Efectos de la combinación de salinidad y exceso de boro en las relaciones hídricas del tomate (Solanum lycopersicum L.) tolerante cv. Poncho Negro y su relación con la funcionalidad de las acuaporinas
Resumen
En muchas ocasiones niveles elevados de boro (B) van acompañados de condiciones de excesiva salinidad, cuyasconsecuencias pueden ser drásticas para los cultivos, por lo que es fundamental encontrar variedades que puedan tolerar
estas condiciones. En este trabajo, se estudió cómo la interacción entre la salinidad y el exceso de B afecta a la
actividad de las acuaporinas y a las relaciones hídricas, así como al ajuste osmótico de las plantas. Se cultivó en hidroponíatomate cv Poncho Negro en una cámara de crecimiento con ambiente controlado con los tratamientos control, NaCl (75 y 150 mM) y/o B (5 ó 20 mg L–1). No se observó ningún efecto aditivo (sinergia) del exceso de B y la
salinidad. Las plantas aumentaron su turgencia en condiciones salinas, compensando así la disminución del potencial hídrico foliar, a través de la reducción de su potencial osmótico por la acumulación de azúcares solubles y prolina. La participación de acuaporinas insensibles al Hg+2 o del gradiente osmótico, como la principal fuerza impulsora del flujo del agua, a través de la vía apoplástica, deben ser contemplados. Finalmente, todos los datos revelan que el tomate cv. Poncho Negro puede ser un germoplasma de interés agronómico y una buena alternativa para cultivar en condiciones de alto contenido de sales y exceso de B del suelo y del agua de riego.
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Alpaslan M., Gunes A., 2001. Interactive effects of B and salinity stress on the growth, membrane permeability and mineral composition of tomato and cucumber plants. Plant Soil 236, 123-128. http://dx.doi.org/10.1023/A:1011931831273
Azaizeh H., Steudle E., 1991. Effects of salinity on water transport of excised maize (Zea mays L.) roots. Plant Physiol 97, 1136-1145. http://dx.doi.org/10.1104/pp.97.3.1136 PMid:16668500 PMCid:1081133
Bastías E., Fernández-García N., Carvajal M., 2004a. Aquaporin functionality in roots of Zea mays in relation to the interactive effects of boron and salinity. Plant Biol 5, 415-421. http://dx.doi.org/10.1055/s-2004-820889 PMid:15248124
Bastías E., González-Moro M.B., Gonzálezmurua C., 2004b. Zea mays L. Amylacea from the Lluta Valley (Arica-Chile) tolerates salinity stress when high levels of boron are available. Plant Soil 267, 73-84. http://dx.doi.org/10.1007/s11104-005-4292-y
Bates L.S., 1973. Rapid determination of free proline for water stress studies. Plant Soil 39, 205-207. http://dx.doi.org/10.1007/BF00018060
Ben-Gal A., Shani U., 2002. Yield, transpiration and growth of tomatoes under combined excess boron and salinity stress. Plant Soil 247, 211-221. http://dx.doi.org/10.1023/A:1021556808595
Bernstein L., 1975. Effects of salinity and sodicity on plant growth. Ann Rev Phytopath 13, 295-312. http://dx.doi.org/10.1146/annurev.py.13.090175.001455
Blum A., 1996. Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20, 135-148. http://dx.doi.org/10.1007/BF00024010
Bramley H., Turner N., Turner D.W., Tyerman S.D., 2009. Roles of morphology, anatomy, and aquaporins in determining contrasting hydraulic behaviour of roots. Plant Physiol 150,348-364. http://dx.doi.org/10.1104/pp.108.134098 PMid:19321713 PMCid:2675714
Carvajal M., Cooke D.T., Clarkson D.T., 1996. Responses of wheat plants to nutrient deprivation may involve the regulation of water channel function. Planta 199, 372-381. http://dx.doi.org/10.1007/BF00195729
Carvajal M., Martínez V., Alcaraz C.F., 1999. Physiological function of water channels, as affected by salinity in roots of paprika pepper. Physiol Plant 105, 95-101. http://dx.doi.org/10.1034/j.1399-3054.1999.105115.x
Carvajal M., Cerda A., Martínez V., 2000. Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating aquaporin activity? New Phytol 145, 439-447. http://dx.doi.org/10.1046/j.1469-8137.2000.00593.x
Cervilla L., Blasco B., Ríos J., Romero L., Ruiz J., 2007. Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100, 747-756. http://dx.doi.org/10.1093/aob/mcm156 PMid:17660516 PMCid:2749626
Chrispeels M.J., Agre P., 1994. Aquaporins: water channel proteins of plant and animal cells. Trends Biochem Sci 19, 421-425. http://dx.doi.org/10.1016/0968-0004(94)90091-4
Chrispeels M.J., Maurel C., 1994. Aquaporins: the molecular basis of facilitated water movement through living plant cells? Plant Physiol 105, 9-13. http://dx.doi.org/10.1104/pp.105.1.9 PMid:7518091 PMCid:159323
Díaz M., 2008. Interacción del boro en la tolerancia a la salinidad de Lycopersicon esculentum Mill. var. 'Poncho Negro' proveniente del Valle de Lluta (Provincia de Arica-Chile). Tesis (Pré-grado). Universidad de Tarapacá, Chile. [In Spanish].
