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Hormonal Changes in Relation to Biomass Partitioning and Shoot Growth Impairment in Salinized Tomato (Solanum Lycopersicum L.) Plants

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Hormonal Changes in Relation to Biomass Partitioning and Shoot Growth Impairment in Salinized Tomato (Solanum Lycopersicum L.) Plants Journal of Experimental Botany, Vol. 59, No. 15, pp. 4119–4131, 2008 doi:10.1093/jxb/ern251 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) RESEARCH PAPER Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants Alfonso Albacete1,*, Michel Edmond Ghanem2,*, Cristina Martı´nez-Andu´ jar1,†, Manuel Acosta3, Jose´ Sa´nchez-Bravo3, Vicente Martı´nez1, Stanley Lutts2, Ian C. Dodd4 and Francisco Pe´rez-Alfocea1,‡ 1 Departamento de Nutricio´n Vegetal, Centro de Edafologı´a y Biologı´a Aplicada del Segura (CEBAS), Consejo Superior de Investigaciones Cientı´ficas (CSIC), Campus Universitario de Espinardo, E-30100, Espinardo, Murcia, Spain 2 Groupe de Recherche en Physiologie Ve´ge´tale, Universite´ catholique de Louvain (UCL), Croix du Sud 5, boıˆte 13, B-1348 Louvain-la-Neuve, Belgium 3 Departamento de Biologı´a Vegetal-Fisiologı´a Vegetal, Facultad de Biologı´a, Universidad de Murcia, Campus Universitario de Espinardo, E-30100, Espinardo, Murcia, Spain 4 The Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK Received 19 June 2008; Revised 11 September 2008; Accepted 15 September 2008 Abstract fected in roots and shoots. Salinity dramatically de- creased the Z+ZR content of the plant, and induced the Following exposure to salinity, the root/shoot ratio is conversion of ZR into Z, especially in the roots, which increased (an important adaptive response) due to the accounted for the relative increase of cytokinins in the rapid inhibition of shoot growth (which limits plant roots compared to the leaf. IAA concentration was also productivity) while root growth is maintained. Both strongly decreased in the leaves while it accumulated processes may be regulated by changes in plant in the roots. Decreased cytokinin content and its hormone concentrations. Tomato plants (Solanum transport from the root to the shoot were probably lycopersicum L. cv Moneymaker) were cultivated induced by the basipetal transport of auxin from the hydroponically for 3 weeks under high salinity (100 mM shoot to the root. The auxin/cytokinin ratio in the NaCl) and five major plant hormones (abscisic acid, leaves and roots may explain both the salinity-induced ABA; the cytokinins zeatin, Z, and zeatin-riboside, ZR; decrease in shoot vigour (leaf growth and leaf number) the auxin indole-3-acetic acid, IAA; and the ethylene and the shift in biomass allocation to the roots, in precursor 1-aminocyclopropane-1-carboxylic acid, agreement with changes in the activity of the sink- ACC) were determined weekly in roots, xylem sap, and related enzyme cell wall invertase. leaves. Salinity reduced shoot biomass by 50–60% and photosynthetic area by 20–25% both by decreasing Key words: Abscisic acid, 1-aminocyclopropane-1-carboxylic leaf expansion and delaying leaf appearance, while acid, indole-3-acetic acid, plant hormones, salt stress, sodium root growth was less affected, thus increasing the chloride, tomato (Solanum lycopersicum L.), zeatin, zeatin- root/shoot ratio. ABA and ACC concentrations riboside. strongly increased in roots, xylem sap, and leaves after 1 d (ABA) and 15 d (ACC) of salinization. By contrast, cytokinins and IAA were differentially af- * AA and MEG contributed equally to this work. y Present address: Department of Horticulture-Seed Biology, Oregon State University, OR 97331, Corvallis, USA. z To whom correspondence should be addressed: E-mail: [email protected] Abbreviations: ABA, abscisic acid; ACC, 1-aminocyclopropane-1-carboxylic acid; CK, cytokinin; CWIN, cell wall invertase; IAA, indole-3-acetic acid; RGR, relative growth rate; RER, relative expansion rate; Z, zeatin; ZR, zeatin riboside. ª 2008 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from http://jxb.oxfordjournals.org at Lancaster University on 10 December 2009 4120 Albacete et al. Introduction concentrations, thus controlling assimilate partitioning between different sink tissues (Hartig and Beck, 2006). Salinity is a major factor reducing crop productivity in These hormonal changes not only influence the agriculture as well as a major cause of the abandonment adaptive response but also affect the normal growth of of lands and aquifers for agricultural purposes. Improving the harvestable organs and thus influence economic the use of such marginal resources requires insight about productivity. Hence, plant hormones are considered their limiting effects on plant development. The release