Aquaporin Functionality in Roots of Zea mays in Relation to the Interactive Effects of Boron and Salinity

Abstract

Zea mays L. cv. amylacea, a plant tolerant of B and salinity, was used to determine the involvement of aquaporin functionality in the interactive effects of B and salinity. Also, growth, chlorophyll concentration, and water relations were studied. While growth and chlorophyll concentration did not show noticeable changes under saline conditions, the decrease in leaf water potential and osmotic potential, together with the marked decrease of stomatal conductance and root hydraulic conductance, showed that the plants were adjusted osmotically. However, no effect of B was observed. The very weak response of the Lp_c of salt-stressed roots to Hg suggested that water channels were greatly reduced in number or, if present, were non-functional. The evidence that substantial B movement can occur through diffusion and channel-mediated transport is compelling, and could account for B uptake under conditions of adequate or greater B supply. Therefore, the reduction in the functionality of aquaporins for NaCl-treated plants could be related to the reduction of B concentrations in roots and leaves in B + NaCl-treated plants, in comparison with plants treated only with B.

Key words

Aquaporins - boron - cell pressure probe - chlorophyll concentration - root hydraulic conductivity - salinity - stomatal conductance - water relations.

References

• 1 Alpaslan M., Gunes A.. Interactive effects of B and salinity stress on the growth, membrane permeability and mineral composition of tomato and cucumber plants.  Plant Soil. (2001);  236 123-128
• 2 Arnon D. L.. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. .  Plant Physiol.. (1949);  24 1-15
• 3 Awang Y. P., Atherton J. G., Taylor A. J.. Salinity effects on strawberry plants grown in rockwool. I. Growth and leaf water relations.  J. Hort. Sci.. (1993);  65 783-790
• 4 Bañuelos G. S., Ajwa H. A., Caceres L., Dyer D.. Germination responses and B accumulation in germplasm from Chile and United States grown with B-enriched water.  Ecotoxicology and Environmental Safety. (1999);  43 62-67
• 5 Ben-Gal A., Shani U.. Yield, transpiration and growth of tomatoes under combined excess B and salinity stress.  Plant Soil. (2002);  247 211-221
• 6 Biela A., Grote K., Otto B., Hoth S., Hedrich R., Kaldenhoff R.. The Nicotiana tabacum plasma membrane aquaporin in NtAQP1 is mercury-insensitive and permeable for glycerol.  Plant J.. (1999);  18 565-570
• 7 Brown P. H., Bellaloui N., Wimmer M. A., Bassil E. S., Ruiz J., Hu H., Pfeffer H., Dannel F., Römheld V.. B in plant biology.  Plant Biology. (2002);  4 205-223
• 8 Carvajal M., Cooke D. T., Clarkson D. T.. Responses of wheat plants to nutrient deprivation may involve the regulation of water-channel function.  Planta. (1996);  199 372-381
• 9 Carvajal M., Martinez V., Alcaraz C. F.. Physiological function of water-channels, as affected by salinity in roots of paprika pepper.  Physiol. Plant.. (1999);  105 95-101
• 10 Chrispeels M. J., Maurel C.. Aquaporins: the molecular basis of facilitated water movement through living plants cell?.  Plant Physiol.. (1994);  105 9-13
• 11 Dannel F., Pfeffer H., Römheld V.. Update on B in higher plants - uptake, primary translocation and compartmentation.  Plant Biology. (2002);  4 193-204
• 12 Delfine S., Alvino A., Zacchini M., Loreto F.. Consequences of salt stress on conductance to CO₂ diffusion, Rubisco characteristics, anatomy of spinach leaves.  Aust. J. Plant Physiol.. (1998);  25 395-402
• 13 Dordas C., Chrispeels M. J., Brown P. H.. Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots.  Plant Physiol.. (2000);  124 1349-1361
• 14 Ehret D. L., Ho L. C.. The effect of salinity on dry matter partitioning and fruit growth in tomatoes growing in nutrient film culture.  J. Hort. Sci.. (1986);  61 361-367
• 15 El-Hamdaoui A., Redondo-Nieto M., Torralba B., Rivilla R., Bonilla I., Bolanos L.. Influence of B and calcium on the tolerance to salinity of nitrogen-fixing pea plants.  Plant Soil.. (2003);  251 93-103
• 16 El-Shintinawy F.. Structural and functional damage caused by B deficiency in sunflower leaves.  Photosynthetica. (1999);  36 565-573
• 17 Ferrol N., Belver A., Roldan M., Rodriguez-Rosales M. P., Donaire J. P.. Effects of B on proton transport and membrane properties of sunflower (Helianthus annuus L.) cell microsomes.  Plant Physiol.. (1993);  103 763-769
• 18 Gerbeau P., Güçlü J., Ripoche P., Maurel C.. Aquaporin Nt-TIPa can account for the high permeability of tobacco cell vacuolar membrane to small neutral solutes.  Plant J.. (1999);  18 577-587
• 19 Gibbs J., Dracup M., Greenway H., McComb J. A.. Effects of high NaCl on growth, turgor and internal solutes of tobacco callus.  J. Plant Physiol.. (1988);  134 61-69
• 48 González-Moro B., Lacuesta M., Becerril J. M., González-Murua C., Muñoz-Rueda A.. Glycolate accumulation causes a decrease of photosynthesis by inhibiting RUBISCO activity in maize.  J. Plant Physiol.. (1997);  150 388-394
