Journal of Plant Physiology 268 (2022) 153581

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Journal of Plant Physiology

journal homepage: www.elsevier.com/locate/jplph

Differential physiological response to heat and cold stress of tomato plants

and its implication on fruit quality
Tania Mesa a, Javier Polo b, Alba Arabia a, Vicent Caselles a, Sergi Munné-Bosch a, b, c, *
a
Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Faculty of Biology, Av. Diagonal 643, E-08028, Barcelona, Spain
b
R&D Department, APC Europe S.L., Granollers, Spain
c
Research Institute of Nutrition and Food Safety, University of Barcelona, Faculty of Biology, Av. Diagonal 643, E-08028, Barcelona, Spain

A R T I C L E I N F O A B S T R A C T

Keywords: The upcoming climate change presents a great challenge for plant growth and development being extremes
Tomato (Solanum lycopersicum L.) temperatures among the major environmental limitations to crop productivity. Understanding the repercussions
Extreme temperature of these extreme temperatures is of high importance to elaborate future strategies to confront crop damages.
Acclimation
Tomato plants (Solanum lycopersicum L.) are one of the most cultivated crops and their fruits are consumed
Fruit quality
Ascorbate
worldwide standing out for their organoleptic characteristics and nutritional value. Tomato plants are sensitive
Tocochromanols to temperatures below 12 ◦ C and above 32 ◦ C. In this study, Micro-Tom cultivar was used to evaluate the effects
of extreme temperatures on the plant of tomato and the fruit productivity and quality from the stressed plants,
either exposed to cold (4 ◦ C for three nights per week) or heat (32 ◦ C during the day, seven days per week)
treatments. Total productivity and the percentage of ripe fruits per plant were evaluated together with foliar
stress markers and the contents of photosynthetic pigments and tocochromanols. Fruit quality was also assessed
determining lycopene contents, total soluble solids, total acidity and ascorbate contents. High temperatures
altered multiple physiological parameters indicating a moderate stress, particularly decreasing fruit yield. As a
response to this stress, plants enhanced their antioxidant contents both at leaf and fruit level. Low temperatures
did not negatively affect the physiology of plants with similar yields as compared to controls, suggesting chilling
acclimation. Both high and low temperatures, but most particularly the former, increased total soluble solids
contents indicating that temperature control may be used as a strategy to modulate fruit quality.

1. Introduction
Recent studies have highlighted that the intensity, frequency, and
duration of extreme weather events have been changing in the last few
years, particularly, temperature extremes (Ummenhofer and Meehl,
2017). According to the Intergovernmental Panel on Climate Change
(Collins et al., 2013), there will be more records of high temperatures
than cold temperatures in a warmer climate. However, it is also stated
that cold extremes will continue to occur in a warmer climate. Plant
growth, development, productivity and quality are highly dependent on
temperature and each species has a temperature range along with an
optimum temperature for each of these processes (Hatfield et al., 2014;
Hatfield and Prueger, 2015). As a result, climate change entails great
challenges for agriculture worldwide, particularly high and low tem­
peratures (Meena et al., 2018). These projections highlight the relevance
of understanding the repercussions of extreme temperatures on plant
growth, development and yield in order to evaluate possible future
strategies to confront crop damages.
Tomato plants (Solanum lycopersicum L.) are endemic to the Andean
region, currently comprising Peru, Colombia, Ecuador and Bolivia
(Gerszberg et al., 2015). Tomato plants arrived in Europe in the 16th
century and subsequently their cultivation spread worldwide (Kimura
and Sinha, 2008). Today, they are one of the most cultivated crops and
their fruits are consumed worldwide with a production of more than 180
million tonnes in a cultivation area of 5.03 million hectares (FAOSTAT,
2017). The main tomato-producing countries are China, the United

Abbreviations: AA, ascorbic acid; DHA, dehydroascorbic acid; FMA, leaflet mass per area; H, hydration; PC-8, plastochromanol-8; TA, total acidity; TSS, total
soluble solids.
* Corresponding author. Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Faculty of Biology, Av. Diagonal 643,
E-08028, Barcelona, Spain.
E-mail address: smunne@ub.edu (S. Munné-Bosch).

