H

OH
OH
metabolites

Review
Deleterious Effects of Heat Stress on the Tomato, Its Innate
Responses, and Potential Preventive Strategies in the Realm of
Emerging Technologies
Qaisar Khan , Yixi Wang, Gengshou Xia, Hui Yang, Zhengrong Luo and Yan Zhang *

Department of Landscape and Horticulture‚ Ecology College‚ Lishui University‚ Lishui 323000‚ China;
qaisar.khan@yahoo.com (Q.K.); yxwangls@163.com (Y.W.); lsxyxgs@163.com (G.X.); lsxyyh@126.com (H.Y.);
zrluo@126.com (Z.L.)
* Correspondence: yzhang@lsu.edu.cn; Tel.: +86-18867805285

Abstract: The tomato is a fruit vegetable rich in nutritional and medicinal value grown in greenhouses
and fields worldwide. It is severely sensitive to heat stress, which frequently occurs with rising
global warming. Predictions indicate a 0.2 ◦ C increase in average surface temperatures per decade
for the next three decades, which underlines the threat of austere heat stress in the future. Previous
studies have reported that heat stress adversely affects tomato growth, limits nutrient availability,
hammers photosynthesis, disrupts reproduction, denatures proteins, upsets signaling pathways,
and damages cell membranes. The overproduction of reactive oxygen species in response to heat
stress is toxic to tomato plants. The negative consequences of heat stress on the tomato have been
the focus of much investigation, resulting in the emergence of several therapeutic interventions.
However, a considerable distance remains to be covered to develop tomato varieties that are tolerant
to current heat stress and durable in the perspective of increasing global warming. This current
review provides a critical analysis of the heat stress consequences on the tomato in the context of
global warming, its innate response to heat stress, and the elucidation of domains characterized by
a scarcity of knowledge, along with potential avenues for enhancing sustainable tolerance against
heat stress through the involvement of diverse advanced technologies. The particular mechanism
Citation: Khan, Q.; Wang, Y.; Xia, G.;
underlying thermotolerance remains indeterminate and requires further elucidatory investigation.
Yang, H.; Luo, Z.; Zhang, Y.
The precise roles and interplay of signaling pathways in response to heat stress remain unresolved.
Deleterious Effects of Heat Stress on
The etiology of tomato plants’ physiological and molecular responses against heat stress remains
the Tomato, Its Innate Responses, and
unexplained. Utilizing modern functional genomics techniques, including transcriptomics, pro-
Potential Preventive Strategies in the
Realm of Emerging Technologies.
teomics, and metabolomics, can assist in identifying potential candidate proteins, metabolites, genes,
Metabolites 2024, 14, 283. https:// gene networks, and signaling pathways contributing to tomato stress tolerance. Improving tomato
doi.org/10.3390/metabo14050283 tolerance against heat stress urges a comprehensive and combined strategy including modern tech-
niques, the latest apparatuses, speedy breeding, physiology, and molecular markers to regulate their
Academic Editor: Marijana Zovko
physiological, molecular, and biochemical reactions.
Končić

Received: 9 April 2024 Keywords: heat stress; reactive oxygen species; heat shock proteins; stress signaling; genome editing;
Revised: 28 April 2024 omics; heat tolerance pyramiding; genetic resources
Accepted: 8 May 2024
Published: 15 May 2024

1. Introduction
Copyright: © 2024 by the authors.
The tomato, scientifically known as Solanum lycopersicum in the Solanaceae family, is
Licensee MDPI, Basel, Switzerland. cultivated in diverse environmental circumstances and geographical regions ranging from
This article is an open access article tropical to temperate environments. The tomato arrived in Europe during the Renaissance
distributed under the terms and and was scattered to the Mediterranean region [1]. The tomato is a fruit vegetable among
conditions of the Creative Commons the most cultivated crop plants on the earth and is grown in greenhouses and fields
Attribution (CC BY) license (https:// worldwide [2]. It is rich in medicinal and nutritional contents, including lycopene, the
creativecommons.org/licenses/by/ valuable compound having anti-oxidative and anti-cancer properties, vitamins A and C,
4.0/). β-carotene, iron, phosphorus, flavonoids, ferulic acid, hydroxycinnamic acid, chlorogenic

Metabolites 2024, 14, 283. https://doi.org/10.3390/metabo14050283 https://www.mdpi.com/journal/metabolites

Metabolites 2024, 14, 283 2 of 28

acid, homovanillic acid, folate, and low calories [3–6]. Around 80% of tomatoes are used
as processed food like ketchup, soup, paste, sauces, and juices [7,8]. Globally, China is the
biggest producer of tomatoes, followed by India and Turkey (FAO-2021) [9].
Earlier researchers have studied and discussed numerous facets of heat stress on
tomatoes, which include plant growth, leaf morphology, photosynthesis, and reproductive
performance, including fruit sets, root growth, ROC species, pollen viability, pollen num-
bers, and inflorescence numbers, focusing on individual aspects. In the context of global
warming, this current review provides a thorough critical analysis of heat stress on toma-
toes, covering all major aspects, including seed germination, growth, and development
and physiological, biochemical, genetic, and molecular reactions. Furthermore, it offers
comprehensive information about the available technologies and potential approaches for
creating imminent heat-tolerant cultivars. This present review provides complete insight
into all significant negative aspects of heat stress on tomatoes, their morphological, physio-
logical, biochemical, and molecular responses, analytical methodologies, and strategies for
developing heat-tolerant tomato cultivars.

2. Heat Stress
The undesirable influence of non-living dynamics and factors on living organisms
in a specified environment is termed abiotic stress [10]. Several abiotic stresses, such as
heat, flood, drought, and salt, reduce the production and yield of tomato crops by up
to 75%; particularity is subjected to the severity of stresses [11]. Generally, heat stress is
defined as an increase in temperature beyond tolerance for an unknown duration, adequate
to trigger irretrievable impairment in plant growth and development. In contrast, heat
tolerance is defined as a plant’s capability of growth and production to an economic yield
level under high temperatures [12,13]. In the context of tomato cultivation, heat stress
is commonly classified as moderate heat stress, ranging from 32 ◦ C to 37 ◦ C, and severe
heat stress, ranging from 38 ◦ C to 45 ◦ C [14]. Climate changes drastically affect tomato
crop production and yield, particularly in Asian countries [15]. It is a common opinion
that soaring temperatures will enhance the average temperature of the earth’s surface
by 0.2 ◦ C every ten years in the coming thirty years, increasing extreme weather and,
consequently, negatively affecting tomato plant growth and development and severely
reducing its production and yield [16,17].

3. Negative Effects of Heat Stress on Growth and Development

Tomato plants can typically grow and develop reproductive organs, pollen grains,
and fruit sets at an optimum temperature between 15 ◦ C and 32 ◦ C; however, tempera-
tures beyond 35 ◦ C badly stress sexual and asexual development [18,19]. Being sessile,
tomato plants often face erratic high-temperature conditions, which adversely influence
them as temperatures go beyond the optimal ranges. Studies have revealed that high
temperatures increase the frequencies of hot and dry days, affecting tomato plant growth,
biomass, phenology, agronomic traits, production, and yield [20,21]. High temperature
significantly disrupted physiological characteristics such as leaf water content, membrane
stability, canopy temperature drop, photosynthesis, stomatal conductance, chlorophyll
content, and fluorescence [22,23]. High heat stress negatively influences the metabolic
processes involved in growth and development [24]. It produces reactive oxygen species,
like hydrogen peroxide (H2 O2 ), superoxide, hydroxyl radical (OH), and singlet oxygen
1[O2], which adversely disturb cellular homeostasis [25–27].
In numerous crops, particularly tomatoes, reproductive growth is highly prone to heat
stress compared with vegetative growth [28]. Seeds are a significant part of plants, which
carry genetic information to descending generations [29]. However, higher temperatures se-
riously threaten seed germination, seedling physiology, and phenotypic expression [30,31].
Seed germination tested at a constant range of temperatures from 24 ◦ C to 37 ◦ C for 8 days
showed that the rate of seed germination started reducing after 28 ◦ C and entirely ceased
at 36 ◦ C. Cotyledon size reduced at a temperature higher than 24 ◦ C but the seedling’s
Metabolites 2024, 14, 283 3 of 28