Dordas C., Brown P.H., 2001. Evidence for channel mediated transport of boric acid in squash (Cucurbita pepo). Plant Soil 235, 95-103. http://dx.doi.org/10.1023/A:1011837903688
Dordas C., Chrispeels M.J., Brown P.H., 2000. Permeability and channel mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 124, 1349-1361. http://dx.doi.org/10.1104/pp.124.3.1349 PMid:11080310 PMCid:59232
Edelstein M., Ben-Hur M., Cohen Y., Burger Y., Ravina I., 2005. Boron and salinity effects on grafted and non-grafted melon plants. Plant Soil 269, 273-284. http://dx.doi.org/10.1007/s11104-004-0598-4
Flowers T.J., 2004. Improving crop salt tolerance. J Exp Bot 396, 307-319. http://dx.doi.org/10.1093/jxb/erh003 PMid:14718494
Fitzpatrick K.L., Reid R.J., 2009. Involvement of aquaglyceroporins in transport of boron in barley roots. Plan Cell Environ 32, 1357-1365. http://dx.doi.org/10.1111/j.1365-3040.2009.02003.x PMid:19552667
Ghanati F., Morita A., Yokota H., 2002. Deposition of suberin in roots of soybean induced by excess boron. Plant Sci 168, 397-405. http://dx.doi.org/10.1016/j.plantsci.2004.09.004
Gupta U.C., Jame Y.W., Cambell C.A., Leyshon A.J., Nichlaichuck W., 1985. Boron toxicity and deficiency. A review. Can J Soil Sci 65, 381-409. http://dx.doi.org/10.4141/cjss85-044
Hachez C., Moshelion M.E., Zelazny E., Cavez D., Chaumont F., 2006. Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62, 305-323. http://dx.doi.org/10.1007/s11103-006-9022-1 PMid:16845476
Hayes J.E., Reid R.J., 2004. Boron tolerance in barley is mediated by efflux of boron from the roots. Plant Physiol 136, 3376-3382. http://dx.doi.org/10.1104/pp.103.037028 PMid:15466242 PMCid:523396
Irigoyen J.J., Einerich D.W., Sánchez-Díaz M., 1992. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicagosativa) plants. Physiol Plantarum 84, 55-60. http://dx.doi.org/10.1111/j.1399-3054.1992.tb08764.x
Jackson M.B., Davies W.J., Else M.A., 1996. Pressure flow relationships, xylem solutes and root hydraulic conductance in flooded tomato plants. Ann Bot 77, 17-24. http://dx.doi.org/10.1006/anbo.1996.0003
Javot H., Maurel C., 2002. The role of aquaporins in root water uptake. Ann Bot 90, 301-313. http://dx.doi.org/10.1093/aob/mcf199
Karabal E., Yücel M., Ökte H.A., 2003. Antioxidants responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Sci 164, 925-933. http://dx.doi.org/10.1016/S0168-9452(03)00067-0
Loomis W.D., Durts R.W., 1992. Chemistry and biology of boron. Biofactors 3, 229-239. PMid:1605832
Lovatt C.J., Bates L.M., 1984. Early effects of excess boron on photosynthesis and growth of Cucurbita pepo. J Exp Bot 35, 297-305. http://dx.doi.org/10.1093/jxb/35.3.297
Maggio A., Joly R.J., 1995. Effects of mercuric chloride on the hydraulic conductivity of tomato root system. Evidence for a channel mediated water pathway. Plant Physiol 109, 331-335. PMid:12228599 PMCid:157593
Martínez-Ballesta M.C., Martínez V., Carvajal M., 2000. Regulation of water channel activity in whole roots and in protoplasts from roots of melon plants grown under saline conditions. Aust J Plant Physiol 27, 685-691.