https://doi.org/10.1016/j.jplph.2021.153581
Received 27 July 2021; Received in revised form 24 November 2021; Accepted 25 November 2021
Available online 6 December 2021
0176-1617/© 2021 The Authors. Published by Elsevier GmbH. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
T. Mesa et al.
States, Turkey and India, while Spain is in the eighth place (FAOSTAT,
2017). There are currently more than 5000 different varieties of to­
matoes (Kimura and Sinha, 2008; Gerszberg et al., 2014). Tomato is an
herbaceous plant that can grow up to 3 m high with a sympodial hairy
stem and its leaves are composed of an odd number of leaflets (Costa
et al., 2017; OECD, 2017). Their bright yellow flowers are hermaphro­
dite and can be self-pollinated (Ozores-Hampton, 2014).
Tomato fruits are red berries of variable size depending on the va­
riety (OECD, 2017). The tomato fruit consists of several parts such as the
pericarp, which contains the exocarp, the mesocarp and the endocarp;
the placenta, formed by parenchyma tissue in the centre of the fruit and
the locular cavity where the seeds are surrounded by a mucilaginous gel
(McCormack, 2004; Rančić et al., 2010). They are climacteric fruits with
six different stages of development and ripening from immature green to
overripe (Takizawa et al., 2014). The tomato fruit stands out for its
organoleptic characteristics and nutritional value, being a great source
of lycopene, vitamins and minerals (Meena et al., 2018). Furthermore,
tomatoes are also of great importance for research since it is a model
species whose genome has already been sequenced (The Tomato
Genome Consortium, 2012).
Some plants have the ability to adjust their growth or senescence of
shoots or roots to upregulate or downregulate individual proteins or
whole metabolic pathways in order to acclimate to stresses (Demmi­
g-Adams et al., 2008). Temperature stress often has a negative effect on
cellular homeostasis, plant metabolism and major physiological pro­
cesses increasing the accumulation of reactive oxygen species (ROS)
(Suzuki and Mittler, 2006). To scavenge these ROS, non-enzymatic an­
tioxidants such as ascorbic acid (AA) and tocochromanols are essential
(Suzuki and Mittler, 2006; Falk and Munné-Bosch, 2010). Ascorbic acid
(or vitamin C) protects cellular components from free radicals generated
in the aqueous phase turning into its oxidized form, dehydroascorbic
acid (DHA) (Beyer, 1994). Tocochromanols, particularly, α-tocopherol
(or vitamin E), scavenge singlet oxygen and lipid peroxyl radicals thus
preventing the propagation of lipid peroxidation in membranes
(Munné-Bosch and Alegre, 2002). However, it is of great importance not
to forget that ROS also act in stress signalling thus indicating that the
role of antioxidants is not to fully eliminate ROS but rather regulate their
concentration (Arrigoni and De Tulio, 2002).
Many crops of topical/subtropical origin such as cotton, maize or
tomato, are chilling-sensitive (Lyons, 1973). Tomato plants are sensitive
to temperatures below 12 ◦ C but also temperatures above 32 ◦ C (Sato
et al., 2001; Liu et al., 2012; Meena et al., 2018). The ability of tomatoes
to acclimate to chilling temperatures has been previously described by
Barrero-Gil et al. (2016), showing acclimation of tomato plants at 10 ◦ C
prior to exposure at 4 ◦ C. For heat stress, exposure to elevated temper­
atures for a short term (heat shocks) have shown to have no positive
effects on tomato growth or development (Abdelmageed and Gruda,
2007). However, tomatoes have multiple mechanisms to survive under
heat stress (Alsamir et al., 2021).
Although multiple studies have previously described some of the
responses of tomato plants to heat and cold stress, none has compared
both low and high temperature stresses in plant and its on-plant ripened
fruits in the same study. Thus, the main purpose of this study was to
evaluate the response of tomato plants in terms of growth, development,
yield and fruit quality to heat and cold stress under controlled
conditions.
2. Materials and methods
2.1. Experimental design and samplings
Seeds of tomato plants (Solanum lycopersicum cv. Micro-Tom) were
obtained from the Experimental Field Facilities of the University of
Barcelona (Barcelona, NE, Spain). Seeds were sown on October 19th,
