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Differential Physiological Response To Heat and Cold Stress of Tomato Plants and Its Implication On Fruit Quality
Differential Physiological Response To Heat and Cold Stress of Tomato Plants and Its Implication On Fruit Quality
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 challenges for agriculture worldwide, particularly high and low tem
peratures (Meena et al., 2018). These projections highlight the relevance
Recent studies have highlighted that the intensity, frequency, and of understanding the repercussions of extreme temperatures on plant
duration of extreme weather events have been changing in the last few growth, development and yield in order to evaluate possible future
years, particularly, temperature extremes (Ummenhofer and Meehl, strategies to confront crop damages.
2017). According to the Intergovernmental Panel on Climate Change Tomato plants (Solanum lycopersicum L.) are endemic to the Andean
(Collins et al., 2013), there will be more records of high temperatures region, currently comprising Peru, Colombia, Ecuador and Bolivia
than cold temperatures in a warmer climate. However, it is also stated (Gerszberg et al., 2015). Tomato plants arrived in Europe in the 16th
that cold extremes will continue to occur in a warmer climate. Plant century and subsequently their cultivation spread worldwide (Kimura
growth, development, productivity and quality are highly dependent on and Sinha, 2008). Today, they are one of the most cultivated crops and
temperature and each species has a temperature range along with an their fruits are consumed worldwide with a production of more than 180
optimum temperature for each of these processes (Hatfield et al., 2014; million tonnes in a cultivation area of 5.03 million hectares (FAOSTAT,
Hatfield and Prueger, 2015). As a result, climate change entails great 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. Journal of Plant Physiology 268 (2022) 153581
States, Turkey and India, while Spain is in the eighth place (FAOSTAT, seedlings were transferred to 1 L pots in a climate-controlled growth
2017). There are currently more than 5000 different varieties of to chamber at a daily mean temperature and relative humidity of 22/22 ◦ C
matoes (Kimura and Sinha, 2008; Gerszberg et al., 2014). Tomato is an and 60% (day/night). Then, on December 4th, when temperature
herbaceous plant that can grow up to 3 m high with a sympodial hairy treatments started, plants were separated into three groups of 6 plants
stem and its leaves are composed of an odd number of leaflets (Costa each (n = 6). The control group was located in a climate-controlled
et al., 2017; OECD, 2017). Their bright yellow flowers are hermaphro growth chamber at a daily mean temperature and relative humidity of
dite and can be self-pollinated (Ozores-Hampton, 2014). 22/22 ◦ C and 60% (day/night); the heat-stressed group at 32/22 ◦ C and
Tomato fruits are red berries of variable size depending on the va 60%; and the cold-stressed group at 22/4 ◦ C and 60% (3 days per week)
riety (OECD, 2017). The tomato fruit consists of several parts such as the and 22/22 ◦ C and 60% (4 days per week). All the plants were located
pericarp, which contains the exocarp, the mesocarp and the endocarp; over trays filled permanently with Hoagland nutrient solution.
the placenta, formed by parenchyma tissue in the centre of the fruit and Leaf samplings were made at midday at 0, 1, 2, 4, 6, 8, 10 and 12
the locular cavity where the seeds are surrounded by a mucilaginous gel weeks since the start of the treatment (on December 4th). In each
(McCormack, 2004; Rančić et al., 2010). They are climacteric fruits with sampling, two leaflets, marked since the beginning, were selected: one
six different stages of development and ripening from immature green to was used to measure leaf growth and hydration and the other was frozen
overripe (Takizawa et al., 2014). The tomato fruit stands out for its in liquid N2 and stored at − 80 ◦ C for subsequent biochemical analyses.