Martínez-Ballesta M.C., Martínez V., Carvajal M., 2004. Osmotic adjustment, water relations and gas exchange in pepper plants grown under NaCl or KCl. Environ Exp Bot 52, 161-174. http://dx.doi.org/10.1016/j.envexpbot.2004.01.012
Martínez-Ballesta M., Bastías E., Zhu C., Schäffner A.R., González-Moro B., Gonzálezmurua C., Carvajal M., 2008. Boric acid and salinity effects on maize roots. Response of aquaporins ZmPIP1 and ZmPIP2, and plasma membrane H+-ATPase, in relation to water and nutrient uptake. Physiol Plantarum 132, 479-490. http://dx.doi.org/10.1111/j.1399-3054.2007.01045.x PMid:18334001
Maurel C., 1997. Aquaporin and water permeability of plant membranas. Ann Rev Plant Physiol Plant Mol Biol 48, 339-430. http://dx.doi.org/10.1146/annurev.arplant.48.1.399 PMid:15012269
Maurel C., Chrispeels M.J., 2001. Aquaporins. A molecular entry into plant water relations. Plant Physiol 125, 135-138. http://dx.doi.org/10.1104/pp.125.1.135 PMid:11154316 PMCid:1539345
Maurel C., Doan-Trung L., Santoni V., Verdoucq L., 2008. Plant aquaporins. Membrane channels with multiple integrated functions. Ann Rev Plant Physiol 59, 595-624.
Munns R., Tester M., 2008. Mechanisms of salinity tolerance. Ann Rev Plant Physiol 59, 651-81.
Munns R., Termaat A., 1986. Whole-plant responses to salinity. Aust J Plant Physiol 13, 143-160. http://dx.doi.org/10.1071/PP9860143
Nable R.O., Lance R.C.M., Cartwright B., 1990. Uptake of boron and silicon by barley genotypes with differing susceptibilities to boron toxicity. Ann Bot 66, 83-90.
Nobel P.S., 1991. Physicochemical and environmental plant physiology. The National Academies Press, London, UK. 489 pp.
Passioura J., 2007. The drought environment: physical, biological and agricultural perspectives. J Exp Bot 58, 113-117. http://dx.doi.org/10.1093/jxb/erl212 PMid:17122406
Power P.P., Woods W.G., 1997. The chemistry of boron and its speciation in plants. Plant Soil 193, 1-13. http://dx.doi.org/10.1023/A:1004231922434
Qi C.H., Chen M., Song J., Wang B.S., 2009. Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity. Plant Sci 176, 200-205. http://dx.doi.org/10.1016/j.plantsci.2008.09.019
Reid R., 2007. Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. Plant Cell Physiol 48, 1673-1678. http://dx.doi.org/10.1093/pcp/pcm159 PMid:18003669
Reid R., Hayes J., Post A., Stangoulis J., Graham R., 2004. A critical analysis of the cause of boron toxicity in plants. Plant Cell Environ 27, 1405-1414. http://dx.doi.org/10.1111/j.1365-3040.2004.01243.x
Rengasamy P., 2002. Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust J Exp Agric 42, 351-361. http://dx.doi.org/10.1071/EA01111
Sade N., Vinocur B.F., Diber A., 2009. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2; 2 a key to isohydric to anisohydric conversion? New Phytol 181, 651-661. http://dx.doi.org/10.1111/j.1469-8137.2008.02689.x PMid:19054338
Shi H., Ishitani M., Kim C., Zhu J.K., 2000. The Arabidopsis thaliana salt tolerance genes SOS1 encodes a putative Na+/H+ antiporter. Proc Nat Acad Sci USA 97,6896-6901. http://dx.doi.org/10.1073/pnas.120170197 PMid:10823923 PMCid:18772
Stangoulis J.C.R., Reid R.J., Brown P.H., Graham R.D., 2001. Kinetic analysis of boron transport in Chara. Planta 213, 142-146. http://dx.doi.org/10.1007/s004250000484 PMid:11523650
Steudle E., Heydt H., 1997. Water transport across tree roots. In: Trees-contributions to modern tree physiology (Rennenberg H., Eschrich W., Ziegler H., eds). Backhuys Publ, Leiden, The Netherlands. pp. 239-255.