2020, in a seedbed and placed in a growth chamber (16 h light/8 h dark,
at 21.9 ◦ C and 65% relative humidity). On November 19th, 2020, 18
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Journal of Plant Physiology 268 (2022) 153581
seedlings were transferred to 1 L pots in a climate-controlled growth
chamber at a daily mean temperature and relative humidity of 22/22 ◦ C
and 60% (day/night). Then, on December 4th, when temperature
treatments started, plants were separated into three groups of 6 plants
each (n = 6). The control group was located in a climate-controlled
growth chamber at a daily mean temperature and relative humidity of
22/22 ◦ C and 60% (day/night); the heat-stressed group at 32/22 ◦ C and
60%; and the cold-stressed group at 22/4 ◦ C and 60% (3 days per week)
and 22/22 ◦ C and 60% (4 days per week). All the plants were located
over trays filled permanently with Hoagland nutrient solution.
Leaf samplings were made at midday at 0, 1, 2, 4, 6, 8, 10 and 12
weeks since the start of the treatment (on December 4th). In each
sampling, two leaflets, marked since the beginning, were selected: one
was used to measure leaf growth and hydration and the other was frozen
in liquid N2 and stored at − 80 ◦ C for subsequent biochemical analyses.
Fruit samplings were made at the time point where all the plants
from one specific treatment had at least 2 ripe tomatoes (or Stage V, as
described by Takizawa et al., 2014). The samplings were performed on
February 1st, 2021, for the control group, February 2nd, for the
cold-stressed group and February 16th, for the heat-stressed group. All
the ripe tomatoes of each plant were harvested in each sampling: one
was frozen in liquid N2 and stored at − 80 ◦ C for subsequent biochemical
analyses. The rest were used to analyse quality parameters.
2.2. Chlorophyll fluorescence, leaf morphology and water status
The maximum efficiency of photosystem II (Fv/Fm), leaflet mass per
area ratio (FMA), hydration (H) and relative water content (RWC) of one
leaflet per plant were measured in six plants per treatment at each
sampling point. Fv/Fm was measured with a fluorimeter Mini-PAM II
(Photosynthesis Yield Analyser, Walz, Germany) in leaves sampled and
adapted to dark conditions for 1 h. The H was obtained following the
formula [(FW - DW)/DW] and the RWC was obtained using the formula
[(FW - DW)/(TW - DW) x 100], where FW is the fresh weight, TW is the
turgid weight (after rehydrating samples for 24 h in the dark at 4 ◦ C) and
DW is the dry weight (after oven-drying samples at 75 ◦ C until constant
weight). Leaflet area was measured with a flat-bed scanner and an image
processor (ImageJ 1.52p, National Institutes of Health, Bethesda, MD,
United States). The FMA was calculated as DW/Foliar area.
2.3. Photosynthetic pigments quantification
For the quantification of chlorophylls and carotenoids, 50 mg of
frozen leaves were ground in liquid nitrogen and extracted with cold
methanol +0.01% BHT (w/v) using ultrasonication (Branson 2510 ul­
trasonic cleaner, Bransonic, Danbury, CT, USA). The extract was then
centrifuged for 10 min at 4 ◦ C and 13000 rpm, and the supernatant was
collected. The pellet was re-extracted until colourless, pooling at the end
all the supernatants obtaining a final volume of 1.2 mL.
Photosynthetic pigments, including chlorophyll a and b and total
carotenoids, were analysed using UV/Visible spectroscopy of double
beam using a CE Aquarius UCE7400 (Cecil Instruments Ltd, Cambridge,
UK). The absorbance of the supernatants was read at 470 nm, 653 nm,
666 nm and 750 nm. Chlorophyll and carotenoids content were calcu­
lated following the equations developed by Lichtenthaler and Wellburn
(1983).
2.4. Tocochromanols analyses
Tocochromanol analyses, including the four different tocopherol
homologues, the four tocotrienol homologues and plastochromanol-8
(PC-8), were followed as described by Amaral et al. (2005). 50 mg of
ground frozen leaves or 100 mg of ground frozen fruit were extracted
with methanol containing 0.01% BHT (w/v) and 5 ppm (w/v) of tocol as
an internal standard. Extraction was performed using 30 min of ultra­
sonication and then the extract was centrifuged for 10 min at 4 ◦ C and
T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581

