Hormonal and metabolic regulation of tomato fruit sink activity and yield under salinity

Abstract

Salinization of water and soil has a negative impact on tomato (Solanum lycopersicum L.) productivity by reducing growth of sink organs and by inducing senescence in source leaves. It has been hypothesized that yield stability implies the maintenance or increase of sink activity in the reproductive structures, thus contributing to the transport of assimilates from the source leaves through changes in sucrolytic enzymes and their regulation by phytohormones. In this study, classical and functional physiological approaches have been integrated to study the influence of metabolic and hormonal factors on tomato fruit sink activity, growth, and yield: (i) exogenous hormones were applied to plants, and (ii) transgenic plants overexpressing the cell wall invertase (cwInv) gene CIN1 in the fruits and de novo cytokinin (CK) biosynthesis gene IPT in the roots were constructed. Although salinity reduces fruit growth, sink activity, and trans-zeatin (tZ) concentrations, it increases the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) during the actively growing period (25 days after anthesis). Indeed, exogenous application of the CK analogue kinetin to salinized actively growing fruits recovered sucrolytic activities (mainly cwInv and sucrose synthase), sink strength, and fruit weight, whereas the ethylene-releasing compound ethephon had a negative effect in equivalent non-stressed fruits. Fruit yield was increased by both the constitutive expression of CIN1 in the fruits (up to 4-fold) or IPT in the root (up to 30%), owing to an increase in the fruit number (lower flower abortion) and in fruit weight. This is possibly related to a recovery of sink activity in reproductive tissues due to both (i) increase in sucrolytic activities (cwInv, sucrose synthase, and vacuolar and cytoplasmic invertases) and tZ concentration, and (ii) a decrease in the ACC levels and the activity of the invertase inhibitor. This study provides new functional evidences about the role of metabolic and hormonal inter-regulation of local sink processes in controlling tomato fruit sink activity, growth, and yield under salinity.

Keywords: Cell wall invertase; cytokinins; fruit; salinity; sink activity; tomato..

Fig. 1.

Linear correlations between fruit sink strength (A, measured as the amount of radioactivity accumulated in Bq) or fruit sink activity (B, expressed as logarithm of the amount of radioactivity accumulated in Bq per gram of fresh weight), and the fruit fresh weight of tomato plants (cv. Durinta F1) cultivated for 40 d in the absence (closed circles) or presence (open circles) of 100mM NaCl.

Fig. 2.

Final fruit fresh weight (A) and equatorial diameter (B) of tomato fruit (cv. Durinta F1) sprayed with different hormones and cultivated in the presence of 75mM NaCl. Sucrolytic activities in percentage relate to the water-treated fruits (C) and cell wall invertase activity (D) of actively growing tomato fruits (25 DAA) sprayed with different hormones and cultivated in the presence of 75mM NaCl. Data are means of 6 plants±SE. Values marked with a same letter are not significantly different at P<0.05 according to the Student–Newman–Keuls test. OP = original population.

Fig. 3.

Trans-Zeatin (tZ) and 1-aminocyclopropane-1-carboxylic acid (ACC) concentrations (A) in actively growing fruits (25 DDA) of tomato plants cultivated for 40 d in the absence (light-grey bars) or presence (dark-grey bars) of 100mM NaCl. Data are means of 6 plants±SE. Values marked with a same letter are not significantly different at P<0.05 according to the Student-Newman-Keuls test. Linear correlations between fruit sink strength (B, measured as the amount of radioactivity accumulated in Bq) or fruit sink activity (C, expressed as logarithm of the amount of radioactivity accumulated in Bq per gram of fresh weight), and the fruit fresh weight of non-salinized (sprayed with ethephon) and salinized (100mM NaCl, treated with kinetin) tomato fruits (cv. Durinta F1).

Fig. 4.

Fruit yield (A), fruit fresh weight (B), and number of fruits (C) of wild-type tomato plants (cv. P-73) and a segregating T₂ tomato population containing the InvLp6g::CIN1 construct and cultivated under moderate salinity (75mM NaCl). Fruit yield (D), fruit fresh weight (E), and number of fruits (F) of wild-type tomato plants (cv. P-73) and the selected CIN1-93 line theInvLp6g::CIN1 construct and cultivated under control conditions. Linear correlations (G) between fruit number (open circles) or weight (closed circles) and fruit yield. Black bars indicate selected lines. Data are presented as means±SE.

Fig. 5.

CIN1 expression in the fruit (A), fruit fresh weight (bars) and fruit yield (line) (B), flower abortion index (bars) and fruit number (line) (C), and linear correlations between fruit sink activity (logarithmic scale) and fruit fresh weight (D) of wild-type tomato plants (cv. P-73) and two selected homozygous lines expressing the InvLp6g::CIN1 construct and cultivated under moderate salinity (75mM NaCl). Data are means of 3 plants±SE. Values marked with a same letter are not significantly different at P<0.05 according to the Student–Newman–Keuls test.

Fig. 6.

Cell wall invertase (A), vacuolar invertase (B), cytoplasmic invertase (C), and sucrose synthase (D) activities, hexose (glucose + fructose) concentrations (E), and invertase inhibitor activity (F) in tomato fruits of wild-type tomato plants (cv. P-73) and two selected homozygous lines expressing the InvLp6g::CIN1 construct and cultivated under moderate salinity (75mM NaCl). Data are means of 3 plants±SE. Values marked with a same letter are not significantly different at P<0.05 according to the Student–Newman–Keuls test.

Fig. 7.

Trans-Zeatin (A), 1-aminocyclopropane-1-carboxylic (B), indoleacetic acid (C), and abscisic acid (D) concentrations in tomato fruits of wild-type tomato plants (cv. P-73) and two selected homozygous lines expressing the InvLp6g::CIN1 construct and cultivated under moderate salinity (75mM NaCl). Data are means of 3 plants±SE. Values marked with a same letter are not significantly different at P<0.05 according to the Student–Newman–Keuls test.

Fig 8.

Yield-related (re-plotted from Ghanem et al. 2011), hormonal, and metabolic parameters in salinized (75mM NaCl) tomato plants (cv. P-73) grafted onto rootstocks overexpressing the 35::IPT construct (WT/IPT), denoted in percentage with respect to grafted tomato plants (cv. P-73) onto UC-82B rootstocks (WT/WT). Asterisks indicate statistical differences at P<0.05 according to the Student–Newman–Keuls test.