hypocotyl length increased by 1.9 cm (24 ◦ C), 4.1 cm (28.5 ◦ C), and 2.6 cm (31.5 ◦ C), which
shows that temperatures higher than 28.5 ◦ C also affect hypocotyl length negatively. In the
same study, tomato seedlings aged 12 days (germination: 24 ◦ C) were exposed to 37 ◦ C
for 24 h, and a 1 h heat wave (45 ◦ C) damaged the seedling’s recovery ability. Exposure to
a 45 ◦ C heat wave for 1 h, 3 h, 6 h, and 12 h showed that the seedlings started drying at
6 h and lost recovery capability at 12 h. The number of lateral roots was reduced, but the
growth of the primary root was stopped at 37 ◦ C. Although 45 ◦ C did not affect lateral roots
significantly, it halted the growth of the primary root [32,33]. High temperature reduces
tomato root growth and nutrient uptake, affecting root–shoot source–sink relationships
that affect fruit yield and quality [28,34]. The 30-day-old seedlings of two tomato culti-
vars (Dafnis and Minichal) were subjected to heat stress of 40 ◦ C for 7 days in a growth
chamber, and the results indicated that the effects of high temperature on tomato leaves
started to appear on the second day. However, a big difference was noticed on the seventh
day. The damage to the leaves of the Dafnis cultivar was over 60%, but Minichal showed
resistance [35], which suggests that heat is a serious problem for tomato plants, and the
creation of heat-resistant varieties is very important to avoid economic losses.

4. Adverse Impacts of Heat Stress on Photosynthetic Parameters

Exposure of tomato plants to higher temperatures leads to significant disruption of
the chloroplast, which produces adenosine triphosphate (ATP) and phytochemicals. A
good performance of the photosynthetic apparatus under high-temperature stress shows
the ability of a plant to tolerate and adapt to stressful conditions [36,37]. However, HS
negatively affects several important components of photosynthesis (Figure 1). Heat stress
inhibits chlorophyll formation; hence, measuring chlorophyll (a, b) concentrations can
be a parametric indication for identifying heat-resistant plants. Under directly applied
high-temperature stress of 45 ◦ C (severe stress) for 2 h, a heat-resistant tomato cultivar
showed a decline in the ratio of chlorophyll (a:b) and an increase in the ratio of chlorophyll
to carotenoid in contrast to the control condition of 25/20 ◦ C (day/night). Heat-sensitive
cultivars, on the other hand, showed a decrease in the CO2 assimilation rate (A), the net
photosynthetic rate (Pn), and photosystem II efficiency (Fv/Fm), which represents the
highest quantum efficacy of photosystem II (PSII) and is used to assess chloroplasts’ normal
or superior functioning under heat stress conditions [38–42].
Photosynthesis in plants is a heat-sensitive physiological process that influences chloro-
phyll content, CO2 integration, D1 and D2 protein turnover, chloroplast components, and
heat-responsive protein deactivation [43]. Plant growth, development, production, yield,
and future food security are deeply connected with photosynthesis [44,45]. Persistent
higher heat stress inhibits photosynthetic activities, which affect the growth and production
of plants. Photosystems I and II (PSI, II), chlorophyll, the electron transport chain, and CO2
assimilation are among the significant photosynthesis process components, so damage to
any of them retard the photosynthetic mechanism [46]. A study by reference [47] revealed
that the production of protochlorophyllide (Pchlide), an intermediate in the biosynthetic
pathway of chlorophyll, was repressed by 70% at high temperature (42 ◦ C) compared with
a control (25 ◦ C), which reduced chlorophyll manufacture to 60% in cucumber seedlings.
Similarly, in the same study, the activities of the 5-aminolevulinic acid dehydratase (ALAD)
enzyme, which is responsible for converting 5-aminolevulinic acid (ALA) into porphobilino-
gen (PBG), an intermediate in chlorophyll biosynthesis, and porphobilinogen deaminase
(PBGD), which is necessary for converting PBG into urogen, were reduced by 45% and 28%
at a higher temperature compared with a control. The PSII electron transport system is
highly vulnerable to high temperature because it increases thylakoid membrane fluidity,
which knockouts the PSII light-garnering system from the thylakoid membrane and, conse-
quently, destroys PSII integrity [48,49]. High temperature severely disturbs tomato plants’
photosynthetic activities, specifically in susceptible tomato varieties [50].
Metabolites 2024, 14, x FOR PEER REVIEW 4 of 29

Metabolites 2024, 14, 283 severely disturbs tomato plants’ photosynthetic activities, specifically in susceptible
4 ofto-
28
mato varieties [50].

Figure 1. The negative impacts of heat stress on photosynthetic parameters.

Figure 1. The negative impacts of heat stress on photosynthetic parameters.
5. Heat Stress Represses Reproductive Performance
5. Heat Stress Represses Reproductive Performance
Cultivated tomatoes are autogamous plants, and high temperatures negatively im-
Cultivated
pact their tomatoes
pollination [51].are autogamous
Under high heatplants,
stress,and
the high
tomato temperatures
style, whichnegatively im-
is the female
pact their pollination [51]. Under high heat stress, the tomato style, which
reproductive part of the flower gynoecium holding the stigma, extends abnormally and is the female
reproductive
goes part of thecones,
out the antheridial flowerminimizing
gynoecium theholding
chancesthe of
stigma, extends
pollination abnormally
and, and
consequently,
goes out the
reducing fruitantheridial cones,
sets (Figure minimizing
2) [52–55]. Heatthe chances
stress of pollination
distorts pollen grain and, consequently,
development by
reducing the
reducing fruitamount
sets (Figure 2) [52–55]. Heat
of carbohydrates at thestress
earlydistorts
stages ofpollen grain development
development, reducing the by
reducing
sugar the amountinofmature
concentration carbohydrates
pollens, at theresulting
and early stages of development,
in slashed reducing
pollen viability the
[56,57].
sugar
The concentration
responses in mature and
of heat-resistant pollens, and resulting
susceptible genotypesin slashed pollen viability
of Lycopersicon esculentum[56,57].
Mill.
The responses of heat-resistant and susceptible genotypes of Lycopersicon esculentum
and L. pimpinellifolium Mill. to heat stress was evaluated by subjecting plants to optimal Mill.
and L. ◦pimpinellifolium
(27/23 C, day/night) and Mill.high-temperature
to heat stress was
(35/23 ◦ C) regimes
evaluated by subjecting plants toThe
in a greenhouse. optimal
heat
(27/23 °C,ratings
tolerance day/night) and
of the high-temperature
genotypes (35/23 °C)
were determined by regimes in athe
calculating greenhouse.
percentageThe heat
of fruit
that successfully developed under high and optimal temperatures. The fruit sets varied
from 41% to 84% in the temperature-sensitive genotypes and 45% to 91% in the heat-tolerant
genotypes at optimal temperatures. The genotypes with great heat sensitivity did not yield
 tolerance ratings of the genotypes were determined by calculating the percentage of fruit
that successfully developed under high and optimal temperatures. The fruit sets varied
from 41% to 84% in the temperature-sensitive genotypes and 45% to 91% in the heat-tol-
Metabolites 2024, 14, 283 5 of 28
erant genotypes at optimal temperatures. The genotypes with great heat sensitivity did
not yield any fruit. In contrast, the genotypes that could withstand high temperatures
produced fruit set rates ranging from 45% to 65% [58]. Stigma and stylar exsertion nega-
any fruit.
tively In fruit
affect contrast, the genotypes
set forming that could
capabilities becausewithstand high
of elevated temperatures
temperatures produced
[59]. It is es-
fruit setto
sential rates ranging
create from 45%tomato
heat-resistant to 65%varieties
[58]. Stigma
with and stylar
higher fruitexsertion negatively
sets as these varietiesaffect
will
fruit set forming capabilities because of elevated temperatures [59]. It is essential
benefit tomato crop yield in areas where the growing season’s average temperature is to create
heat-resistant
35 °C or higher. tomato varieties with higher fruit sets as these varieties will benefit tomato
crop yield in areas where the growing season’s average temperature is 35 ◦ C or higher.