13000 rpm, and lastly, the supernatant was collected. The pellet was
re-extracted until colourless, pooling at the end all the supernatants. The
supernatants were then filtered with a hydrophobic PTFE filter of 0.22
μm (Phenomenex, Torrance, CA, USA). Tocochromanols were injected
into the High-Performance Liquid Chromatography system (consisting
of a Waters 600 controller pump, a Waters 717 plus auto-sampler and a
Jasco FP-1520 fluorescence detector). Fluorescence detection was at an
excitation wavelength of 290 nm and emission at 330 nm. The mobile
phase was a mixture of n-hexane and 1,4-dioxane (95.5:4.5, v/v) at a
flow rate of 0.7 mL/min. Tocochromanols were separated using an
Inertsil 100A column (5 μm, 30 × 250 mm, GL Sciences Inc., Tokyo,
Japan). A calibration curve was established with each of the tocochro­
manols analysed and corrected with the tocol recovery.

2.5. Yield and fruit quality parameters

Mean total fruits per plant and mean ripe fruits per plant were
measured once a week for the first 4 weeks and twice a week for the next
weeks since the 4th of December, where the first fruits appeared, until
the end of the experiment. In addition, the fresh weight of fruits was
measured by weighing freshly harvested fruits.
Titratable acidity (TA) was estimated with the juice obtained from a
pool of 4 tomatoes per plant. Five mL of each juice were diluted in 50 mL
of MiliQ water and used for titratable acidity determination with 0.1 M
NaOH and 1% phenolphthalein as an indicator to estimate citric acid
content as described by Latimer (2012). To obtain the ◦ Brix, and esti­
mate TSS, in 1 mL of tomato juice, we used a refractometer HI 96801
(Hannah Instruments, Italy).
Lycopene was estimated as previously described by Fish et al. (2002).
50 mg of ground frozen fruit were extracted with 250 μL of MiliQ water,
450 μL of acetone, 450 μL of ethanol and 675 μL of n-hexane. The apolar
phase was recovered and the rest was re-extracted with 675 μL of
n-hexane. The recovered phases were combined, and the absorbance
was read at 503 nm and 800 nm with quartz microplates.
The analysis of vitamin C was adapted from Takahama and Oniki
(1992) and Queval and Noctor (2007). 50 mg of ground frozen fruit
were extracted with 6% meta-phosphoric acid (w/v) and 0.2 mM
diethylene triamine pentaacetic acid using ultrasonication and centri­
fugation for 10 min at 4 ◦ C and 13000 rpm. The pellet was re-extracted
once more. The levels of ascorbic acid (AA) and dehydroascorbic acid
(DHA) were determined spectrophotometrically (xMark Microplate
Spectrophotometer, Bio-Rad, Hercules, CA, USA) with quartz micro­
plates reading the absorbance at 265 nm. Total ascorbate was calculated
as the sum of AA + DHA and Redox state was calculated as [AA/(AA +
DHA) x 100].

2.6. Statistical analyses

A two-way mixed ANOVA of repeated measures was performed for

the foliar analyses including between (Treatment) and within factors
(Time). All analyses were performed using the lme4 and afex packages
in R. A one-way ANOVA was performed for the fruit analyses. The Tukey
test was used as a posthoc method.
3. Results
3.1. Differential impact of temperature treatments on fruit development
Fig. 1. Fruit development variations in heat and cold stress groups compared to
controls. (A) Total yield, (B) Ripe fruits per plant and fresh weight per ripe fruit
and (C) % Ripe per total fruits. Data are mean of n = 6 ± SE. P values of two-
way mixed ANOVA of repeated measures are shown in the inlets and P values
> 0.05 were considered as not significant (NS). Different letters represent dif­
ferences between temperature treatments.

Temperature treatments had a differential effect on fruit develop­ 1.87 ± 0.49 g per fruit, respectively). The percentage of ripe fruits on a
ment. The heat-stressed group presented significant differences total fruit basis per plant (Fig. 1C) showed that the fruits from the heat-
compared to the control group whereas the cold-stressed group stressed group ripened faster than the other two groups after one month
remained unaffected (Fig. 1). Total fruits per plant and ripe fruits per since the first fruits were harvested.
plant (Fig. 1A and B) were a 62.99% and a 54.34% lower in the heat-
stressed group than in control group, respectively. However, the fruits
of this group presented a significantly higher fresh weight (3.57 ± 0.57 g
per fruit) than the control and cold-stressed groups (1.94 ± 0.73 and

