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Response of three broccoli cultivars to salt stress, in relation to water status and expression of two leaf aquaporins

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Abstract

The aim of this study was to compare differences in water relations in the leaves of three broccoli cultivars and differential induction of the expression of PIP2 aquaporin isoforms under salt stress. Although broccoli is known to be moderately tolerant to salinity, scarce information exists about the involvement of leaf aquaporins in its adaptation to salinity. Thus, leaf water relations, leaf cell hydraulic conductivity (Lpc), gas exchange parameters and the PIP2 expression pattern were determined for short- (15 h) and long- (15 days) term NaCl treatments. In the long term, the lower half-time of water exchange in the cells of cv. Naxos, compared with Parthenon and Chronos, and its increased PIP2 abundance may have contributed to its Lpc maintenance. This unmodified Lpc in cv. Naxos under prolonged salinity may have diluted NaCl in the leaves, as suggested by lower Na+ concentrations in the leaf sap. By contrast, the increase in the half-time of water exchange and the lower PIP2 abundance in cvs. Chronos and Parthenon would have contributed to the reduced Lpc values. In cv. Parthenon, there were no differences between the ε values of control and salt-stressed plants; in consequence, cell turgor was enhanced. Also, the increases in BoPIP2;2 and BoPIP2;3 expression in cv. Chronos for the short-term NaCl treatment suggest that these isoforms are involved in osmotic regulation as downstream factors in this cultivar, in fact, in the short-term, Chronos had a significantly reduced osmotic potential and higher PIP2 isoforms expression.

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Abbreviations

G s :

Stomatal conductance

IgG:

Immunoglobulin G

PIP:

Plasma membrane intrinsic protein

QRT-PCR:

Quantitative real-time PCR

T :

Transpiration rate

Ψw :

Water potential

Ψ π :

Osmotic potential

Ψ t :

Turgor potential

References

  • Ashraf M (2004) Photosynthetic capacity and ion accumulation in a medicinal plant henbane (Hyoscyamus niger L.) under salt stress. J Appl Bot Food Qual 78:91–96

    CAS  Google Scholar 

  • Bayuelo-Jiménez JS, Debouck DG, Lynch JP (2003) Growth, gas exchange, water relations, and ion composition of Phaseolus species grown under saline conditions. Field Crops Res 80:207–222

    Article  Google Scholar 

  • Benlloch-Gonzalez M, Fournier JM, Benlloch M (2010) K+ deprivation induces xylem water and K+ transport in sunflower: evidence for a co-ordinated control. J Exp Bot 61:157–164

    Article  PubMed  CAS  Google Scholar 

  • Boursiac Y, Chen S, Luu DT, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805

    Article  PubMed  CAS  Google Scholar 

  • Cabañero FJ, Carvajal M (2007) Different cation stresses affect specifically osmotic root hydraulic conductance, involving aquaporins, ATPase and xylem loading of ions in Capsicum annuum L. plants. J Plant Physiol 164:1300–1310

    Article  PubMed  Google Scholar 

  • Cabañero FJ, Martínez V, Carvajal M (2004) Does calcium determine water uptake under saline conditions in pepper plants, or is it water flux which determines calcium uptake? Plant Sci 166:443–450

    Article  Google Scholar 

  • Casado-Vela J, Muries B, Carvajal M, Iloro I, Elortza F, Martínez-Ballesta MC (2010) Analysis of root plasma membrane aquaporins from Brassica oleracea: post-translational modifications, de novo sequencing and detection of isoforms by high resolution mass spectrometry. J Proteome Res 9:3479–3494

    Article  PubMed  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporins activity. Plant Physiol 122:1025–1034

    Article  PubMed  CAS  Google Scholar 

  • Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 143:122–133

    Article  PubMed  CAS  Google Scholar 

  • Denna DW (1970) Transpiration and the waxy bloom of Brassica oleracea L. Aust J Biol Sci 23:27–30

    Google Scholar 

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ, Hajiba Gheri MA, Yeo AR (1991) Ion accumulation in the cell-walls of rice plants growing under saline conditions—evidence for the Oertli hypothesis. Plant Cell Environ 14:319–325

    Article  Google Scholar 

  • Forrest KL, Bhave M (2008) The PIP and TIP aquaporins in wheat form a large and diverse family with unique gene structures and functionally important features. Funct Integr Genomic 8:115–133

    Article  CAS  Google Scholar 

  • Frangne N, Maeshima M, Schaffner AR, Mandel T, Martinoia E, Bonnemain JL (2001) Expression and distribution of a vacuolar aquaporin in young and mature leaf tissues of Brassica napus in relation to water fluxes. Planta 212:270–278

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Zelazny E, Chaumont F (2006) Modulating the expression of aquaporin genes in planta: a key to understand their physiological functions? Biochim Biophys Acta 1758:1142–1156

