant Physiology 151, 33-40.
69. Wang Y, Stass A, Horst WJ. 2004. Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiology 136, 3762-3770.
70. Welcker C, Théc C, Andréau B, et al. 2005. Heterosis and combining ability for maize adaptation to tropical acid soils: Implications for future breeding strategies. Crop Science 45, 2405-2413.
71. Westgate ME, Boyer JS. 1985. Osmotic adjustment and the inhibition of leaf, root, stem and silk growth at low water potentials in maize. Planta 164, 540-549.
72. Wojciechowski CL, Fall F. 1996. A continuous fluorometric assay for pectin methylesterase. Analytical Biochemistry 137, 103-108.
73. Wu Y, Cosgrove DJ. 2000. Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins. Journal of Experimental Botany 51, 1543-1553.
74. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Wu P, Zheng SJ. 2008. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiology 146, 602-611.
75. Yang ZB, You JF, Xu MY, Yang ZM. 2009. Interaction between aluminum toxicity and manganese toxicity in soybean (Glycine max). Plant and Soil 319, 277-289.
76. Yaniv Z, Werker E. 1983. Absorption and secretion of polyethylene glycol by Solanaceous plants. Journal of Experimental Botany 34, 1577-1584.
77. Zhang G, Taylor GJ. 1989. Kinetics of aluminum uptake by excised roots of aluminum-tolerant and aluminum-sensitive cultivars of Triticum aestivum L. Plant Physiology 91, 1094-1099.