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T. Mesa et al.
3.2. Plant physiological response to temperature stress
Regarding the water status, there were no differences in RWC
(Fig. 2A) but there were in H (Fig. 2B) as the leaflets from the heat stress
group had lower H (5.74 ± 1.15 gwater/g dry weight) than the other two
groups (6.35 ± 0.87 and 6.44 ± 1.09 gwater/g dry weight, respectively),
particularly since the fourth week from the start of the treatment.
About the chlorophyll fluorescence (Fig. 2C), the two stressed groups
had their Fv/Fm slightly diminished in contrast to the control group.
Some individuals reached minimums of 0.67 for the heat-stressed group
and 0.69 for the cold-stressed group. However, none of the groups had
mean values below the established threshold of 0.75 neither between
treatments nor within time.
Leaflet biomass and leaflet area (Fig. 2D and E) did not show any
differences because of the temperature treatments during the duration of
the study. On the contrary, when focusing on FMA (Fig. 2F), a significant
difference can be observed between the heat and the cold stress group,
being the latter one a 16.19% lower than the former one.
Total chlorophyll, total carotenoids, and the carotenoids/chlorophyll
ratio (Fig. 3A, C and 3D) presented differences within time but there
were no differences between treatments. However, the chlorophyll a/b
ratio (Fig. 3B) did present significant differences between treatments as
it was a 10.66% higher in the cold-stressed group than in the heat-
stressed group. Therefore, photosynthetic pigments were not highly
affected by temperature stress.
In contrast, tocochromanols did show significant differences because
Fig. 2. Variations in the physiological status of tomato leaves in heat and cold stress groups compared to controls. (A) Relative water content (RWC), (B) Hydration
(H), (C) Maximum efficiency of photosystem II; FvFm, (D) Leaflet biomass, (E) Leaflet area and (F) Leaflet mass per area. Data are mean of n = 6 ± SE. P values of
two-way mixed ANOVA of repeated measures are shown in the inlets and P values > 0.05 were considered as not significant (NS).
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Journal of Plant Physiology 268 (2022) 153581
of the treatments. From all the different forms of tocochromanols, only
α-tocopherol and plastochromanol-8 (PC-8) were detected in tomato
leaves in all three treatments. In both α-tocopherol and PC-8 (Fig. 4A
and B), the heat-stressed group had significantly higher levels than
control group presenting an increase of 41.52% and 155.77% of
α-tocopherol and PC-8, respectively. The cold-stressed group did not
show any differences with the control group. When α-tocopherol is
presented based on the chlorophyll content (Fig. 4C), there are no dif­
ferences between the heat-stressed and the cold-stressed group while
PC-8 on chlorophyll basis follow the same pattern as described before for
this tocochromanol form.
3.3. Impact of the temperature treatments on fruit quality
Temperature treatments had a significant impact on total soluble
solids (TSS), total acidity (TA) and the TSS/TA ratio (Fig. 5C, D and 5E).
TSS was increased by a 34.59% and a 77.44% in cold and heat-stressed
groups compared to control group, respectively. TA was only affected by
heat stress decreasing by a 34.12%. Regarding the ratio TSS/TA, we can
observe that it is increased in the heat-stressed group although the
posthoc test does not show significant differences between the groups.
Neither H nor lycopene contents were affected by either of the two
treatments (Fig. 5A and B). From all tocochromanol forms, α-tocopherol,
γ-tocopherol and plastochromanol-8 (PC-8) were detected in tomato
fruits (Fig. 6) together with tocotrienols traces (data not shown). None of
the treatments had an effect on the tocochromanols contents. On the
T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581

Fig. 3. Variations in the content of photosynthetic pigments of tomato leaves in heat and cold stress groups compared to controls. (A) Chlorophyll a+b, (B)
Chlorophyll a/b ratio (Chl a/b), (C) Total carotenoids and (D) Carotenoids/chlorophylls ratio (Car/Chl). Data are mean of n = 6 ± SE. P values of two-way mixed
ANOVA of repeated measures are shown in the inlets and P values > 0.05 were considered as not significant (NS).

Fig. 4. Foliar tocochromanols variations in heat and cold stress groups compared to controls. (A) α-tocopherol, (B) Plastochromanol-8 (PC-8), (C) α-tocopherol per
chlorophyll a+b, and (D) PC-8 per chlorophyll a+b. Data are mean of n = 6 ± SE. P values of two-way mixed ANOVA of repeated measures are shown in the inlets
and P values > 0.05 were considered as not significant (NS).

contrary, vitamin C presented significant differences due to the different
temperature treatments. The heat-stressed group presented significantly
higher content of AA (20.00 ± 1.46 mg/g dry weight) than the control
group (13.96 ± 1.24 mg/g dry weight) (Fig. 7A). However, the oxidized
form DHA did not show any changes (Fig. 7B). The heat-stressed group
presented an increase of 44.14% of total ascorbate content (Fig. 7C)
compared to the control group while the cold-stressed group presented
no differences. Regarding the redox state (Fig. 7D), no significant dif­
ferences were observed between the different treatments.
4. Discussion
The upcoming climate change presents a great challenge for plant
growth and development being extremes temperatures among the major