Figure 2. Phenotypic changes in the tomato (cv. Saladette) flowers subjected to heat stress. (a,b) are
Figure 2. Phenotypic changes in the tomato (cv. Saladette) flowers subjected to heat stress. (a,b) are
young ◦ C). (c,d) are
youngflower
flowerbuds
budsand
andflowers at at
flowers thethe
blooming
bloomingstage under
stage normal
under temperatures
normal (26/19
temperatures (26/19 °C). (c,d)
flower budsbuds
and opened flowers under heat heat
stressstress
(36/26 ◦ C).°C).
are flower and opened flowers under (36/26

6. Negative Impacts of Heat Stress on Agronomic Traits

Agronomic traits refer to the characteristics of plants that exert influence on their
productivity, quality, and ability to cope with biotic and abiotic stressors. The adverse
effects of heat stress hinder the overall capacity of tomatoes to reach the desired agronomic
performance. Several investigations have been carried out to assess the negative impacts of
heat stress on different aspects of tomato leaves, such as fresh mass, the leaf area, the leaf
area ratio, the specific leaf area, and plant height and stem diameter under multiple heat
stress levels [60,61]. The total area of all leaves on a single plant is referred to as the leaf
Metabolites 2024, 14, 283 6 of 28

area (LA) [62]. The specific leaf area (SLA) is a crucial statistic for plant growth modelers as
it specifies the amount of fresh leaf area to allocate for each unit of biomass produced; it is
calculated by dividing the leaf area by the leaf mass (LA/LM) [63]. Heat stress negatively
affects plant leaves in several other ways, including reducing their capacity to retain water
and early leaf mortality [64,65]. Heat stress causes glucose reserve shortages because it
impedes starch accumulation, which results in a decrease in soluble sugar concentration
obtained from the decomposition of starch in fully developed pollen grains [66]. These
incidents can potentially decrease tomato pollen fertilization capacity [67]. An increase in
diurnal temperature over 25 ◦ C adversely impacted fruit quantity, weight, and seed count
per fruit markedly [68].

Heat Stress and Heat Shock Combined Effects

The tomato cultivars Kervic F1 (heat-resistant) and UC 82-B (heat-susceptible) at the
age of 35 days after heat shock at 50 ◦ C for 30 s were subjected to a heat stress of 35/27 ◦ C
(day/night) compared to control 26/20 ◦ C (day/night) conditions to study agronomic
traits including the leaf area (LA), leaf area ratio (LAR), specific leaf area (SLA), number of
pollen grains per flower (NPGF), number of fruits per plant (NFP), and fruit fresh mass
per plant (FFMP) [69]. Heat stress and heat shock negatively influenced the agronomic
traits of tomatoes, particularly the leaf area, pollen grains, fruit sets, and fruit weight
(Figure
Metabolites 2024, 14, x FOR PEER REVIEW 3). The heat stress repercussions mentioned herein hinder the overall capacity of
7 of 29
tomatoes to perform better agronomically. Therefore, it is crucial to extensively examine all
physiological and agronomic characteristics to address heat stress issues effectively.

Figure
Figure 3.3. Effects
Effects of
of heat
heat stress
stress and
and heat
heat shock
shock on
on the
the agronomic
agronomic parameters
parametersof
of resistant
resistant(Kervic
(KervicF1)
F1)
and
and sensitive (UC 82-B) tomato cultivars. (a) Heat-resistant cultivar (Kervic F1) under heat stressstress
sensitive (UC 82-B) tomato cultivars. (a) Heat-resistant cultivar (Kervic F1) under heat after
after heat shock stress. (b) Heat-resistant cultivar (Kervic F1) under heat stress without heat shock
heat shock stress. (b) Heat-resistant cultivar (Kervic F1) under heat stress without heat shock stress.
stress. (c) Heat-sensitive cultivar (UC 82-B) under heat stress after heat shock stress. (d) Heat-sensi-
(c) Heat-sensitive cultivar (UC 82-B) under heat stress after heat shock stress. (d) Heat-sensitive
tive cultivar (UC 82-B) under heat stress without heat shock stress. The X-axis indicates the types of
cultivar (UC
agronomic 82-B) under
parameters heat stressand
investigated, without heat shows
the Y-axis shock stress. The
values of X-axisin
changes indicates the parame-
agronomic types of
agronomic
ters parameters
under heat stress. investigated, and the Y-axis shows values of changes in agronomic parameters
under heat stress.
7. Over Production of Reactive Oxygen Species (ROS)
An equilibrium among numerous pathways in diverse cell compartments maintains
cellular homeostasis under an optimal temperature. The sustainability of homeostasis
cannot be guaranteed when temperatures go beyond the optimal level because various
pathways have diverse optimum temperatures within the cell, and heat stress upsets this
functional balance between different pathways [70]. ROS are over-produced in response
Metabolites 2024, 14, 283 7 of 28

7. Over Production of Reactive Oxygen Species (ROS)

An equilibrium among numerous pathways in diverse cell compartments maintains
cellular homeostasis under an optimal temperature. The sustainability of homeostasis
cannot be guaranteed when temperatures go beyond the optimal level because various
pathways have diverse optimum temperatures within the cell, and heat stress upsets this
functional balance between different pathways [70]. ROS are over-produced in response
to high-temperature stress and other harmful factors that affect several intracellular path-
ways [71,72]. ROS include free and non-free radicals that contain oxygen and are capable
of self-regulating survival with one or more unpaired electrons (Figure 4). Free-radical
ROS, like hydroxyl ion radical (OH•), superoxide anion radical (O2 •− ), and alkoxyl (RO• ),
carbonate (CO3 •− ), peroxyl (RO2 • ), hydroperoxyl (HO2 • ) molecular oxygen (O2 ), and non-
free radical species such as ozone (O3 ), hydrogen peroxide (H2 O2 ), singlet oxygen (1 O2 ),
hypobromous acid (HOBr), hydroperoxy (ROOH), hypoiodous acid (HOI), hypochlorous
acid (HOCl), are severely toxic to plant growth and development [73–76]. In response to
heat stress, ROS are generated in different cellular parts, like the plasma membrane, mito-
chondria,
Metabolites 2024, 14, x FOR PEER REVIEW cell wall, chloroplast, peroxisome, endoplasmic reticulum, and apoplast
8 of 29 [77,78].
Excessive production of ROS damages molecules and compounds in plant cells like lipids,
deoxyribonucleic acid (DNA), ribonucleic acid (RNA), proteins, and carbohydrates [79–81].

Figure
Figure 4. A4.display
A display showing various
showing various types
typesof of
reactive oxygen
reactive species
oxygen functioning
species in tomatoinplants.
functioning tomato plants.

8. Heat Stress Causes Oxidative Stress

Tomato plants are sensitive to high temperatures, even a little beyond optimal, which
causes the overproduction of reactive oxygen species (ROS) [82]. An equivalence between
ROS production and antioxidants is essential for the proper growth and development of
plants [83], but high temperatures are known to disrupt this equivalence in tomato plants.
Metabolites 2024, 14, 283 8 of 28

8. Heat Stress Causes Oxidative Stress

Tomato plants are sensitive to high temperatures, even a little beyond optimal, which
causes the overproduction of reactive oxygen species (ROS) [82]. An equivalence between
ROS production and antioxidants is essential for the proper growth and development
of plants [83], but high temperatures are known to disrupt this equivalence in tomato
plants. The tomato variety “Tmknvf2 ” was subjected to oxidative metabolism analysis at an
optimal temperature of 25 ◦ C and a high temperature of 35 ◦ C by reference [84], focusing
Metabolites 2024, 14, x FOR PEER REVIEW 9 of 29

on superoxide dismutase (SOD), ascorbate peroxidase (APX), dehydroascorbate peroxidase

(DHAR), guaiacol peroxidase (GPX), catalase (CAT), ascorbate (AsA), glutathione reductase
(GR), hydrogen
ally, the peroxide
activities (H2 OAPX,
of the CAT, 2 ), dehydroascorbate
DHAR, GR, and(DHA), glutathione
GPX enzymes are (GSH),
enhanced oxidized
in re-
glutathione
sponse (GSSG),
to higher total ascorbate,
temperatures total
[85,86]; glutathione,
however, and of
in the case dryreference
weight (DW). Generally,
[84], their activi-
the activities
ties of thebecause
were reduced CAT, APX, highDHAR, GR, anddenatured
temperatures GPX enzymestheseare enhanced
proteins. Theinconcentra-
response
to higher temperatures [85,86]; however, in the case of reference [84],
tions of GSH, GSSG, DHA, AsA, total ascorbate, and glutathione antioxidant compounds their activities were
reduced because high temperatures denatured these proteins. The concentrations
were higher at 35 °C than at 25 °C. These substrates are utilized by CAT, APX, DHAR, GR, of GSH,
GSSG,
and DHA,
GPX AsA,
in the total ascorbate, and glutathione
ascorbate–glutathione antioxidant
cycle, but their compounds
activities were reduced wereby higher
higherat
◦
35 C than at 25 ◦ C. These substrates are utilized by CAT,
temperatures (35 °C), resulting in a higher accumulation of APX, DHAR, GR,
these substrates and GPX
(Figure in
5) and
the ascorbate–glutathione cycle, but their activities were reduced by
increased hydrogen peroxide (H2O2) accumulation in tomato leaves. Overproduction of higher temperatures
(35 ◦
ROSC), resulting
seriously in a higher
impairs accumulation
plant growth, of these substrates
development, (Figure
and yield [87]. 5) and increased
Therefore, hy-
it is impera-
drogen peroxide (H 2 O 2 ) accumulation in tomato leaves. Overproduction
tive to investigate oxidative metabolism in tomato plants thoroughly and develop heat- of ROS seriously
impairs plant
tolerant growth, development, and yield [87]. Therefore, it is imperative to investigate
varieties.
oxidative metabolism in tomato plants thoroughly and develop heat-tolerant varieties.

