Climate change is causing temperature increment in crop production areas worldwide, generating conditions of heat stress that negatively affect crop productivity. Tomato (Solanum lycopersicum), a major vegetable crop, is highly susceptible to conditions of heat stress. When tomato plants are exposed to ambient day/night temperatures that exceed 32°C/20°C respectively during the reproductive phase, fruit set and fruit weight are reduced, leading to a significant decrease in yield. Processing tomato cultivars are cultivated in open fields, where environmental conditions are not controlled, therefore plants are exposed to multiple abiotic stresses, including heat stress. Nonetheless, information on stress response in processing tomatoes is very limited. Understanding the physiological response of modern processing tomato cultivars to heat stress may facilitate the development of thermotolerant cultivars. Here, we compared two tomato processing cultivars, H4107 and H9780, that we found to be constantly differing in yield performance. Using field and temperature-controlled greenhouse experiments, we show that the observed difference in yield is attributed to the occurrence of heat stress conditions. In addition, fruit-set and seed production were significantly higher in the thermotolerant cultivar H4107, compared with H9780. Despite the general acceptance of pollen viability as a measure of thermotolerance, there was no difference in the percentage of viable pollen between H4107 and H9780 under either of the conditions tested. In addition to observations of similar pollen germination and bud abscission rates, our results suggest that processing tomato cultivars may present a particular case, in which pollen performance is not determining reproductive thermotolerance. Our results also demonstrate the value of combining controlled and uncontrolled experimental settings, in order to validate and identify heat stress related responses, thus facilitating the development of thermotolerant processing tomato cultivars.
Experimental design scheme. The experimental flow is described, indicating main results. In yellow: parameters in which H4107 was higher than H9780. In orange: parameters in which no significant difference was found between H4107 and H9780. FS, fruit set. SN, seeds number per fruit. PV, pollen viability. Y, yield.
Consistent difference in yield between H4107 and H9780 across years and locations. (A) Average yield of H4107 and H9780 in years and locations testing both cultivars. The test average obtained by yield measurements of multiple cultivars is presented as well. (B) Average yield of H4107 and H9780 across years and locations presented in A. *, statistically significant difference (P-value < 0.05).
Fruit set and seed number measurements in the field experiments during 2018. (A) Fruit set of H4107 and H9780 in Upper Galilee (left) and Volcani (right) fields. (B) Seeds number per fruit for H4107 and H9780 in Upper Galilee (left) and Volcani (right) fields. *, statistically significant difference (P-value < 0.05).
Controlled experiment conditions and reproductive measurements. (A) Temperatures measured every five minutes in both control (blue) and MCHS (brown) greenhouses. Black arrows denote day of flowering and day of stress initiation. Threshold temperatures for heat stress conditions in tomato are marked by dotted lines. (B) Fruit set for H4107 ad H9780 under control (white bars) and MCHS (grey bars) conditions. (C) Seeds number per fruit in H4107 and H9780 under control (white bars) and MCHS (grey bars) conditions. MCHS, moderate chronic heat stress. *, statistically significant difference (P-value < 0.05). ns, not significant.
Pollen viability and germination under heat stress conditions. Percentage of viable pollen from post-anthesis flowers of H4107 and H9780 at the (A) Upper Galilee field, (B) Volcani field and (C) controlled greenhouses, under control (white bars) and MCHS (grey bars) conditions. (D) Pollen germination rate in the controlled experiment. MCHS, moderate chronic heat stress. ns, not significant.
Current literature on processing tomatoes in general and on their response to heat stress in particular is very limited. Here, we identified a consistent difference in yield between two processing cultivars: H4107 and H9780, across multiple years and locations. This difference is manifested by higher fruit set and total fruit weight of H4107. Both H4107 and H9780 were bred and adapted for humid and arid environments by the Heinz company, but heat stress tolerance was not addressed so far. We aim to understand the source of this difference in order to promote breeding for high yield in field-grown processing tomatoes. Since the field environment imposes various stresses to the plants, and tomato being particularly sensitive to elevated temperatures, we set to test the possibility that high temperature conditions are causing the observed difference in yield. We found that H4107 is more heat stress tolerant than H9780, presenting better reproductive performance in terms of fruit set and seed production under high temperature conditions. Although relative humidity is known to affect fruit set and yield in tomato (Harel et al. 2014), this factor did not account for the difference between H4107 and H9780 as relative humidity levels were similar between control and MCHS conditions (Figure S2).
One of the earliest studies on heat stress response in tomato showed that bud abscission and style exertion were more pronounced in heat-susceptible cultivars, leading to low fruit set under heat stress (Levy et al. 1978). Later observations demonstrated that stigma exertion in different tomato genotypes ranges from 25 to 55% under high-temperature conditions (Saeed et al. 2007). More recently, bud abscission and style exertion were correlated with reduced fruit set under field conditions as well (Singh et al. 2015; Kugblenu et al. 2013). In processing tomato cultivars, however, the phenomena of style exertion is very rare, and we did not detect it in our experiments (by visual inspection). Bud abscission was monitored in the Upper Galilee and Volcani fields, but no difference was found between H4107 and H9780 (Figure S3).
Pollen viability is widely recognized as a main parameter determining plant heat stress tolerance (Dane et al. 1991; Paupière et al. 2017; Driedonks et al. 2018). Therefore, we tested whether the heat stress tolerance of H4107 can be at least partially explained by a higher degree of pollen viability under heat stress conditions. However, our results show that there is no difference in pollen viability between H4107 and H9780 either under stressful field conditions, or under chronic heat stress imposed artificially (Figure 5). Therefore, we conclude that the thermotolerance of H4107 is not caused by better pollen viability, nor pollen germination capabilities. We found only one publication reporting a similar observation (i.e., pollen viability not affecting fruit set and yield under heat stress) for several greenhouse tomato cultivars (Ayenan et al., 2021). Thus, our results suggest that while pollen viability is a valid trait demonstrating heat stress tolerance in various tomato genotypes, it may not apply to all cultivars, and special attention should be paid for processing tomato. Other factors may mediate the tolerance in this system, possibly related to female reproduction development and function and post-pollination interactions (Peet et al., 1997; Xu et al., 2017). These issues were not addressed in this study and will be a relevant direction in future studies.
Generally, in plant science research, field and greenhouse data are inconsistent, explained by the big difference in environmental conditions between the two experimental systems. In our case, fruit set was very similar between field (28-36% and 17% for H4107 and H9780, respectively) and controlled heat stress (36% and 19% for H4107 and H9780, respectively), supporting the occurrence of heat stress conditions in the field experiments. Importantly, these results confirm that the observed difference in yield and other reproductive traits under open field conditions are due to high temperatures. Thus, our results demonstrate consistency in regard to a complex trait (yield), suggesting that in our system, controlled greenhouse experiments are highly relevant for agricultural conditions, facilitating translating research from lab to practice. This approach is being recognized recently, with the emerging of publications testing the response to heat stress in tomato, importantly comparing greenhouse with field conditions (Bhattarai et al. 2021; Ro et al. 2021; Poudyal et al. 2019).
In order to address the challenge of maintaining crop productivity in areas of temperature increment, the development of thermo-tolerant cultivars is needed. To achieve that, a comprehensive understanding of the agronomical, physiological and molecular responses of crop plants to heat stress is vital (Berry and Bjorkman 1980; Brestic et al. 2018). In light of the research presented here, which demonstrates an unusual feature of specific cultivars, emphasis should be put on relevant cultivars that may offer different attributes in terms of response to the environment. Additionally, our results demonstrate the importance of temperature-controlled experimental systems in isolating specific heat-stress related phenomena.