5
T. Mesa et al.
Fig. 5. Fruit quality variations in heat and cold stress groups compared to controls. (A) Hydration (H), (B) Lycopene, (C) Total soluble solids (TSS), (D) Total acidity
(TA) and (E) TSS/TA ratio are shown. Data are mean of n = 6 ± SE. P values of one-way ANOVA are shown in the inlets and P values > 0.05 were considered as not
significant (NS). Different letters represent differences between temperature treatments.
environmental limitations to crop productivity (Ashraf and Foolad,
2007). Extreme temperature events, such as frost, chill and heat waves,
are projected to become more intense and more frequent (Hatfield and
Prueger, 2015), thus it is of great importance to understand the possible
impacts on plant growth and development and the mechanisms that
plants possess to cope with and adapt to them. Previous studies using
other tomato varieties have shown their sensitivity to temperatures
below 12 ◦ C and above 32 ◦ C (Sato et al., 2001; Liu et al., 2012). Here,
we showed that Micro-Tom variety is particularly sensitive to temper­
atures above 30 ◦ C. Heat-stressed plants suffered a decrease in produc­
tion, while the cold-stressed plants showed no difference compared to
the control group. When plants face heat stress, their reproduction is
highly affected as high temperatures cause a decrease in the number of
fruit set, pollen viability and the number of released pollen grains (Sato
et al., 2006). In addition, with higher temperatures, there is also an
increase in flower abscission and thus a decrease in yield (Alsamir et al.,
2021). Furthermore, it has been shown that high temperatures accel­
erate ripening so that, in general, the average weight of harvested fruit is
usually reduced (Adams et al., 2001; Ruiz-Nieves et al., 2021). Despite
having a decreased total yield and an accelerated ripening, in our study,
the fresh weight of the ripe tomatoes of the heat stress group was higher
than that of the control group. This, as suggested by Hernández et al.
(2018), may be related to the increase in flower abortion to compensate
for the weight loss by temperature stress. Previous studies have shown
that yield is also highly affected by low temperatures (Fernandez-Muñoz
et al., 1995; Lozano et al., 1998). Under these conditions, tomato plants
produce flowers showing alterations in the number, morphology and
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Journal of Plant Physiology 268 (2022) 153581
pattern of fusion of floral organs in addition to reductions in final pro­
duction both in terms of the number of fruits and total yield (Lozano
et al., 1998; Meena et al., 2018). The latter is associated with slower CO2
fixation and partitioning of photosynthates of fruit (Meena et al., 2018).
In our study, however, no differences in yield were observed using the
micro-Tom variety between the control group and the cold-stressed
group. This suggests that the cold-stressed tomato plants were able to
acclimate to the induced stress. Many crops of tropical or subtropical
origin, such as cotton, maize, rice and tomato, are chilling-sensitive
(Barrero-Gil et al., 2016). In particular, several tomato varieties are
very sensitive to temperatures below 10–12 ◦ C (Lyons, 1973). However,
previous studies have shown that prior incubation of tomato plants at
suboptimal growth (10 ◦ C) temperatures alleviate chilling injury
symptoms via protective mechanisms such as the accumulation of
compatible solutes, the activation of antioxidant systems (including
enhanced flavonoids and anthocyanins contents and ascorbate peroxi­
dase and superoxide dismutase activities) and the readjustment of the
photosynthetic machinery (Barrero-Gil et al., 2016). In our study, the
acclimation was made by subjecting the plants to cold stress and re­
covery cycles of 3 and 4 days, respectively.
Apart from the differences in production, the plants showed varia­
tions in their physiological state due to the different temperatures. The
decrease of chlorophyll content may be an adaptive response to a
decreased H in heat-stressed plants since a reduction of chlorophylls
entails a decrease in energy absorption and, therefore, lower leaf heating
(Berova et al., 2009). Moreover, the phytol obtained from chlorophyll
degradation can serve as a substrate for the synthesis of tocopherols,
T. Mesa et al.
Fig. 6. Fruit tocochromanols variations in heat and cold stress groups
compared to controls. (A) α-tocopherol, (B) γ-tocopherol and (C)
plastochromanol-8 (PC-8) are shown. Data are mean of n = 6 ± SE. P values of
one-way ANOVA are shown in the inlets and P values > 0.05 were considered as
not significant (NS).
which are involved in protection against oxidative stress (vom Dorp
et al., 2015). In our study, heat-stressed plants presented higher contents
of α-tocopherol and PC-8. As previously described in non-acclimated
tomatoes, the increased concentration of α-tocopherol may be due to