• 20 Greenway H., Munns R.. Mechanism of salt tolerance in nonhalophytes.  Ann. Rev. Plant. Physiol.. (1980);  31 149-190
• 21 Grieve C. M., Poss J. A.. Wheat response to interactive effects of B and salinity.  J. Plant Nutr.. (2000);  23 1217-1226
• 22 Hoffman G. J.. Guidelines for reclamation of salt-affected soils.  Appl. Agr. Res.. (1986);  1 65-72
• 23 Holloway R. E., Alston A. M.. The effects of salt and B on growth of wheat.  Aust. J. Agric. Res.. (1992);  43 987-1001
• 24 Ismail A. M.. Response of maize and sorghum to excess B and salinity.  Biol. Plant.. (2003);  47 313-316
• 25 Jackson M. B., Davies W. J., Else M. A.. Pressure-flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants.  Ann. Bot.. (1996);  77 17-24
• 26 Johansson I., Larsson C., Ek B., Kjelbom P.. The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca²⁺ and apoplastic water potential.  Plant Cell.. (1996);  8 1181-1191
• 27 Kurt E., Cramer G. R., Lauchli A., Epstein E.. Effects of NaCl and CaCl₂ on root cell enlargement and cell production in cotton roots.  Plant Physiol.. (1986);  82 1102-1106
• 28 Leidi E. O., Silberbush M., Lips S. H.. Wheat growth as affected by nitrogen type, pH and salinity. II. Photosynthesis and transpiration.  J. Plant Nutr.. (1991);  14 247-256
• 29 Li Y. L., Stanghellini C., Challa H.. Effect of electrical conductivity and transpiration of production of greenhouse tomato (Lycopersicum esculentum L.).  Sci. Hortic.. (2001);  88 11-29
• 30 Maas E. V.. Salt tolerance of plants.  Appl. Agric. Res.. (1986);  1 12-26
• 31 Maggio A., Joly R. J.. Effects of mercuric chloride on the hydraulic conductivity of tomato root systems. Evidence for a channel mediated water pathway.  Plant Physiol.. (1995);  109 331-335
• 32 Martínez-Ballesta M. C., Aparicio F., Payas V., Martínez V., Carvajal M.. Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. .  J. Plant Physiol.. (2003 a);  160 689-697
• 33 Martínez-Ballesta M. C., Diaz R., Martínez V., Carvajal M.. Different blocking effects of HgCl₂ and NaCl on aquaporins of pepper plants.  J. Plant Physiol.. (2003 b);  160 1487-1492
• 34 Matt J. K., Chuah H. H., Neufeld J. H.. Applications of improved azoinethime-H method in the determination of B in soils and plants.  Anal. Lett.. (1975);  8 8559-8568
• 35 Papadakis I. E., Dimassi K. N., Therios I. N.. Response of two citrus genotypes to six B concentrations: concentration and distribution of nutrients, total absorption, and nutrient use efficiency.  Aust. J. Agr. Res.. (2003);  54 571-580
• 36 Parker I., Paratori O.. Distribución geográfica, clasificación y estudio del maiz (Zea mays) en Chile.  Agricultura Tecnica.. (1965);  25 70-86
• 37 Schäffner A. R.. Aquaporin function, structure, and expression: are there more surprises to surface in water relations?.  Planta. (1998);  204 131-139
• 38 Shennan C., Grattan S. R., May D. M., Hillhouse C. J., Schachtman D. P., Wander M., Raberts B., Tafoya S., Burau R. S., McNeish C., Lelinshi C.. Feasibility of cyclic reuse of saline drainage in a tomato cotton rotation.  J. Environ. Qual.. (1995);  24 476-486
• 39 Sotiropoulos T. E., Therios I. N., Dimassi K. N., Bosabalidis A., Kofidis G.. Nutritional status, growth, CO₂ assimilation, and leaf anatomical responses in two kiwifruit species under B toxicity.  J. Plant Nutr.. (2002);  25 1249-1261
• 40 Sternberg P. D., Ulery A. L., Villa-C. M.. Salinity and B effects on growth and yield of terapy and kidney beans.  HortScience. (2001);  36 1269-1272
• 41 Steudle E.. Pressure probe techniques: basic principles and application to studies of water and solute relations at the cell, tissue, and organ level. Smith, J. A. C. and Griffith, H., eds. Water Deficits: Plant Responses From Cell to Community. Oxford; BIOS Scientific Publishers (1993): 5-36
• 42 Steudle E., Tyerman S. D.. Determination of permeability coefficients, reflection coefficients and hydraulic conductivity of Chara corallina using pressure probe: effects of solute concentrations.  J. Memb. Biol.. (1983);  75 85-96
• 43 Takano J., Noguchi K., Yasumori M., Kobayashi M., Gajdos Z., Miwa K., Hayashi H., Yoneyama T., Fujiwara T.. Arabidopsis boron transporter for xylem loading.  Nature. (2002);  420 337-340
• 44 Wang Y., Nii N.. Changes in chlorophyll ribulose bisphosphate carboxygenase, glycine betaine content, photosynthesis and transpiration in Amaranthus tricolor leaves during salt stress.  J. Hortic. Sci. Biotech.. (2000);  75 623-627
• 45 Wimmer M. A., Muhling K. H., Lauchli A., Brown P. H., Goldbach H. E.. The interaction between salinity and B toxicity affects the subcellular distribution of ions and proteins in wheat leaves.  Plant Cell Environ.. (2003);  26 1267-1274
• 46 Zhu J. K.. Plant salt tolerance.  Trends Plant Sci.. (2001);  6 66-71
• 47 Zimmermann U.. Physics of turgor and osmo-regulation.  Annu. Rev. Plant Physiol.. (1978);  29 121-148

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