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Heinen RB, Draye X, Chaumont F (2008) The expression pattern of plasma membrane aquaporins in maize leaf highlights their role in hydraulic regulation. Plant Mol Biol 68:337–353

    Article  PubMed  CAS  Google Scholar 

  • Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985

    Article  PubMed  CAS  Google Scholar 

  • Hill AE, Shachar-Hill B, Shachar-Hill Y (2004) What are aquaporins for? J Membr Biol 197:1–32

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DT, Arnon DI (1938) The water culture method for growing plants without soil. Calif Agr Expt Sta Circ 347:1–39

    CAS  Google Scholar 

  • Karlsson M, Johansson I, Bush M, McCann MC, Maurel C, Larsson C, Kjellbom P (2000) An abundant TIP expressed in mature highly vacuolated cells. Plant J 21:83–90

    Article  PubMed  CAS  Google Scholar 

  • Katsuhara M, Shibasaka M (2007) Barley root hydraulic conductivity and aquaporins expression in relation to salt tolerance. Soil Sci Plant Nutr 53:466–470

    Article  CAS  Google Scholar 

  • Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San Diego

    Google Scholar 

  • Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  PubMed  CAS  Google Scholar 

  • Ktitorova IN, Skobeleva OV (1999) Changes in elastic properties of cell walls and some parameters of plant water relations in response to acidification of the medium. Russ J Plant Physiol 46:201–206

    CAS  Google Scholar 

  • Li GW, Zhang MH, Cai WM, Sun WN, Su WA (2008) Characterization of OsPIP2;7, a water channel protein in rice. Plant Cell Physiol 49:1851–1858

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCt method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • López-Berenguer C, García-Viguera C, Carvajal M (2006) Are root hydraulic conductivity responses to salinity controlled by aquaporins in broccoli plants? Plant Soil 279:13–23

    Article  Google Scholar 

  • López-Berenguer C, Martinez-Ballesta MC, García-Viguera C, Carvajal M (2008) Leaf water balance mediated by aquaporins under salt stress and associated glucosinolate synthesis in broccoli. Plant Sci 174:321–328

    Article  Google Scholar 

  • López-Pérez L, Fernández-García N, Olmos E, Carvajal M (2007) The Phi thickening in roots of broccoli plants: an acclimation mechanism to salinity? Int J Plant Sci 168:1141–1149

    Article  Google Scholar 

  • López-Pérez L, Martínez-Ballesta MC, Maurel C, Carvaja M (2009) Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry 70:492–500

    Article  PubMed  Google Scholar 

  • Maathuis FJM, Filatov V, Herzyk P, Krijger GC, Axelsen KB, Chen S, Green BJ, Li Y, Madagan KL, Sánchez-Fernández R, Forde BG, Palmgren MG, Rea PA, Williams LE, Sanders D, Amtmann A (2003) Transcriptome analysis of root transporters reveals participation of multiple gene families in the response to cation stress. Plant J 35:675–692

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Ballesta MC, Aparicio F, Pallás V, Martínez V, Carvajal M (2003) Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. J Plant Physiol 160:689–697

    Article  PubMed  Google Scholar 

  • Martínez-Ballesta MC, 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

    Article  Google Scholar 

  • Montalvo-Hernandez L, Piedra-Ibarra E, Gomez-Silva L, Lira-Carmona R, Acosta-Gallegos JA, Vazquez-Medrano J, Xoconostle-Cázares B, Ruíz-Medrano R (2008) Differential accumulation of mRNAs in drought-tolerant and susceptible common bean cultivars in response to water deficit. New Phytol 177:102–113

    PubMed  CAS  Google Scholar 

  • Munns R (1993) Physiological processes limiting plant-growth in saline soils—some dogmas and hypotheses. Plant Cell Environ 16:15–24

    Article  CAS  Google Scholar 

  • Muries B, Mohamed F, Carvajal M, Martínez-Ballesta MC (2011) Differential aquaporin expression induced by salinity in broccoli plants. Mol BioSyst 7:1322–1335

    Article  PubMed  CAS  Google Scholar 

  • Murphy R, Smith JAC (1994) A critical comparison of the pressure-probe and pressure-chamber techniques for estimating leaf-cell turgor pressure in Kalanchoë daigremontiana. Plant Cell Environ 17:15–29

    Article  Google Scholar 

  • Nobel PS (1991) Physicochemical and environmental plant physiology. Academic Press, San Diego

    Google Scholar 

  • Ohshima Y, Iwasaki I, Suga S, Murakami M, Inoue K, Maeshima M (2001) Low aquaporin content and low osmotic water permeability of the plasma and vacuolar membranes of a CAM plant Graptopetalum paraguayense: comparison with radish. Plant Cell Physiol 42:1119–1129