an increased requirement for lipid antioxidants caused by heat stress
(Spicher et al., 2016). Furthermore, the increase in PC-8 may also
indicate a protective role in thylakoid membranes as it is described as a
quencher of singlet oxygen (Kruk et al., 2014; Fleta-Soriano and
Munné-Bosch, 2017). Moreover, it has been previously described that
α-tocopherol plays a role in retrograde signalling in the acquisition of
heat tolerance (Fang et al., 2019; see also Munné-Bosch, 2019).
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Journal of Plant Physiology 268 (2022) 153581
Therefore, the increase in tocochromanols may be exerting not only a
stress sensing and signalling function, but also an antioxidant protective
role allowing the acclimation of heat-stressed plants to high tempera­
tures avoiding damage in PSII and promoting the survival of the plant.
Fruit quality in tomatoes involves different parameters including
physical appearance, firmness, flavour and nutritive value (Jones and
Scott, 1983). Lycopene content is an important parameter to evaluate
fruit colour since it is the principal pigment responsible for it in ripe
tomatoes (Shi and Le Maguer, 2000). Some studies have previously
shown that heat stress causes a decrease in lycopene contents although
the percentage of reduction of lycopene is highly dependent on the va­
riety (Vijayakumar et al., 2021). In our study, no differences between
temperatures were observed in lycopene contents suggesting that
Micro-Tom variety does not show high lycopene variations because of
high temperatures. A similar situation happens with cold stress, since it
has also been shown to decrease lycopene contents in other varieties
(Khan et al., 2015; Meena et al., 2018) and, as it happened with heat
stress, this decrease was not observable in our study, suggesting that
again the variety has an important impact on the response. Furthermore,
sugars, acids, and their interactions are important to the overall flavour
of tomatoes (Gierson and Kader, 1986). Temperature influences both
transport and storage from source to sink during fruit development and
the biochemical transformation during fruit ripening (Guichard et al.,
2001). TSS increased with either of the treatments while TA decreased
with heat stress. These results are in accordance with the tendency
presented in the results of Gautier et al. (2008) that showed that an
increase from 21 to 26 ◦ C transiently increased TSS and reduced TA in
off-plant ripened tomatoes. This contrast with other studies that showed
an increase in both TSS and TA because of an increased temperature of
36 ± 2 ◦ C (Vijayakumar et al., 2021) or 40 ± 2 ◦ C (Lokesha et al., 2019)
in on-plant ripened tomatoes. Lowering the temperature has been shown
to either decrease TSS (Meena et al., 2018), yet these results were ob­
tained from a field experiment with no controlled ambient temperature
where the average minimum temperatures were below 10 ◦ C for 4
months out of the two years of duration of the experiment, or maintain
TSS concentration (Fleisher et al., 2006), where low temperature
treatment was done by lowering the temperature down to 16 ◦ C/11 ◦ C
for two weeks and then allowing the recovery of the plants for one
month.
When analyzing the tocochromanol contents in tomato fruits, only
three forms where detected, α-tocopherol, γ-tocopherol and PC-8. Heat
and cold stress did not significantly alter neither of the three tocochro­
manol forms. These results contrast with previous studies that described
how fruit tocochromanols may be altered by changing temperatures,
either decreasing α-tocopherol content because of cold temperatures
(Meena et al., 2018), or increasing it due to high temperatures (Almeida
et al., 2020). The AA acts as an antioxidant that eliminates reactive
oxygen species, and most particularly hydrogen peroxide (Hernández
et al., 2018). Total ascorbate was shown to be higher in heat-stressed
plants in comparison to the control group mainly because of an in­
crease in AA content while no differences were observed for DHA and
the ascorbate redox state. In previous studies, Gautier et al. (2008)
showed that an increase in temperature reduced ascorbate concentra­
tions when the stress was applied to harvested mature green fruits. In
contrast, Hernández et al. (2018) carried out an experiment analysing
the concentration of vitamin C in tomato when heat stress was applied at
different developmental stages in plant-ripened fruits and found higher
vitamin C in tomatoes when plants were subjected to the stress from
flowering, which is in agreement with our results. Despite high tem­
peratures may limit ascorbate accumulation as its synthesis is reduced
and its degradation favoured by oxidation (Rosales et al., 2006; Gautier
et al., 2008; Hernández et al., 2018), the increase in vitamin C con­