organoleptic characteristics and nutritional value, being a great source Fruit samplings were made at the time point where all the plants
of lycopene, vitamins and minerals (Meena et al., 2018). Furthermore, from one specific treatment had at least 2 ripe tomatoes (or Stage V, as
tomatoes are also of great importance for research since it is a model described by Takizawa et al., 2014). The samplings were performed on
species whose genome has already been sequenced (The Tomato February 1st, 2021, for the control group, February 2nd, for the
Genome Consortium, 2012). cold-stressed group and February 16th, for the heat-stressed group. All
Some plants have the ability to adjust their growth or senescence of the ripe tomatoes of each plant were harvested in each sampling: one
shoots or roots to upregulate or downregulate individual proteins or was frozen in liquid N2 and stored at − 80 ◦ C for subsequent biochemical
whole metabolic pathways in order to acclimate to stresses (Demmi analyses. The rest were used to analyse quality parameters.
g-Adams et al., 2008). Temperature stress often has a negative effect on
cellular homeostasis, plant metabolism and major physiological pro 2.2. Chlorophyll fluorescence, leaf morphology and water status
cesses increasing the accumulation of reactive oxygen species (ROS)
(Suzuki and Mittler, 2006). To scavenge these ROS, non-enzymatic an The maximum efficiency of photosystem II (Fv/Fm), leaflet mass per
tioxidants such as ascorbic acid (AA) and tocochromanols are essential area ratio (FMA), hydration (H) and relative water content (RWC) of one
(Suzuki and Mittler, 2006; Falk and Munné-Bosch, 2010). Ascorbic acid leaflet per plant were measured in six plants per treatment at each
(or vitamin C) protects cellular components from free radicals generated sampling point. Fv/Fm was measured with a fluorimeter Mini-PAM II
in the aqueous phase turning into its oxidized form, dehydroascorbic (Photosynthesis Yield Analyser, Walz, Germany) in leaves sampled and
acid (DHA) (Beyer, 1994). Tocochromanols, particularly, α-tocopherol adapted to dark conditions for 1 h. The H was obtained following the
(or vitamin E), scavenge singlet oxygen and lipid peroxyl radicals thus formula [(FW - DW)/DW] and the RWC was obtained using the formula
preventing the propagation of lipid peroxidation in membranes [(FW - DW)/(TW - DW) x 100], where FW is the fresh weight, TW is the
(Munné-Bosch and Alegre, 2002). However, it is of great importance not turgid weight (after rehydrating samples for 24 h in the dark at 4 ◦ C) and
to forget that ROS also act in stress signalling thus indicating that the DW is the dry weight (after oven-drying samples at 75 ◦ C until constant
role of antioxidants is not to fully eliminate ROS but rather regulate their weight). Leaflet area was measured with a flat-bed scanner and an image
concentration (Arrigoni and De Tulio, 2002). processor (ImageJ 1.52p, National Institutes of Health, Bethesda, MD,
Many crops of topical/subtropical origin such as cotton, maize or United States). The FMA was calculated as DW/Foliar area.
tomato, are chilling-sensitive (Lyons, 1973). Tomato plants are sensitive
to temperatures below 12 ◦ C but also temperatures above 32 ◦ C (Sato 2.3. Photosynthetic pigments quantification
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 For the quantification of chlorophylls and carotenoids, 50 mg of
Barrero-Gil et al. (2016), showing acclimation of tomato plants at 10 ◦ C frozen leaves were ground in liquid nitrogen and extracted with cold
prior to exposure at 4 ◦ C. For heat stress, exposure to elevated temper methanol +0.01% BHT (w/v) using ultrasonication (Branson 2510 ul
atures for a short term (heat shocks) have shown to have no positive trasonic cleaner, Bransonic, Danbury, CT, USA). The extract was then
effects on tomato growth or development (Abdelmageed and Gruda, centrifuged for 10 min at 4 ◦ C and 13000 rpm, and the supernatant was
2007). However, tomatoes have multiple mechanisms to survive under collected. The pellet was re-extracted until colourless, pooling at the end
heat stress (Alsamir et al., 2021). all the supernatants obtaining a final volume of 1.2 mL.
