**1. Introduction**

Industrialization and urbanization have continuously accelerated climate change, as seen in the increase in air temperature to date [1,2]. The global average temperature is predicted to increase by approximately 0.3 ◦C in every decade, thereby rising by 1–4 ◦C from the year 2081 to 2100 compared to the temperature recorded from 1986 to 2005, according to the Intergovernmental Panel on Climatic Change (IPCC) [3,4]. An elevated temperature of approximately 3–4 ◦C may result in a drastic reduction in crop yields by a maximum of 35% in Asia, Africa, and the Middle East [5].

High temperature (HT) is closely associated with heat stress (HS), which is one of the major abiotic stresses, including temperature, drought, salinity, and flooding [5]. HS is a detrimental abiotic factor that influences global crop productivity by compromising crop growth during the vegetative and reproductive growth stages [5–7]. In general, HS is considered to be an elevation of temperature over a threshold level for a substantial amount of time, leading to irreversible impairments in crop growth and development [8].

**Citation:** Lee, K.; Rajametov, S.N.; Jeong, H.-B.; Cho, M.-C.; Lee, O.-J.; Kim, S.-G.; Yang, E.-Y.; Chae, W.-B. Comprehensive Understanding of Selecting Traits for Heat Tolerance during Vegetative and Reproductive Growth Stages in Tomato. *Agronomy* **2022**, *12*, 834. https://doi.org/ 10.3390/agronomy12040834

Academic Editors: Channapatna S. Prakash, Ali Raza, Xiling Zou and Daojie Wang

Received: 17 February 2022 Accepted: 26 March 2022 Published: 29 March 2022

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**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

A transiently elevated temperature of 10–15 ◦C above the optimum temperature for plant growth and development is termed as "heat" or "thermal" shock [8,9]. HS is a complex process with many factors, including the intensity and total duration of HT and the speed of the temperature increase [9,10]. For example, the frequency and period of HT can affect the occurrence and intensity of HS in a certain climatic zone during the day or night. In definition, HS tolerance is termed as the survival capability of a plant to grow, develop, and/or produce economic yields in response to HT [8,10].

Tomato (*Solanum lycopersicum*) plants, which belong to the *Solanaceae* family, are grown in a wide variety of climate conditions and areas from tropical to temperate regions. The tomato was introduced to Europe in the 16th century and then spread to the Mediterranean [11]. It is the second most important vegetable crop worldwide after the potato [12]. The cultivation area has reached almost 5,000,000 hectares and worldwide tomato yields amount to 181,000,000 metric tons (FAO, http://www.fao.org/faostat/ (accessed on 7 February 2022)). Tomatoes are consumed fresh and are also a major ingredient in a wide array of cuisines, as well as for sauces and juices [13]. In particular, the tomato fruit is a rich source of vitamins A and C and antioxidants, including lycopene, β-carotene, phenolics, and minerals but is low in calories [14–16], contributing to the maintenance of human health.

Climate change is likely to significantly reduce crop yield in the future [17–19], and a daily temperature that is a few degrees above the average can significantly affect vegetative and reproductive parameters, such as seedling growth, plant height (PH), leaf length and width, pollen grain viability, and the fertility of the female parts [20–22]. Its optimal average day and night temperatures range from 21 to 30 ◦C and from 18 to 21 ◦C, respectively [23]. Tomato production is frequently threatened by HS in diverse cultivated regions [24,25]. HT and drought stress are likely to have a negative impact on the growth, development, and yield of tomato plants in fields, leading to reduced production in its main producing regions from the year 2050 to 2100 [22].