Sutton T., Baumann U., Hayes J., Collins N.C., Shi B., Schnurbusch T., Hay A., Mayo G., Pallotta M., Tester M., Langridge P., 2007. Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318, 1446-1449. http://dx.doi.org/10.1126/science.1146853 PMid:18048688
Takano J., Noguchi K., Yasumori M., Kobayashi M., Gajdos Z., Miwa K., Hayashi H., Yoneyama T., Fujiwara T., 2002. Arabidopsis boron transporter for xylem loading. Nature 420, 337-340. http://dx.doi.org/10.1038/nature01139 PMid:12447444
Takata K., Matsuzaki T., Tajika Y., 2004. Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 39, 1-83. http://dx.doi.org/10.1016/j.proghi.2004.03.001 PMid:15242101
Tester M., Davenport R., 2003. Na+ tolerance and Na+ transport in higher plants. Ann Bot 91, 503-527. http://dx.doi.org/10.1093/aob/mcg058
Vandeleur R.K., Mayo G., Shelden M.C., Gilliham M., Kaiser B.N., Tyerman S.D., 2009. The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149, 445-460. http://dx.doi.org/10.1104/pp.108.128645 PMid:18987216 PMCid:2613730
Voicu M.C., Zwiazek J.J., 2004. Cycloheximide inhibits root water flow and stomatal conductance in aspen (Populus tremuloides) seedlings. Plant Cell Environ 27, 199-208. http://dx.doi.org/10.1111/j.1365-3040.2003.01135.x
Wan X., Zwiazek J.J., 1999. Mercuric chloride effects on root water transport in Aspen seedlings. Plant Physiol 121, 939-946. http://dx.doi.org/10.1104/pp.121.3.939 PMid:10557243 PMCid:59458
Weimberg R., 1987. Modification of foliar solute concentrations by calcium in two species of wheat stressed with sodium chloride and/or potassium chloride. Physiol Plantarum 73, 418-425. http://dx.doi.org/10.1111/j.1399-3054.1988.tb00620.x
Wimmer M.A., Muhling K.H., Lauchli A., Brown P.H., Goldbach H.E., 2003. The interaction between salinity and B toxicity affects the subcellular distribution of ions and proteins in wheat leaves. Plant Cell Environ 26, 1267-1274. http://dx.doi.org/10.1046/j.0016-8025.2003.01051.x
Yang X.H., Wen X.G., Gong H.M., Lu Q.T., Yang Z.P., Tang Y.L., Liang Z., Lu C.M., 2007. Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225, 719-733. http://dx.doi.org/10.1007/s00425-006-0380-3 PMid:16953431
Yermiyahu U., Ben-Gal A., Sarig P., Zipilevitch E., 2007. Boron toxicity in grapevine (Vitis vinifera L.) in conjunction with salinity and rootstock effects. J Hortic Sci Biotech 82, 547-554.
Yermiyahu U., Ben-Gal A., Keren R., Reid R.J., 2008. Combined effect of salinity and excess boron on plant growth and yield. Plant Soil 304, 73-87. http://dx.doi.org/10.1007/s11104-007-9522-z
Yu Q., Hu Y., Li J., Wu Q., Lin Z., 2005. Sense and antisense expression of plasma membrane aquaporin BnPIP1 from Brassica napus in tobacco and its effects on plant drought resistance. Plant Sci 169, 647-656. http://dx.doi.org/10.1016/j.plantsci.2005.04.013
Zhang W.H., Tyerman S.D., 1999. Inhibition of water channels by HgCl2 in intact wheat root cells. Plant Physiol 120, 849-858. http://dx.doi.org/10.1104/pp.120.3.849 PMid:10398721 PMCid:59324
Zhao C.X., Shao H.B., Chu L.Y., 2008. Aquaporin structure-function relationships: water flow through plant living cells. Colloids Surfaces B 62, 163-172. http://dx.doi.org/10.1016/j.colsurfb.2007.10.015 PMid:18063350
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