Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants

Abstract

Following exposure to salinity, the root/shoot ratio is increased (an important adaptive response) due to the rapid inhibition of shoot growth (which limits plant productivity) while root growth is maintained. Both processes may be regulated by changes in plant hormone concentrations. Tomato plants (Solanum lycopersicum L. cv Moneymaker) were cultivated hydroponically for 3 weeks under high salinity (100 mM NaCl) and five major plant hormones (abscisic acid, ABA; the cytokinins zeatin, Z, and zeatin-riboside, ZR; the auxin indole-3-acetic acid, IAA; and the ethylene precursor 1-aminocyclopropane-1-carboxylic acid, ACC) were determined weekly in roots, xylem sap, and leaves. Salinity reduced shoot biomass by 50-60% and photosynthetic area by 20-25% both by decreasing leaf expansion and delaying leaf appearance, while root growth was less affected, thus increasing the root/shoot ratio. ABA and ACC concentrations 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 affected in roots and shoots. Salinity dramatically decreased the Z+ZR content of the plant, and induced the conversion of ZR into Z, especially in the roots, which accounted for the relative increase of cytokinins in the roots compared to the leaf. IAA concentration was also strongly decreased in the leaves while it accumulated in the roots. Decreased cytokinin content and its transport from the root to the shoot were probably induced by the basipetal transport of auxin from the shoot to the root. The auxin/cytokinin ratio in the leaves and roots may explain both the salinity-induced decrease in shoot vigour (leaf growth and leaf number) and the shift in biomass allocation to the roots, in agreement with changes in the activity of the sink-related enzyme cell wall invertase.

Fig. 1.

Shoot (A) and root (B) biomass and root/shoot ratio (C) in tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence (black bars) or presence of 100 mM NaCl (grey bars). Data are means of six plants ±SE. Asterisks indicate significant differences between treatments according to Student–Newman–Keuls test at P <0.05.

Fig. 2.

Leaf number (A), leaf 4 biomass (B), and leaf 4 area (C) in tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence (closed circles) or presence of 100 mM NaCl (open circles). Data are means of six plants. Asterisks: see Fig. 1.

Fig. 3.

Cytokinin (Z, ZR, and Z+ZR) concentrations and Z/ZR ratio in leaf 4 (A, D, G, J), xylem sap (B, E, H, K), and roots (C, F, I, L) of tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence (closed circles) or presence of 100 mM NaCl (open circles). Data are means of three plants ±SE. Asterisks: see Fig. 1. (Leaf data are replotted from Ghanem et al., 2008.)

Fig. 4.

IAA concentration and IAA/(Z+ZR) ratio of leaf 4 (A, C) and root (B, D) of tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence (closed circles) or presence of 100 mM NaCl (open circles). Data are means of three plants ±SE. Asterisks: see Fig. 1. (Leaf data are replotted from Ghanem et al., 2008.)

Fig. 5.

ABA and ACC concentrations of leaf 4 (A, D), xylem sap (B, E), and roots (C, F)) of tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence (closed circles) or presence of 100 mM NaCl (open circles). Data are means of three plants ±SE. Asterisks: see Fig. 1. (Leaf data are replotted from Ghanem et al., 2008.)

Fig. 6.

Cell wall invertase activity (CWIN)of leaf 4 and roots of tomato plants (cv. Moneymaker) grown for three weeks on half-strength Hoagland's medium in the absence (black bars) or presence of 100 mM NaCl (grey bars). Data are means of three plants ±SE. Asterisks: see Fig. 1.

Fig. 7.

Leaf 4/root hormone concentration ratios for zeatin (A), ZR (B), Z+ZR (C), IAA (D), ABA (E), and ACC (F) in tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence (closed circles) or presence of 100 mM NaCl (open circles). Data are ratios of mean hormonal concentrations of three plants.

Fig. 8.

Linear correlations between leaf RGR or RER and the IAA concentrations (A) or the IAA/(Z+ZR) ratio (B) in leaf 4, and between the RGR of the root and the ratio for CK (Z+ZR) contents in the roots compared to the leaf 4 (C) of tomato plants (cv. Moneymaker) grown for 3 weeks on half-strength Hoagland's medium in the absence or presence of 100 mM NaCl.

Fig. 9.

Changes in hormonal concentrations in leaves, xylem sap, and roots in relation to local (shoot, leaf, and root growth) and co-ordinated processes (biomass partitioning) in tomato plants cultivated under salinity (100 mM NaCl) for 3 weeks. The relative increase (arrow up) or decrease (arrow down) in hormone concentration induced by salinity at the end of the experiment is indicated by both arrow and font sizes where the largest, intermediate, and smallest sizes indicate a more than 5-fold, a 2–5 fold, or a less than 2-fold change in hormone concentration.