The effect of HS on tomato plants has chiefly been evaluated during the reproductive stage owing to the importance of its fruits, as well as its sensitivity at the reproductive stage [26–28]. When the day temperature is above optimum, this induces developmental disorders in the flower organs (stamen and ovule) and in fruit development (fruit set, weight and quality, and seed number) [26–31]. In addition, a study has shown that the treatment of transient HS (>45 ◦C, 20 min) results in programmed cell death (PCD) in tomato fruits via DNA fragmentation and cytochrome c release, and induces caspase-like enzyme activity [32]. Vegetative growth parameters are likewise influenced under HS in many crops [8]. Non-photochemical quenching (NPQ), chlorophyll content, photosynthetic rate, transpiration rate, stomatal conductance, and CO2 assimilation are negatively affected by HS, resulting in a reduced growth rate [19,26,33,34].

The evaluated traits and factors in HS conditions are significantly varied among genotypes and growth stages in tomato plants, suggesting that the correlations among these traits and factors can vary during the vegetative and reproductive growth stages [35,36]. It is important to find the association in terms of HT tolerance between germination or seedling stages and flowering stages in tomato plants [37–39] for enhancing the speed of tomato breeding by the early selection of heat-tolerant genotypes as an indirect selection. However, substantial knowledge gaps exist in our understanding of the correlation between vegetative and reproductive growth-related traits or factors under HS.

The development of heat-tolerant tomato cultivars is crucial for adapting to elevated temperatures at present and in the future [5,20], but some bottlenecks and difficulties exist in identifying and applying the traits associated with heat tolerance in breeding programs. There has been a different understanding of the definition of plant responses to HT and a lack of in-depth understanding of the genetic basis and architecture regarding the heat tolerance mechanism during the vegetative and reproductive growth stages [1,20,40]. These problems have led to a deficiency of common screening methods and protocols on evaluating heat-tolerant traits, as well as in screening and selecting heat-tolerant genotypes

to date. Consequently, the identification of heat-tolerant genotypes seems not to be reproducible and reliable to some degree [41]. In this review, we provide an overview of the knowledge of the response of tomato plants to HT, which includes diverse HS regimes, as well as trait associations and key factors related to heat tolerance during the vegetative and reproductive growth stages. Lastly, we examine some promising traits associated with heat tolerance in tomato plants, with a discussion of recent correlation studies using a large number of genotypes.

#### **2. Types of Heat Stress Regimes in Tomato Plants**

The concept of HS is projected to assess temperature intensity and duration and the speed of increments in temperatures [8]. The application of proper HS treatment is a key point when screening heat-tolerant plants. Yeh et al. [42] and Mesihovic et al. [41] reported four major HS regimes for screening the heat-tolerant germplasm in *Arabidopsis* and crop species, suggesting that directly applied HS (DAHS) should be applied for basal thermo-tolerance, pre-induced HS for acquired thermo-tolerance (ATT), gradient HS for ATT, and mild chronic HS (MCHS) for mild heat thermo-tolerance (MHTT) for ATT in greenhouse and open-field conditions [41]. Two HS regimes, DAHS and MCHS, are mainly utilized in screening for and studying the heat tolerance of tomato plants in response to HT at physiological and molecular levels. In general, DAHS is applied for a short period of screening (from an hour to a day) with a high temperature of ≥45 ◦C during the vegetative and/or reproductive stages [41,43]. MCHS is used for a longer period of screening with mild high temperatures of 30–36 ◦C, ranging from several days to the entirety of the plant growth and developmental cycle [41,44]. The MCHS regime has been more widely applied than the DAHS regime to tomato plants for screening heat tolerance in terms of the reproductive parameters, including pollen germination and viability with flower and fruit characteristics in both greenhouses and open fields [20]. This is because the MCHS regime more closely resembles natural field conditions and/or it is difficult to maintain the DAHS regime in field conditions. Tomato plants exhibit different physiological responses to DAHS and MCHS [29]. The effects of HS on tomato cultivars vary significantly, depending on growth stages and experimental environment conditions including the temperature range, light intensity and quality, relative humidity and others; sometimes, different definitions of the same traits have caused variation in HS effects [41]. Therefore, it is indispensable to establish common screening methods and protocols to identify heat-tolerant tomato genotypes by considering the aforementioned climate conditions in a certain target area and/or expanded geological location.