    Article  PubMed  CAS  Google Scholar 

  • Otto B, Kaldenhoff R (2000) Cell-specific expression of the mercury insensitive plasma-membrane aquaporin NtAQP1 from Nicotiana tabacum. Planta 211:167–172

    Article  PubMed  CAS  Google Scholar 

  • Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schäffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152:1418–1430

    Article  PubMed  CAS  Google Scholar 

  • Qi CH, Chen M, Song J, Wang BS (2009) Increase in aquaporin activity is involved in leaf succulence of the euhalophyte Suaeda salsa, under salinity. Plant Sci 176:200–205

    Article  CAS  Google Scholar 

  • Sack L, Holbrook M (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    Article  PubMed  CAS  Google Scholar 

  • Sakurai J, Ahamed A, Murai M, Maeshima M, Uemura M (2008) Tissue and cell-specific localization of rice aquaporins and their water transport activities. Plant Cell Physiol 49:30–39

    Article  PubMed  CAS  Google Scholar 

  • Samdur MY, Manivel P, Jain VK, Chikani BM, Gor HK, Desai S, Misra JB (2003) Genotypic differences and water-deficit induced enhancement in epicuticular wax load in peanut. Crop Sci 43:1294–1299

    Article  Google Scholar 

  • Steudle E (1993) Pressure probe techniques: basic principles and application to studies of water and solute relations at the cell tissue and organ level. In: Smith JAC, Griffith H (eds) Water deficits: Plant responses from cell to community. Bios Scientific, Oxford, pp 5–35

    Google Scholar 

  • Steudle E, Tyerman SD (1983) Determination of permeability coefficients. Reflection coefficients and hydraulic conductivity of Chara corallina using pressure probe: effects of solute concentrations. J Membr Biol 75:85–96

    Article  CAS  Google Scholar 

  • Steudle E, Smith JAC, Lüttge U (1980) Water relations parameters of individual mesophyll cells of the CAM plant Kalanchoë daigremontiana. Plant Physiol 66:1155–1163

    Article  PubMed  CAS  Google Scholar 

  • Steudle E, Zimmermann U, Zillikens J (1982) Effect of cell turgor on hydraulic conductivity and elastic-modulus of Elodea leaf cells. Planta 154:371–380

    Article  Google Scholar 

  • Suga S, Imagawa S, Maeshima M (2001) Specificity of the accumulation of mRNAs and proteins of the plasma membrane and tonoplast aquaporins in radish organs. Planta 212:294–304

    Article  PubMed  CAS  Google Scholar 

  • Suga S, Komatsu S, Maeshima M (2002) Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. Plant Cell Physiol 43:1229–1237

    Article  PubMed  CAS  Google Scholar 

  • Torrecillas A, Guillaume C, Alarcon JJ, Ruiz-Sánchez MC (1995) Water relations of 2 tomato species under water-stress and recovery. Plant Sci 105:169–176

    Article  CAS  Google Scholar 

  • Turner NC (1988) Measurement of plant water status by the pressure chamber technique. Irrig Sci USA 9:289–308

    Article  Google Scholar 

  • Tyree MT, Zimmermann M (2002) Xylem structure and the ascent of sap, 2nd edn. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Article  PubMed  CAS  Google Scholar 

  • Ye Q, Holbrook NM, Zwieniecki MA (2008) Cell-to-cell pathway dominates xylem-epidermis hydraulic connection in Tradescantia fluminensis (Vell. Conc.) leaves. Planta 227:1311–1319

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank the Sakata Company for the gift of the seeds. They also thank Dr. David Walker for corrections of the written English in the manuscript. This work was supported by the Spanish Ministerio de Ciencia e Innovación, CICYT [AGL2009-12720]. M. C. Martínez-Ballesta thanks the Spanish Ministerio de Ciencia e Innovación for funding through the “Ramón y Cajal” programme [Ref RYC-2009-04574].

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Authors and Affiliations

  1. Dpto. Nutrición Vegetal, Centro de Edafología y Biología Aplicada del Segura (CEBAS-CSIC), Campus de Espinardo, 30100, Murcia, Spain

    Beatriz Muries, Micaela Carvajal & María del Carmen Martínez-Ballesta

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  1. Beatriz Muries
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  2. Micaela Carvajal
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  3. María del Carmen Martínez-Ballesta
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Correspondence to María del Carmen Martínez-Ballesta.

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Muries, B., Carvajal, M. & Martínez-Ballesta, M.d.C. Response of three broccoli cultivars to salt stress, in relation to water status and expression of two leaf aquaporins. Planta 237, 1297–1310 (2013). https://doi.org/10.1007/s00425-013-1849-5

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