centration is probably because of a protective mechanism of the
heat-stressed fruits against an increase in ROS concentration. Indeed,
the ripening process itself produces an increase in ROS concentration
(Ioannidi et al., 2009) and heat-stressed fruits ripened faster than the
T. Mesa et al.
Fig. 7. Fruit ascorbate variations in heat and cold stress groups compared to controls. (A) Ascorbic acid, (B) Dehydroascorbic acid (DHA), (C) Total ascorbate and (D)
% Redox state are shown. Data are mean of n = 6 ± SE. P values of one-way ANOVA are shown in the inlets and P values > 0.05 were considered as not significant
(NS). Different letters represent differences between temperature treatments.
other two groups suggesting that a higher accumulation of ROS may be
occurring, thus heat-stressed tomatoes may increase their vitamin C
levels as a defensive mechanism to counteract enhanced ROS
production.
Micro-Tom is known as a convenient model system for research on
different fields such as physiology, agronomy and genetics, hence, un­
derstanding its responses against different environmental conditions is
of great importance even though it is not used as a commercial variety.
This cultivar’s phenotype is mainly due to at least three mutations: self-
pruning (which produces a determinate phenotype), dwarf (responsible
for the small plant size as a result of a reduction of brassinosteroids (BR)
content) and a still uncharacterized mutation suggested to be on the
miniature allele (which would contribute to the small plant size) (Martí
et al., 2006; Campos et al., 2010). Micro-Tom mutations have been
previously presented as a concern considering their potential influence
on the different results (Campos et al., 2010). Micro-Tom is a mild BR
mutant and it has been proven that dwarf mutants have reduced levels of
active BR in vegetative tissues and normal levels in fruits (Nomura et al.,
2005; Carvalho et al., 2011). However, these reduced levels of BR could
be interfering with our main results, if we were to compare them with
other tomato cultivars. BRs have been previously seen to reduce the
effects of thermal stresses by increasing the accumulation of heat-shock
proteins, increasing the yield due to an increase in fruit number and
increasing the activities of antioxidant enzymes (Dhaubhadel et al.,
1999, 2002; Ogweno et al., 2008). BRs are also involved in cold stress
responses since they have the capability to uncouple cold stress toler­
ance from trade-offs in terms of growth and yield (Ramirez and Pop­
penberger, 2020). Thus, the thermal impact observed in our study,
mainly on fruit yield and antioxidant response, could be overestimated if
we were to extrapolate them to other varieties with higher BRs content.
5. Conclusion
Overall, we have seen that heat and cold stress prompted a differ­
ential response in plants and their fruits. Both treatments caused only
moderate stress in leaves since parameters such as Fv/Fm or chlorophyll
8
Journal of Plant Physiology 268 (2022) 153581
content were not highly affected. In contrast, plant productivity was
highly affected in heat-stressed plants suggesting that warmer temper­
atures caused by climate change would have a negative effect on tomato
productivity. Heat stressed plants increased the contents of antioxidants,
such as tocochromanols in leaves and ascorbic acid in fruits, as a
mechanism to confront the stress. Altogether, heat stress improved fruit
quality in terms of total soluble solids and vitamin C, while cold stress
improved total soluble solids contents, although to a lower extent. It is
suggested that temperature modulation may be used as an approach to
improve tomato quality, most particularly cold temperature, which did
not negatively influence production. Further studies are however
needed to confirm the validity of this approach in commercial and non-
dwarf tomato varieties, including as well additional measurements
dealing with tomato fruit volatiles and flavor.
CRediT authorship contribution statement
Tania Mesa: Conceptualization, Methodology, Software, Validation,
Formal analysis, Investigation, Data curation, Writing – original draft,
Writing – review & editing, Visualization, Supervision. Javier Polo:
Resources, Funding acquisition, Writing – original draft, All authors
have read and agreed to the published version of the manuscript. Alba
Arabia: Methodology, Investigation, Writing – original draft, Method­
ology, Investigation, Software, Writing – original draft. Vicent Caselles:
Resources, Software. Sergi Munné-Bosch: Conceptualization, Valida­
tion, Resources, Writing – original draft, Writing – review & editing,
Supervision, Project administration, Funding acquisition, Formal anal­
ysis, Data curation.
Declaration of competing interest
The authors declare no conflict of interest.
T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581

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