Figure 5. The activities of enzymes and substrates in tomato plants under heat stress. Measurement
units, SOD:
SOD: unit
unitmgmgprotein −−1
protein min−−11,, H
1 min H22O mmolgg−1−1(FW),
O22: :mmol (FW),W.D: plant−1−,1 GPX,
W.D:gg plant , GPX,CAT,
CAT,APX,
APX, AsA,
AsA,
DHAR, DHA, GR, GSH, total ascorbate, and total glutathione: µmol µmol mg-prot− −11min−1−
min .. 1

9. Phenological
9. Phenological Modifications
Modifications in in Response
Response to to Heat
Heat Stress
Stress
Plant heat
Plant heat resistance
resistance refers
refers to
to the
the ability
ability of
of plants
plants to
to thrive
thrive and
and produce
produce the
the required
required
yield under high temperatures, which is specifically linked to the plant species
yield under high temperatures, which is specifically linked to the plant species or poten- or poten-
tially to the distinct organs and tissues within the same plant. Plant reactions to heat
tially to the distinct organs and tissues within the same plant. Plant reactions to heat stress stress
depend on the threshold degree, exposure period, and plant nature. The effects of heat
depend on the threshold degree, exposure period, and plant nature. The effects of heat
stress on
stress on aa plant’s
plant’s many
many functioning
functioning processes, such as
processes, such as seed
seed germination, development,
germination, development,
growth, procreation, and yield, are toxic [88,89]. Under conditions of severely high tem-
perature, serious damage to cells, even complete breakdown of cellular structures, and
cell demise might occur rapidly [90]. In response to high temperatures, plants implement
several short-term acclimation mechanisms and long-term evolutionary strategies for per-
Metabolites 2024, 14, 283 9 of 28

growth, procreation, and yield, are toxic [88,89]. Under conditions of severely high tem-
perature, serious damage to cells, even complete breakdown of cellular structures, and
cell demise might occur rapidly [90]. In response to high temperatures, plants implement
several short-term acclimation mechanisms and long-term evolutionary strategies for per-
sistence (Figure 6) [91]. Among these stratagems are stomatal closure, leaf position changes,
variations in the lipid configuration of the membrane, larger xylem, reduced water loss,
fast
Metabolites 2024, 14, x FOR PEER maturation, increased transpiration, decreased absorption of radiation,10an
REVIEW of increase
29 in
the number of hairs on the surface, cuticle layer thickening, adoption of paraheliotropism,
an increase in wax, late embryogenesis abundant proteins, transcriptional regulation, more
regulation,
vigorous more vigorous
antioxidant defense,antioxidant
signaling defense, signaling
cascades cascades stimulation,
stimulation, osmopro-
osmoprotectant, and pheno-
tectant, and phenological, morphological, biochemical, anatomical, molecular,
logical, morphological, biochemical, anatomical, molecular, and genetic adaptations and ge- [92,93].
netic adaptations [92,93]. Numerous heat-inducible genes, often referred to as heat shock
Numerous heat-inducible genes, often referred to as heat shock genes (HSGs), exhibit
genes (HSGs), exhibit upregulation in response to thermal stress. These genes encode
upregulation
HSPs, whichin are
response
essentialtoforthermal
plants tostress.
surviveThese genes encode
in life-threatening heatHSPs, whichHeat
stress [94,95]. are essential
for plants to survive
shock proteins in life-threatening
(HSPs) heatonly
are biologically active stress [94,95].
during Heat
certain shock
plant proteins
development and(HSPs) are
biologically active
growth stages, only during
including certain plant
seed germination, development
embryo and growth
microsporogenesis, and fruitstages,
ripeningincluding
seed[96,97].
germination, embryo microsporogenesis, and fruit ripening [96,97].

Figure
Figure 6. Various
6. Various long-and
long- andshort-term
short-term phenological
phenologicalchanges adopted
changes by tomato
adopted plants inplants
by tomato response
in response
to heat stress.
to heat stress.
Under elevated temperatures, tomato plants manifest symptoms including stunted
growth, aberrant development, poor photosynthesis, reduced crop output, and even plant
Metabolites 2024, 14, 283 10 of 28

Under elevated temperatures, tomato plants manifest symptoms including stunted

growth, aberrant development, poor photosynthesis, reduced crop output, and even plant
mortality [98]. However, it is essential to note that not all genotypes of tomatoes are suscep-
tible to high temperatures [99]. Some studies found that growing tomatoes between 21 ◦ C
and 26 ◦ C decreased the entire carotene concentration but did not affect lycopene quantity.
In contrast, cultivating tomatoes within the temperature range of 27 to 32 ◦ C reduced
ascorbate and lycopene levels while concurrently enhancing the levels of routine caffeic
acid derivatives and glucosides [100]. Moreover, tomato fruit firmness and better shelf life
were found in F1 hybrids, having mutant genes such as alcobaca (alc), ripening inhibitor
(rin), and non-ripening (nor). These hybrids can maintain, to a greater extent, tomato hue,
feel, taste, and nutritional value even when exposed to high-heat-stress conditions [101].
High temperatures during fruit development negatively affect assimilation, distribution,
and shelf storage. The fruit produces several structural and functional elements throughout
the ripening process, including starch and secondary metabolites that affect the interior
quality of fruits [102]. The sucrose that fruit receives from the leaves as photosynthesized
sugars adds to the fruit’s dry matter. A tomato’s flavor results from transforming carbs
like sucrose into organic acids and aromatic compounds [103]. Environmental parameters,
such as temperature, water irradiation, and photosynthesis, affect fruit quality [104]. These
problems, because of heat stress, draw our attention to exploring, selecting, and utilizing
cultivars of tomatoes capable of enduring high temperatures during the cultivation period.
Therefore, it is critical to understand the molecular and genetic mechanisms regulating
plants’ short- and long-term natural defense strategies in response to heat stress, which
could be applied to regulate the heat stress problem in crops, particularly in heat-sensitive
plants like tomatoes.

10. Heat Shock Signaling Pathway Modulation

In the face of heat stress, plants have several free and dependent pathways to perceive
external and internal signals, which significantly regulate the development of responses to
create resistance to cope with the situation [105]. These responses entail the overexpres-
sion of several genes and the activation of complex integrated circuits involving various
pathways. Cofactors and signaling molecules such as mitogen-activated protein kinase
(MAPK/MPKs), sugar compounds, and Ca-dependent protein kinases (CDPKs) play a
fundamental role in activating stress-responsive genes [106,107]. However, an intrinsic
study must fully elucidate and understand the signaling molecules and pathways involved
in developing heat tolerance.