of a primary component of the signalling pathways control- salt-tolerant crops to optimize the use of salt-contaminated ling these processes. water and soil resources has been a much prosecuted This integrated plasticity in plant development probably scientific goal but with little success to date, as few major involves long-distance communication between different determinant genetic traits of salt tolerance have been organs with hormones playing an essential role (Sachs, identified (Flowers, 2004; Munns, 2005). Although main- 2005) or differential changes in root and shoot hormone tenance of ionic and water homeostasis is necessary for concentrations. Although salinity increased plant ABA plant survival, salinity decreases crop productivity both by concentration in all plant compartments (Wolf et al., reducing leaf growth and inducing leaf senescence. This 1990; Kefu et al., 1991), its role in growth regulation has lowers the total photosynthetic capacity of the plant, thus been equivocal as different studies have suggested it can limiting its ability to generate further growth or harvest- inhibit (Dodd and Davies, 1996) or maintain growth by able biomass and also to maintain defence mechanisms restricting the evolution of ethylene, another potential against the stress (Yeo, 2007). growth inhibitor (Sharp and LeNoble, 2002). Both The major physiological processes believed to be cytokinins and auxins act as endogenous mitogens whose involved in the control of plant growth under salinity concentrations can be environmentally modulated to have been water relations, hormonal balance, and carbon regulate the formation of roots and shoots and their supply, with their respective importance depending on the relative growth (Werner et al., 2001; Sachs, 2005). It has time scale of the response (Munns, 2002). Salinity affects been hypothesized that a decrease in CK supply from the plant growth in two phases (Munns, 1993). During the root to the shoot could inhibit leaf growth while a low CK initial phase of salinity, the osmotic effect predominates content would promote root growth and thus the root/ and induces water stress due to the high salt concentration shoot ratio (van der Werf and Nagel, 1996; Rahayu et al., in the root medium. During this phase, shoot growth arrest 2005). It has been reported that salinity decreased the occurs very quickly (seconds to minutes) but recovers auxin indoleacetic acid (IAA) levels in the roots but not in (over several hours) to a new steady-state that is the leaves of tomato plants (Dunlap and Binzel, 1996), considerably lower than under non-stress conditions. while leaf zeatin concentration declined under osmotic These changes seem to be driven by changes in water stress in tomato (Walker and Dumbroff, 1981). However, relations (Munns, 2002), but during this initial period since many of these (relatively scarce) studies were only when osmotic effects predominate (days to weeks), able to measure one or two of the major hormone groups growth seems to be regulated by hormones and/or following a step-change in salinity or any other stress, carbohydrates. During the second phase of the stress interpretation of changes in biomass allocation by specific (weeks to months), growth is governed by toxic effects authors has generally favoured the hormones that each due to the high salt accumulation in leaf tissues. author measured, and thus there are several divergent Overall, salinity affects plant productivity by reducing hypotheses of the regulation of biomass allocation (van the photosynthetic area by inhibiting cell division and cell der Werf and Nagel, 1996; Munns and Cramer, 1996; expansion rates during leaf growth and by affecting Sachs, 2005) that co-exist in the literature. developmental programmes regulating leaf emergence, The advent of multi-analyte techniques for hormone the production of lateral primordia, and the formation of quantification allows a far more comprehensive analysis reproductive organs (Munns, 2002). However, the mech- of the changes in plant hormone status following salinity. anism(s) that down-regulates leaf growth and shoot Accordingly, the endogenous concentrations of five major development under the osmotic phase of salinity is not plant hormones; ABA, ACC, IAA, and two major active known. It has been hypothesized that leaf growth in- cytokinins (Davey and van Staden, 1976) in tomato, Z and hibition must be regulated by hormones or their precur- ZR, were analysed in leaves of a cultivated tomato sors, because the reduced leaf growth rate is independent genotype submitted to salinity stress (100 mM NaCl for 3 of carbohydrate supply, water status, nutrient deficiency, weeks), in order to study the
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