The effects of the combination of salinity and excess boron on the water relations of tolerant tomato (Solanum lycopersicum L.) cv. Poncho Negro, in relation to aquaporin functionality

  1. Contreras, C.
  2. Montoya Matute, Ana
  3. Pacheco Cartagena, Patricia
  4. Martínez Ballesta, María Carmen
  5. Carvajal, M.
  6. Bastías, Elizabeth
Revista:
Spanish journal of agricultural research

ISSN: 1695-971X,  2171-9292

Ano de publicación: 2011

Volume: 9

Número: 2

Páxinas: 494-503

Tipo: Artigo

DOI: 10.5424/SJAR/20110902-168-10 DIALNET GOOGLE SCHOLAR lock_openDialnet editor

Outras publicacións en: Spanish journal of agricultural research

Repositorio institucional: lock_openAcceso aberto Editor

Obxectivos de Desenvolvemento Sustentable

Resumo

As elevated levels of boron (B) are accompanied by conditions of excessive salinity with drastic consequences for crops, it is crucial to find a crop that is tolerant to these conditions. In this work, the interaction between salinity and excess B with respect to aquaporin-mediated changes by blockade of mercury and water relations were studied as well as the osmotic adjustment of the plants. The treatments, for tomato �Poncho Negro� cultivated hydroponically in a controlled environment chamber, were control (75 and 150 mM) NaCl and/or 5 mg L�1 or 20 mg L�1 B. Hydraulic conductance (L0) of detached exuding root systems exhibits large variations in response to abiotic stimuli. No additive (synergic) effects of B and salinity were observed. Under salinity, the plants increased their turgor, compensating for the decrease in the leaf water potential through the reduction in the leaf osmotic potential by the accumulation of soluble sugars and proline. The involvement of Hg2+-insensitive aquaporins or the osmotic gradient as the main force for water flow through the apoplastic pathway must be contemplated. Finally, all the data reveal the tomato cv. Poncho Negro to be a germplasm of agronomic interest and a good alternative for cultivation areas with high content of salts and the excess B of the soil and irrigation water.

Referencias bibliográficas

  • 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
Fonte de datos: Dialnet