11. Heat Shock Protein (HSP) Production

Heat stress often triggers the activation of heat-inducible genes known as heat shock
genes (HSGs), which produce heat shock proteins (HSPs) that are essential for a plant’s exis-
tence under very high temperatures [108]. HSPs act as chaperones to safeguard intracellular
proteins from decomposition and maintain their integrity and functionality by facilitating
protein folding [109]. Previously, scientists thought heat stress was the main trigger for
HSP formation. However, they have since learned that many biotic and abiotic stimuli
could cause HSP formation. They show up- or downregulation responses to biotic and
abiotic stress situations, but further research is needed to understand signal recognition and
transmission processes fully [6]. Additionally, a plant can overcome these obstacles with the
help of post-transcriptional modifications, including alternative splicing and micro RNA
(miRNA). Alternative splicing creates many transcripts from a single gene, while miRNA
binds to mRNA to inhibit translation or induce mRNA cleavage at any location [110,111].
In plants, heat shock proteins can be divided into five categories, including small HSP20
(sHSP20), HSP60 (GroE), HSP70 (DnaK), HSP90, and (HSP100). Among these HSPs, HSP60
and HSP70 are incredibly conserved, suggesting their crucial function in the heat stress
response [112]. HSP20s is a low-molecular-mass (15 to 42 kDa) family with a 90-amino
acid alfa-crystallin domain (ACD) that forms a seven-stranded β-sandwich flanked by a
Metabolites 2024, 14, 283 11 of 28

variable N-terminal domain (NTD) with fewer to 85 amino acids and a short C-terminal
extension (CTE) and is predominantly induced by heat stress in several higher plants [113].
Plants sense heat stress principally at the plasma membrane, leading to the opening
of particular calcium channels, permitting calcium ions to enter the cell, and triggering
the activation of mitogen-activated and calcium-dependent protein kinases, which in turn
activate the heat stress response (HSR) [114–116]. At the time of the HSR, numerous specific
genes are upregulated essentially, leading to the accumulation of a significant amount of
HSPs in different cellular compartments, which play a crucial role in signaling and heat
resistance mechanisms during the HSR; HSPs are commonly regulated by heat shock
factors (HSFs) [117,118]. Various pathways transmit heat signals to HSFs, activating HSPs
and heat-responsive genes (HRGs) and playing a significant role in plant heat adaption
mechanisms, which suggests that the HSF-HSP pathway is critical in governing plant
responses to heat stress [119].

12. Heat Shock Factor (HSF) Activation

Heat shock factors (HSFs) are activators that trigger the transcription of heat shock
genes and bind to heat shock sequence elements (HSEs) found throughout the genome,
which consist of a tandem array of three oppositely orientated “AGAAN” motifs or a
variant of them that is less similar [120,121]. The structure of plant HSFs is very conserved
and consists of several vital parts such as the oligomerization domain (OD), DNA binding
domain (DBD), transcriptional activation motif (AHA), nuclear export signal (NES), and
the nuclear localization signal (NLS) [122]. The oligomerization domain (OD) consists
of a bipartite heptad pattern of hydrophobic amino acid residues in the HR-A and HR-B
regions, and a flexible linker links it to the DNA-binding domain (DBD) [123]. The N-
terminal DNA binding domain (DBD) is distinguished by a core helix–turn–helix motif
that particularly attaches to the target promoter’s heat stress elements (HSEs), activating
stress-inducible gene transcription [124]. The plant HSF C-terminal stimulation domain
is described by short peptide motifs (AHA) that consist of giant hydrophobic and acidic
amino acid residues. These residues are unique to HSFA and are absent in the HSFB and
C classes [125]. The nuclear localization signal (NLS) and nuclear export signal (NES)
of HSFs play a significant role in forming a nuclear entrance complex consisting of the
target protein and the receptor-mediated export complex, including the NES receptor
exportin-α [126]. The classification of plant HSFs into HSFA, HSFB, and HSFC is based
on the number of amino acid residues inserted into the HR-A and HR-B regions and the
linker length area between the DBD and HR-A and HR-B regions [127]. Class A HSFs
have the transcriptional activation domain, while classes B and C HSFs lack this specific
amino acid motif and cannot promote transcriptional activation alone [128,129]. It is now
well-established that several HSF classes modulate HSP expression in tomato plants and
have a positive regulatory role in osmotic, oxidative, thermal, anoxia, and stress tolerance,
particularly by HSFA [130].

The Heat Shock Factor A1 Class (HSFA1)

Investigations on model crop plants, including tomato [131], A. thaliana [132], and
soybean [133], have shown that HSFA1-related genes are expressed constitutively under
normal circumstances; however, their expression increases rapidly under heat stress, which
designates them as significant master regulators of the heat stress response. In tomatoes,
there are four members of the class HSFA1, namely, HsfA1a (Solyc08g005170), HsfA1b
(Solyc03g097120), HsfA1c (Solyc08g076590), and HsfA1e (Solyc06g072750). Among these
members, HSFA1a is the master regulator because of its consistent expression in control and
heat stress (HS) conditions across all tissues. On the other hand, HSFA1c and HSFA1e are
typically significantly expressed in red ripe fruits, while HSFA1b is strongly stimulated in
all fruit stages [134]. HSFA2 plays a crucial role in the priming mechanism of tomato plants,
which is responsible for maintaining pollen thermotolerance throughout the process of
microsporogenesis [135]. A previous study provided evidence that the expression reduction
Metabolites 2024, 14, 283 12 of 28

in HSFA2 resulted in a decrease in the viability and germination rate of pollen exposed
to HS during the meiosis and microsporogenesis phases, which supports the notion that
it plays a crucial role in maintaining thermotolerance [136]. The expression levels of
tomato HSF genes, namely, SlyHSF01, SlyHSF8, SlyHSF9, SlyHSF10, and SlyHSF11, have
been observed to be significantly higher in leaf tissues under a high temperature (45 ◦ C)
compared with a control (30 ◦ C) situation [137]. The cytoplasm is the site for tomato HSFA3
(Solyc09g009100) expression under a controlled environment, while the nucleus is the
site of its expression under HS circumstances [138]. According to reports, tomato HsfA4s
(Solyc07g055710, Solyc03g006000, and Solyc02g072000) significantly boost the expression of
HS genes, while HSFA5 (Solyc12g098520) is a particular inhibitor of HSFA4 action [139,140].
A reduction in HSFB4a ((Solyc04g078770) expression and a boost in HSFA7 levels regulate
thermo-tolerance in tolerant tomato cultivars [141]. The overexpression of SUMO E3
ligase (SlSIZ1) in tomatoes led to an enhanced heat tolerance by regulating the activities
of HSFA1 and promoting the accumulation of HSP70 [142]. In a heat-resistant tomato
cultivar (CLN1621L), the gene notabilis (Solyc07g056570) and acyl-sugar acyltransferase
(Solyc09g014280) exhibit upregulation as positive regulators of HS tolerance, while the gene
Pin-II proteinase inhibitor (Solyc03g020030) shows downregulation as a negative regulator
of thermotolerance, indicating that the inverse expression of these genes encodes enzymes
and proteins that play significant roles in mitigating heat stress [143].

13. Involvement of Omics Approaches

Omics technologies are distinguished by their systematic investigation and analysis of
extensive datasets that capture the entirety of a biological system’s structure and function
at a specific level, which has significantly transformed the approaches used to study bio-
logical systems [144]. Multi-omics strategies involve techniques such as transcriptomics,
genomics, metabolomics, proteomics, epigenomics, proteogenomics, lipidomics, interac-
tomics, ionomics, phenomics, and bioinformatics, which produce a significant amount
of data that can be utilized to understand the physiological and molecular mechanisms
functioning in plants under stresses and devise effective strategies for mitigating the ad-
verse impacts of such stresses [145,146]. However, relying exclusively on a single omics
approach is inadequate to fully elucidate the complexities of plant responses to abiotic
stresses, particularly HS. The utilization and incorporation of multi-omics methodologies
are necessary to achieve promising results. Hence, integrating multi-omics methods is
essential for satisfactory inferences [147,148].

13.1. Genomics
Genomics research explores a genome’s structure, function, evolution, mapping, and
changes. At the same time, the latest advances in molecular biology have quickened the rate
of high-throughput genome sequencing, genomic characterization, and gene expression
analysis [149]. Functional genomics involves the analysis of partial or unbiased genome
sequencing data to elucidate gene functions and interactions, which is achieved through a
forward approach consisting of investigating randomly obtained mutants of a particular
phenotype and identifying the responsible gene or a reverse approach by disrupting a
known gene to examine the organism’s phenotype [150,151]. Genome-wide association
studies (GWASs) involve the comprehensive analysis of a complete genome to uncover
DNA changes associated with a particular trait [38]. The main objective of GWASs is to
determine genomic regions related to agronomic or morphological characteristics and
any phenotypes that may serve as markers, genes, or QTLs for gene identification, intro-
gressive hybridization, and marker-assisted breeding (MAB) [152,153]. GWASs revealed
the upregulation of SlTFT6, a gene belonging to the Sl14-3-3 family, which improved
thermotolerance in tomato plants [154]. Structural genomics focuses on elucidating the
three-dimensional configuration of genes to ascertain their identity, position, and arrange-
ment along the chromosome [155]. Genomic selection represents an innovative approach
to enhancing quantitative traits by leveraging marker and phenotypic data obtained from
Metabolites 2024, 14, 283 13 of 28

