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

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.

The high fruit soluble sugar content in wild Lycopersicon species and their hybrids with cultivars depends on sucrose import during ripening rather than on sucrose metabolism.

Soluble sugar content has been studied in relation to sucrose metabolism in the hexose-accumulating cultivated tomato Lycopersicon esculentum Mill, the wild relative species Lycopersicon cheesmanii Riley, in the sucrose-accumulating wild relative species Lycopersicon chmielewskii Rick, Kesicky, Fobes & Holle. and in two hexose-accumulating interspecific F1 hybrids (L. esculentum × L. cheesmanii; L. esculentum × L. chmielewskii), cultivated under two irrigation regimes (control: EC = 2.1 and saline: EC = 8.4 dS m-1). Under control conditions the total soluble sugar content (as hexose equivalents) in the ripe fruits of L. cheesmanii was 3-fold higher than in L. esculentum, while L. chmielewskii and both F1 hybrids contained twice as much as the cultivar. With the exception of L. esculentum × L. cheesmanii, salinity increased the sugar content by 1.3 (wild species) and 1.7 times (cultivar and L. esculentum × L. chmielewskii) with respect to control fruits. Wild germplasm or salinity provided two different mechanisms for the increases in fruit sugar content. The hexoses accumulated in ripe fruits were strongly influenced by those accumulated at the start of ripening, but the hydrolysed starch before start of ripening only partially explained the final hexose levels and especially the increase under salinity. The early cell wall acid invertase and the late neutral invertase activities appeared to be related to the amount of hexoses accumulated in ripe fruits. However, no metabolic parameter was positively related to the amount of sugar accumulated (including sucrose). The major differences between genotypes appeared in ripe fruits, in which up to 50% of the total amount of sugars accumulated in the wild species (mainly in L. cheesmanii) and hybrids cannot be explained by the sugars accumulated and the starch hydrolysed before the start of ripening stage. As a consequence, the higher fruit quality of the wild species compared with L. esculentum may depend more on the continuation of sucrose import during ripening than on osmotic or metabolic particularities such as the hexose / sucrose-accumulator character or specific enzyme activities.

Sucrolytic activities during fruit development of Lycopersicon genotypes differing in tolerance to salinity.

The different growth responses under control and moderate salinity (70 mM NaCl) in relation to the carbon partitioning and sucrose metabolism in developing tomato fruits [20 days after anthesis (DAA), start of ripening and ripe stages] were studied in the cultivated tomato Lycopersicon esculentum Mill (cv. H-324-1), in the wild relative species L. cheesmanii (ac. LA-530) (hexose-accumulators), L. chmielewskii (ac. LA-1028) (sucrose-accumulator) and in two interspecific F1 hybrids (hexose-accumulators) (F1-530: H-324-1 x A-530, F1-1028: H-324-1 x A-1028). The higher salt-tolerance of the wild species and hybrids with respect to the domestic tomatoes was also observed at the fruit level because these genotypes were less affected in the assimilation of dry weight (DW) under salinity. With the exception of the wild tomatoes, the sink strength, evaluated as the dry matter accumulation rate (mg DW day-1) and the sink activity, evaluated as a relative growth rate (mg DW mg-1 day-1), were reduced during the early fruit growing period (20 DAA-start ripening). However, a total recovery of growth was registered in the salinized hybrid fruits during the late growing period (start of ripening-ripe fruits). The early reduction in sink activity in the hybrid and domestic fruits was related to a sucrose accumulation and a decrease in the total sucrolytic activity at 20 DAA, especially the cytoplasmic sucrolytic activities sucrose synthase (EC 2.4.1.13) and neutral invertase (EC 3.2.1.26). The further recovery in sink strength of the hybrid fruits was related to the maintenance of the insoluble acid invertase (EC 3.2.1.25) and the induction of the cytoplasmic sucrolytic activities, namely at the start of ripening stage, demonstrating the existence of an inverse relationship between these activities, which suggests a regulatory mechanism in order to maintain the sink capacity. The roles of different enzymes in the control of assimilate import under salinity in relation to the sucrose transport and possible regulatory mechanisms are discussed.