The effects of drought, waterlogging and heat stress on tomatoes (Solanum lycopersicon L.)

Abstract

Field production of tomatoes generally involves exposure to various sub optimal environmental conditions and environmental stress factors including high temperature, scarcity of water or excessive water. This study investigated morphological, physiological and biochemical responses to water stress (water deficit and waterlogging) of two tomato (Solanum lycopersicon L.) cultivars ('Best Boy Bush' and 'Scoresby Dwarf') at three developmental stages (vegetative, flowering and fruiting) in the glasshouse, and at the fruiting stage in a kinetic study in the field. These cultivars, together with the cultivar 'Soprano' were further investigated in a heat stress experiment (at 40/30 °C day/ night temperatures). Generally, growth parameters including leaf length and leaf area as well as plant biomass accumulation were reduced by the three stress factors. The reduction in growth-related traits was more pronounced at the earlier stages of plant development (i.e. the vegetative stage). The impact of heat stress was characterised by a significant increase in the number of abscised flowers (5.4 fold) and of flowers with stigma tube elongation (3.5 fold), as well as the prevention of fruit set. Trials to examine physiological responses to water stress showed reductions in plant water status (leaf relative water content and leaf water potential) and leaf gas exchange (photosynthesis, stomatal conductance and transpiration). Osmotic adjustment was observed under water deficit by virtue of a reduction in adjusted osmotic potential and an increase in proline production. For instance, adjusted osmotic potential decreased by 29%, and proline levels increased by 48% in the leaves and by 65% in the roots in plants subjected to drought stress in the glasshouse study. A reduction of osmotic potential (-91%) and an accummulation of free proline (from Day 2 to Day 8) were also observed in drought treated plants in the field trial. In contrast, free proline levels decreased under waterlogging. Tomato plants responded to both water stress treatments with the accumulation of hydrogen peroxides, which resulted in oxidative stress. High levels of H₂O₂ were observed in leaves and roots of water-stressed plants in the glasshouse and field trials. However, the H₂O₂ levels in the roots of plants subjected to waterlogging were slightly lower in the glasshouse trial. As a consequence of the elevated oxidative load (H₂O₂ production), there was greater damage to lipids, proteins and DNA in water-stressed plants. The activities of enzymatic antioxidants were all increased under drought stress but were inactivated in plants at the reproductive developmental stage under waterlogging conditions in the glasshouse trial. As a result, activities of superoxide dismutase, catalase, ascorbate peroxidase, glutathione reductase and glutathione peroxidase all increased under drought stress, but decreased under waterlogging following the accumulation of H₂O₂ and the occurrence of oxidative stress. In the field experiment, the activities of these enzymatic antioxidants increased two days after exposure to water stress and continued to rise as the period of water stress increased. In contrast, enzyme activity reached a plateau five days after the start of waterlogging. The production of non-enzymatic antioxidants such as ascorbate and glutathione increased in tissues of plants subjected to water deficit under both growing conditions. Levels of these antioxidants were either slightly increased or significantly decreased in plants subjected to waterlogging in both growing conditions (glasshouse and field). Waterlogging induced hypoxia in plants as measured by increasing ADH activity in the roots of waterlogged plants. ADH levels began rising from Day 2 and continued to rise with duration of the waterlogging period. The activities of glyoxalase enzymes increased in parallel with an accumulation of methylglyoxal in both leaf and root tissues. Ascorbic acid levels and total antioxidant capacity both increased in tomato fruits sampled from drought stressed plants. However, these antioxidants decreased in tomato fruits harvested from plants subjected to waterlogging. Total carotenoid content was reduced in the pericarp of 'Best Boy Bush' fruits grown under water deficit and waterlogging, but not in the pericarp of 'Scoresby Dwarf' fruits. The biological activity of these water stressed tomato fruits was assessed using an in vitro gastrointestinal digestion coupled with Caco-2 cell cultures. Caco-2 cell viability under oxidative stress was improved when the cells were pre-treated with digested tomato fruit grown under water stress. There were significant cultivar differences in many stress responses under glasshouse conditions, with lower levels of oxidative damage and increased protective responses of the antioxidant apparatus in ‘Scoresby Dwarf’ under water stress. There were also indications of heat stress tolerance in the cultivar ‘Scoresby Dwarf’, which had lower numbers of abscised flowers and lower incidence of flowers with elongated stigma tubes in response to high temperature stress, compared to ‘Best Boy Bush’. Taken together, this study provides a guide for the identification of stress tolerant genotypes and improves the understanding of the importance of biochemical changes in plants experiencing oxidative stress. The findings can be used for the selection and development of stress tolerant tomato cultivars, and suggest merit for the application of targeted drought treatments to boost the production of antioxidant phytochemicals in tomato fruits that are of benefit for human health.