observed populations, thereby evaluating the influence of all genetic loci [156]. Genome
sequencing and mapping comprise several systems, such as the Roche 454GS FLX Titanium
or Illumina Solexa Genome Analyzer, which are considered next-generation sequencing
(NGS) platforms and have significantly reduced the cost and time required for sequencing
compared with traditional methods like the Sanger method [157]. These platforms have
provided comprehensive information regarding the characteristics of genomes, including
coding and non-coding genes, GC contents, repetitive elements, and regulatory sequences,
which have facilitated the development of improved crop varieties such as tomato, rice,
wheat, maize, sorghum, and soybean [158,159]. Molecular markers, also known as genetic
markers, are segments of DNA that may detect changes in a population’s DNA or polymor-
phisms, including deletions, insertions, and substitutions of bases [160]. Various molecular
markers, such as random amplified polymorphic DNA (RAPD), simple sequence repeats
(SSRs), sequence-tagged sites (STSs), restriction fragment length polymorphism (RFLP),
single-nucleotide polymorphism (SNP), and amplified fragment length polymorphism
(AFLP), have been recently identified as valuable tools for identifying polymorphisms in
plants [161]. The investigation of comparative genomics involves the alignment of bio-
logical sequences and the identification of conserved sequences, which reveals significant
synteny among related species [162] and enables the detection of small-scale changes within
different genomes, including protein-coding regions and their impact on protein structure
and function [163].

13.2. Transcriptomics
The term “transcriptome” covers the complete collection of ribonucleic acid (RNA)
molecules within an organism or a particular cell type, which mainly ranges from protein-
coding messenger RNA (mRNA) to various non-coding RNAs such as transfer RNA
(tRNA), long non-coding RNA (lncRNA), ribosomal RNA (rRNA), primary microRNA (pri-
miRNA), and small nuclear RNA (snRNA) [164–166]. The transcriptomic approach covers
multiple facets of RNA-seq evaluation, especially experimental design, quality control,
read alignment, quantification of gene and transcript levels, visualization, differential gene
expression, alternative splicing, functional analysis, gene fusion detection, and expression
quantitative trait loci (eQTL) mapping [167,168]. The primary focus of transcriptomic
research is to examine gene transcripts or RNA linked to a plant’s phenotypic expression
under various stress conditions [169] by employing a range of techniques, including serial
analysis of gene expression (SAGE), DNA microarrays, and high-throughput technologies
based on next-generation sequencing (NGS) for conducting digital gene expression (DGE)
and RNA sequencing (RNAseq) [170,171]. The transcriptomic analysis of microspores from
a heat-tolerant tomato cultivar (cv. Hazera 3042) revealed elevated levels of heat-responsive
gene expression, specifically LeHSFA2, LeHSP17.4-CII, homologs of LeHSP90 (Laternula
elliptica), and AtVAMP725 (A. thaliana), compared with a control [172]. The transcriptomic
study findings indicated a notable increase in the expression of SAUR (small auxin upregu-
lated RNA) family proteins, MYB (myeloblastosis viral oncogene homolog) transcription
factors, and NAC (no apical meristem) domain proteins in response to arid environmental
conditions. Furthermore, it was observed that the heat-tolerant line exhibited a significant
inclusion of heat shock proteins and proteinase inhibitors [173]. The transcriptomic analysis
of tomato plants subjected to heat stress at temperatures of 35/25 ◦ C, in conjunction with
specific nitrogen fertilizer levels, showed a significant upregulation of genes, including
cell wall invertase (CWINV2; Solyc10g085650.2, Solyc10g085640.1) and sucrose trans-
porter (SUT1; Solyc11g017010.2), while hexokinase 2 (HK2) (Solyc06g066440.3), SWEET2
(Solyc07g062120.4), and SWEET1 (Solyc04g064610.3) exhibited downregulation [174].

13.3. Metabolomics
Metabolomics is the scientific investigation of naturally occurring tiny, low-molecular-
weight metabolites, including carbohydrates, fatty acids, amino acids, steroids, and lipids,
which play distinctive roles in interpreting cellular biochemistry [175,176]. The function of
Metabolites 2024, 14, 283 14 of 28

a metabolite can be significantly altered by minor alterations in its chemical structure and
the presence of external abiotic or biotic stimuli [177]. Metabolomics inquiry offers distinct
advantages over other omics because metabolites are the downstream products of gene
and protein activities, which determine the impact on biological phenotype and other phys-
iologic processes [178]. Plant metabolites can be primary metabolites, which are crucial for
growth and significantly impact physiological processes, and secondary metabolites, which
are vital for defense mechanisms in response to various stressors [179,180]. A variety of ad-
vanced techniques exist for the analysis of plant metabolites, including gas chromatography
(GC), high-performance liquid chromatography (HPLC), thin-layer chromatography (TLC),
paper chromatography (PC), nuclear magnetic resonance (NMR), metabolic flux analysis
(MFA), extracellular flux analysis (EFA), direct-inject mass spectrophotometry (DIMS),
Fourier transform infrared spectroscopy (FTIR), capillary electrophoresis (CE), and mass
spectrometry (MS), which have proven to be valuable tools for researchers [181,182]. A
metabolic investigation of tomatoes under elevated temperatures and relative air humidity
revealed the disruption of enzymes involved in sucrose metabolism, resulting in a decrease
in the fruit-soluble sugar content. Conversely, an increase in the activities of enzymes
associated with phosphopyruvate carboxylase (PEPC), mitochondria aconitase (MDH), and
citrate synthetase (CS) led to an elevated content of malic acid [183]. Metatomic analysis
has shown a significant association among sucrose, glucose, fructose, the TCA cycle, starch
production, and HS tolerance [184]. Liquid chromatography–mass spectrometry (LC-MS)
identified an increased accumulation of secondary metabolites, specifically flavonoids,
within the pollen microspore of tomatoes under heat stress [185]. A metabolic analysis
of tomatoes using gas chromatography–mass spectrometry (GC-MS) revealed that heat
treatment mitigated the effects of chilling on fruits by modifying the concentrations of
several fruit metabolites, including arabinose, fructose-6-phosphate, valine, and shikimic
acid, in the chilled samples as compared with a control [186].

13.4. Proteomics
Proteomics comprehensively explores protein composition, structure, expression, mod-
ification status, connections, and interactions among proteins [187]. Basic proteomics tech-
niques include one-dimensional (1D) and two-dimensional (2D) gel electrophoresis (2-DE)
methodologies [188]. Several other high-throughput screening technologies such as shotgun
proteomics (SP), nanoflow liquid chromatography coupled to tandem mass spectrometry
(nLC-MS/MS) [189], stable isotope labeling by amino acids in cell culture (SILAC) [190,191],
multidimensional protein identification technology (MudPIT) [192], isobaric tags utilized in
relative and absolute quantitation (ITRAQ) [193,194], the Western blot (WB) technique [195],
multiple reactions monitoring mass spectrometry (MRM-MS) [196], and tandem mass tags
(TMTs) [197,198] are available for utilization according to research objectives. Proteomic
analysis of the tomato revealed better pollen tolerance to heat stress following ethephon pre-
treatment by increasing protein abundance in processes of protein synthesis, degradation,
the tricarboxylic acid cycle, and RNA regulation [199]. Another proteome analysis of toma-
toes subjected to high-light-induced stress revealed a notable presence of oxygen-evolving
complex and PSII complex proteins, including PsbH, PsbS, PsbR, and Psb28, within the leaf
zone that exhibited the maximum damage [200]. Tandem mass tag (TMT)-based analysis
of pollen mother cells at the initial anther developmental stage in the Maxifort tomato
variety revealed the upregulation of 96 proteins including heat shock proteins, calreticulin,
and exocytosis associated with protein folding/refolding/targeting/removal along with
the secretion of aggregated and damaged proteins/peptides and the downregulation of
158 proteins active in ubiquitin-mediated protein breakdown, antioxidant mechanisms,
and the metabolism of lipids and carbohydrates [201].

14. Genome Editing Strategy Application

Genome editing has emerged as a promising tool in tomato breeding, offering the
potential for immense success and fully utilizing genome information and phenotyping
Metabolites 2024, 14, 283 15 of 28

technologies. It is divided into two major approaches, first, as site-directed nuclease

(SDNs) and, second, as oligonucleotide-directed mutagenesis (ODMs) involved in creating
mutations in the genome [202]. Its application could enhance HS resistance by introduc-
ing mutations into negative regulatory genes, which have a pivotal role in tomato HS
tolerance [203]. It entails the utilization of several DNA-cleaving enzymes, known as nu-
cleases, specifically designed to cleave the DNA at a pre-established site through diverse
DNA binding systems. Several techniques can be applied to carry out specific DNA cleav-
ages, such as zinc finger nucleases (ZFNs), mega-nucleases (MNs), clustered regularly
interspaced short palindromic repeat (CRISPR)-associated proteins (CRISPR/Cas), and
transcription activator-like effector nucleases (TALENs). These are entitled site-directed
nucleases (SDNs), representing the fundamental concept of using a DNA-cutting enzyme
(nuclease) to create a specific DNA break at a particular location [204,205]. CRISPR/Cas
systems are further divided into classes 1 and 2 based on effector molecules. The class
1 system has multiple effector molecules and is subdivided into three types, including I,
III, IV, and 12 subtypes found in 90% of the CRISPR loci in bacteria and archaea targeting
DNA and RNA. The class 2 system is characterized by a single effector molecule, with
three types, including II, V, and VI, and nine subtypes, which represent 10% of the CRISPR
loci targeting DNA and RNA and are found in bacteria. The most prevalent CRISPR/Cas
systems utilized for gene editing are type II-A Cas9 from Streptococcus pyogenes and
type V-A Cas12a (Cpf1) from Acidaminococcus sp. and Lachnospiraceae [206–208]. The
CRISPR/Cas9-mediated removal of SlUDPGT52 resulted in improved drought tolerance
because of increased reactive oxygen species (ROS) scavenging [209]. The efficacy of
CRISPR/Cas9 in facilitating the introduction of de novo domestication of elite features
from wild relatives to the cultivated tomato, as well as the reverse process, has been demon-
strated. CRISPR/Cas9 technology has been utilized to manipulate and examine a range
of attributes about tomatoes, including leaf, stem, and male sterility, parthenocarpy, fruit
maturation, quality, nutrition, heat, drought, salinity stress, carbon–nitrogen metabolism,
and herbicide resistance [210,211]. Genome editing technology has contributed to the
heat-tolerant breeding of tomatoes via the identification of critical genes associated with
acquired thermotolerance mechanisms, including SlIAA9, HsfA2, JA/COI1, HsfB1, and
SlAGL6 [212]. It has improved tomato resistance by regulating genes such as lateral or-
gan boundaries domain (SlLBD40) (Solyc02g085910), mitogen-activated protein kinase
(SlMAPK3), and cytidine base editor (CBE) against biotic and abiotic stressors [213].

15. Development of Heat-Tolerant Tomato Varieties

There has been a global demand for the development of heat-tolerant varieties to
effectively respond to both present and anticipated rises in heat stress. However, breeding
for heat tolerance has encountered challenges related to the intricate nature of heat stress
and plant reactions and the limited comprehension of the genetic underpinnings of heat
tolerance characteristics [214]. The efficacy of heat-tolerant breeding is contingent on the
proficient determination and description of constituent qualities that underlie heat resis-
tance processes in the presence of heat stress, as well as the comprehensive understanding
of their genetic structure throughout both the vegetative and reproductive phases [215,216].
Affordable and technologically sophisticated high-throughput genotyping is being applied;
however, accurate phenotyping is a significant barrier to understanding the genetic basis
of required but intricate traits, which slows down breeding programs [217,218]. Effective
plant breeding programs have to prioritize the development of phenotyping techniques that
are cost-effective, precise, reliable, less labor-intensive, reproducible, and easily applicable,
targeting traits such as increased yield, resistance to biotic and abiotic stress, improved
quality, photosensitivity, synchronous maturity, and detoxification ability. To develop
tomato genotypes resistant to high temperatures, it is crucial to examine cultivated and
wild tomato genetic resources thoroughly. To create heat-resistant tomato varieties that
have high production and yield, it is essential to comprehend the genetic architecture of
heat-tolerance traits to effectively regulate the increase in metabolites, osmoprotectant,
Metabolites 2024, 14, 283 16 of 28

photosynthetic activity efficiency, membrane stability, the number of flowers per inflores-
cence, inflorescence number, pollen number, female fertility, pollen viability, fruit set, fruit
number, and fruit weight and the decrease in canopy temperature, style protrusion, and
style length [219–221]. Previous breeding projects have not derived significant benefits
from the sizeable range of wild tomatoes, mainly because of problems such as progeny
sterility, self-incompatibility, and linkage drag [222]. For breaking linkage drag, various
techniques, including chromosome segment substitution lines (CSSLs), advanced backcross
quantitative trait loci (QTL) analysis, and backcross inbred lines (BILs), could be applied
to generate lines that possess small fragments of donor parent chromosomes [223–225]. A
practical approach in tomato breeding efforts to enhance resistance to abiotic and biotic
stressors is incorporating native germplasm and wild relatives into existing varieties by
introducing novel allelic combinations. Multiple tomato introgression lines have been
developed by using wild cousins such as Solanum pimpinellifolium, Solanum habrochaites,
and Solanum pennellii, which exhibit resistance to abiotic and biotic stressors [226–228].

16. Genetic Resource Development

Genetic resources or germplasm includes plants, parts of plants, and seeds, which
are significant for breeding, research, and conservation. For example, seeds of an ancient
heirloom tomato variety passed down to current time are just seeds produced by a gardener
or company, but they are germplasm when part of a breeding program for new variety
development, collected for the preservation of the genetic diversity, or preserved as geneti-
cally governed traits [229]. Lycopersicum tomato species are diploid (2n = 2x = 24) with
similar chromosome numbers and structures [230] that produce perfect hermaphrodite
flowers and have a complete range of mating systems from autogamous L. cheesmanii and
L. parviflorum to obligately outcrossed self-incompatible biotypes of L. chilense, L. hirsutum,
L. peruvianum, and L. pennellii [231], while the tendency of self-fertility with different levels
of facultative outcrossing is present in L. chmielewskii, L. esculentum, L. pimpinellifolium, and
the self-compatible biotypes of L. hirsutum and L. pennellii [232]. In the quest for specific
genetic traits, contemporary and prospective researchers and crop breeders must have
full access to landraces, diverse varieties, and relevant wild species. Multiple institutes
have developed tomato genetic resources to cater to the needs of researchers and breeders
studying heat tolerance and other agronomic features. About 62.8 thousand tomato acces-
sions, both wild and domesticated varieties (L. esculentum), are present in gene banks across
the globe and are ready to be used for genealogical research [233]. The Tomato Genetics
Resource Center (TGRC) at the University of California (Davis) (http://tgrc.ucdavis.edu/,
accessed on 11 December 2023), the United States of America, is a well-recognized and
valuable repository of various germplasm and wild species. The World Vegetable Center
(http://seed.worldveg.org, accessed on 11 December 2023), located in Taiwan, China,
maintains a vast assortment of around 8835 tomato accessions, of which 6676 are readily
available for procurement upon request. A wide variety of tomato genetic resources have
been collected by the National Agriculture and Food Research Organization (NARO) gene
bank (https://www.gene.affrc.go.jp, accessed on 22 January 2024) and the National Bio-
Resource Project (NBRP) of tomato (https://tomato.nbrp.jp, accessed on 24 January 2024)
in Japan. The National Bio-Resource Project (NBRP) maintains a collection of more than
10,000 Micro-Tom mutants that have been generated using the techniques of gamma-ray
irradiation and ethyl methane sulfonate (EMS) mutagenesis [234,235]. The Micro-Tom
plant is a model for investigating fruit production and its ability to withstand different
abiotic and biotic challenges [236]. Data about Micro-Tom mutants can be retrieved from
the TOMATOMA database, found at http://tomatoma.nbrp.jp/index.jsp (accessed on 8
February 2024) [237]. Several other genetic resources are available from which seeds or
genetic material could be obtained, including the Solanaceae Genomics Network (SGN,
http://solgenomics.net/, accessed on 8 February 2024), the United States Department of
Agriculture (USDA) (https://www.usda.gov/, accessed on 14 February 2024), the Tomato
Genetics Cooperative (TGC) (https://tgc.ifas.ufl.edu/, accessed on 17 February 2024) at
Metabolites 2024, 14, 283 17 of 28

the University of Florida, USA, the Ohio State Tomato Breeding and Genetics Program
(OSTBGP) (https://tomato.cfaes.ohio-state.edu/, accessed on 17 February 2024), Vavilov
Institute, Russia (VIR) (https://www.vir.nw.ru/en/, accessed on 3 March 2024), and Insti-
tuto de Investigaciones Fundamentales en Agricultura Tropical (INIFAT), Cuba [238,239].
These genetic resource reservoirs could be accessed and explored to obtain genes for tomato
heat resistance improvement and other targeted breeding programs.

17. Conclusions and Future Aspects

The average global temperature has significantly increased because of global climate
change, which has also put food security and agricultural output at risk [240]. Reduced
photosynthesis, decelerated growth and development, and reduced nutrient uptake are
just a few of the physiological and biochemical processes upset by heat stress in tomatoes,
resulting in yield losses [220,241]. Over the next several years, it is anticipated that the
damaging consequences of heat stress will get worse. Uncertainty surrounds the magnitude
of the potential consequences associated with global warming. Changes can have both
direct and indirect impacts on food production conditions. Direct changes can lead to
significant changes in food production, resulting in increased mortality rates because of
floods, storms, heat waves, and droughts. On the other hand, indirect effects may include
unemployment in rural areas requiring specific climate conditions for crop growth, such as
cultivating tomatoes in open fields [242,243].
Environmental change, particularly a rise in ambient temperatures, substantially
affects plant growth, development, production, and yield, leading to a severe decline in
crop yield and jeopardizing international food security. Increasing heat stress disrupts
various physiological and biochemical systems in tomato plants. Tomato seed pollen
viability and root development are significantly affected by elevated temperatures in
different parts of the world. The emerging data indicate that reactive oxygen species
(ROS) cause cellular oxidative damage but also serve as signaling molecules in the heat
stress response (HSR), triggering adaptive responses. However, the exact mechanism
underlying the interconnections among various signaling pathways linked with ROS has
not yet been fully understood. Understanding the interaction between ROS and redox
signals and identifying the precise redox pathways activated in different cell compartments
is essential for adjusting HSR in response to varying HS intensity and duration levels. The
molecular processes behind the pollen heat-stress response and thermotolerance remain
largely unexplored. In the context of escalating global warming, there is an urgent need
for molecular and genetic research to ascertain the genes responsible for conferring heat
tolerance in tomatoes, thereby mitigating the detrimental effects of high temperatures.
The primary objective of high-throughput phenotyping should be to investigate several
aspects of plant physiology, including canopy temperature, pollen viability, photosynthetic
efficiency, membrane thermostability, sugar content, and osmoprotectant activity, to obtain
full inside knowledge.
In our opinion, to enhance the overall resilience of tomatoes against heat stress, it is
crucial to elucidate the molecular and physiological mechanisms underlying the negative
correlations among seed germination, plant growth, development, pollen viability, fruit sets,
fruit size, fruit weight, other agronomic traits, and thermal stress. Collecting diverse tomato
genetic resources, including various cultivars and wild species, would be valuable for future
genetic engineering, particularly in developing heat-resistant tomato plants. Including wild
tomato species in breeding programs incurs some drawbacks since introducing genes from
wild relatives into advanced lines might alter the already established horticultural features
owing to linkage drag. Transgenic technology has the potential to serve as an advantageous
instrument for enhancing the heat stress resistance of tomatoes, especially when integrated
with conventional techniques. Integrating marker-assisted breeding with high throughput
phenotyping can significantly improve the breeding performance of tomatoes in terms of
heat resilience. Understanding the genetic foundations of novel populations is of utmost
importance, including approaches like chromosomal segment substitution lines (CSSLs),
Metabolites 2024, 14, 283 18 of 28

introgression lines (ILs), backcross inbred lines (BILs), and mutants for trait identification.
Genome editing could identify the molecular mechanism of heat stress transcription factors
and enhance heat tolerance features, like increasing the number of inflorescences and
flowers per inflorescence.
Despite certain advancements in translational genomics, particularly with the backing
of the gene-editing technology CRISPR/Cas9, some significant difficulties remain, for ex-
ample, several features subject to quantitative regulation require several genes. Hence, it is
imperative to manipulate several new genes to induce new desired phenotypes in modified
tomato crops. Further challenges include the lack of effective delivery routes for gene
editing reagents such as mRNA (sgRNA), DNA plasmid, and ribonucleoprotein (RNP),
technical bottlenecks, and ethical concerns. Moreover, there is a lack of comprehensive ge-
netic data regarding the necessary dietary components, and generating accurate alterations
in DNA sequences is challenging. Nevertheless, several gene-editing techniques offer
effective and precise gene editing of plants, including base editors, replicons, and targeted
non-homologous insertions. The continuous progress in sequencing technology can be
utilized to find reference genome sequences for previously unknown tomato wild cousins,
which will serve as a great approach to exploit the genetic variability in these species.
Genome editing facilitates the development of novel domestication tactics that selectively
utilize tomato relatives. Establishing more vibrant collaboration between private plant
breeding enterprises and public sector gene banks at regional, national, and worldwide
levels is essential. It has significant benefits, particularly in enhancing the conservation and
utilization of tomato genetic resources.
A holistic approach is required to comprehensively elucidate the causes of tomato
susceptibility to heat stress and the development of heat-resistant varieties in the interfaces
of continuously increasing global temperature. So, integrated strategies (Figure 7) based
on sophisticated technologies involving high-throughput genotyping, genome editing,
and multi-omics approaches like transcriptomics, genomics, metabolomics, proteomics,
epigenomics, proteogenomics, lipidomics, interactomics, ionomics, phenomics, bioinfor-
matics genetic engineering, genetic resources collection, preservation, and utilization would
enable researchers and breeders to develop heat-tolerant tomato varieties with capabilities
to combat increasing temperature stress for a long time.
Metabolites 2024, 14, x FOR PEER REVIEW 20 of 29
Metabolites 2024, 14, 283 19 of 28

Figure 7. Improving heat tolerance in tomatoes through integrated approaches, including genomics,
Figure 7. Improving heat tolerance in tomatoes through integrated approaches, including genomics,
transcriptomics, proteomics, metabolomics, gene editing, and genetic resources.
transcriptomics, proteomics, metabolomics, gene editing, and genetic resources.

Author Contributions: Conceptualization, Q.K. and Y.Z.; methodology monitoringand H.Y.; formal
Author Contributions: Conceptualization, Q.K. and Y.Z.; methodology monitoringand H.Y.; formal
analysis, G.X., Q.K., H.Y., Z.L. and Y.Z.; investigation, Q.K., Y.Z., H.Y. and G.X.; visualization, Y.W.,
analysis, G.X., Q.K., H.Y., Z.L. and Y.Z.; investigation, Q.K., Y.Z., H.Y. and G.X.; visualization, Y.W.,
G.X., Y.Z., Z.L. and H.Y.; data curation, Y.W., G.X. and Q.K.; writing—original draft preparation,
G.X., Y.Z., Z.L. and H.Y.; data curation, Y.W., G.X. and Q.K.; writing—original draft preparation, Q.K.,
Q.K., Y.Z. and Z.L.; writing—review and editing, Y.W., G.X., Z.L. and H.Y.; funding acquisition, Y.Z.
Y.Z. and Z.L.; writing—review and editing, Y.W., G.X., Z.L. and H.Y.; funding acquisition, Y.Z. All
All authors have read and agreed to the published version of the manuscript.
authors have read and agreed to the published version of the manuscript.
Funding: This research was supported by the Zhejiang Provincial Natural Science Foundation of
Funding: This research was supported by the Zhejiang Provincial Natural Science Foundation of
China under Grant No. LY22C150007, the Zhejiang Provincial Natural Science Foundation of China
China under Grant No. LY22C150007, the Zhejiang Provincial Natural Science Foundation of China
under Grant No. LY20C030002, the Key Research and Development Program of Lishui under Grant
under Grant No. LY20C030002, the Key Research and Development Program of Lishui under Grant
No. 2020ZDYF08, and Lishui University Initial Funding under Grant No. QD1503.
No. 2020ZDYF08, and Lishui University Initial Funding under Grant No. QD1503.
Metabolites 2024, 14, 283 20 of 28

Institutional Review Board Statement: No experiments with humans or animals were performed in
this study, so ethical clearance was not required.
Informed Consent Statement: All authors agreed to contribute to this manuscript.
Data Availability Statement: All the necessary data are included in this manuscript.
Conflicts of Interest: The authors declare that they have no conflicts of interest.

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