Although multiple studies have previously described some of the Photosynthetic pigments, including chlorophyll a and b and total
responses of tomato plants to heat and cold stress, none has compared carotenoids, were analysed using UV/Visible spectroscopy of double
both low and high temperature stresses in plant and its on-plant ripened beam using a CE Aquarius UCE7400 (Cecil Instruments Ltd, Cambridge,
fruits in the same study. Thus, the main purpose of this study was to UK). The absorbance of the supernatants was read at 470 nm, 653 nm,
evaluate the response of tomato plants in terms of growth, development, 666 nm and 750 nm. Chlorophyll and carotenoids content were calcu
yield and fruit quality to heat and cold stress under controlled lated following the equations developed by Lichtenthaler and Wellburn
conditions. (1983).
2.1. Experimental design and samplings Tocochromanol analyses, including the four different tocopherol
homologues, the four tocotrienol homologues and plastochromanol-8
Seeds of tomato plants (Solanum lycopersicum cv. Micro-Tom) were (PC-8), were followed as described by Amaral et al. (2005). 50 mg of
obtained from the Experimental Field Facilities of the University of ground frozen leaves or 100 mg of ground frozen fruit were extracted
Barcelona (Barcelona, NE, Spain). Seeds were sown on October 19th, with methanol containing 0.01% BHT (w/v) and 5 ppm (w/v) of tocol as
2020, in a seedbed and placed in a growth chamber (16 h light/8 h dark, an internal standard. Extraction was performed using 30 min of ultra
at 21.9 ◦ C and 65% relative humidity). On November 19th, 2020, 18 sonication and then the extract was centrifuged for 10 min at 4 ◦ C and
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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.
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].
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. Journal of Plant Physiology 268 (2022) 153581
3.2. Plant physiological response to temperature stress of the treatments. From all the different forms of tocochromanols, only
α-tocopherol and plastochromanol-8 (PC-8) were detected in tomato
Regarding the water status, there were no differences in RWC leaves in all three treatments. In both α-tocopherol and PC-8 (Fig. 4A
(Fig. 2A) but there were in H (Fig. 2B) as the leaflets from the heat stress and B), the heat-stressed group had significantly higher levels than
group had lower H (5.74 ± 1.15 gwater/g dry weight) than the other two control group presenting an increase of 41.52% and 155.77% of
groups (6.35 ± 0.87 and 6.44 ± 1.09 gwater/g dry weight, respectively), α-tocopherol and PC-8, respectively. The cold-stressed group did not
particularly since the fourth week from the start of the treatment. show any differences with the control group. When α-tocopherol is
About the chlorophyll fluorescence (Fig. 2C), the two stressed groups presented based on the chlorophyll content (Fig. 4C), there are no dif
had their Fv/Fm slightly diminished in contrast to the control group. ferences between the heat-stressed and the cold-stressed group while
Some individuals reached minimums of 0.67 for the heat-stressed group PC-8 on chlorophyll basis follow the same pattern as described before for
and 0.69 for the cold-stressed group. However, none of the groups had this tocochromanol form.
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 3.3. Impact of the temperature treatments on fruit quality
differences because of the temperature treatments during the duration of
the study. On the contrary, when focusing on FMA (Fig. 2F), a significant Temperature treatments had a significant impact on total soluble
difference can be observed between the heat and the cold stress group, solids (TSS), total acidity (TA) and the TSS/TA ratio (Fig. 5C, D and 5E).
being the latter one a 16.19% lower than the former one. TSS was increased by a 34.59% and a 77.44% in cold and heat-stressed
Total chlorophyll, total carotenoids, and the carotenoids/chlorophyll groups compared to control group, respectively. TA was only affected by
ratio (Fig. 3A, C and 3D) presented differences within time but there heat stress decreasing by a 34.12%. Regarding the ratio TSS/TA, we can
were no differences between treatments. However, the chlorophyll a/b observe that it is increased in the heat-stressed group although the
ratio (Fig. 3B) did present significant differences between treatments as posthoc test does not show significant differences between the groups.
it was a 10.66% higher in the cold-stressed group than in the heat- Neither H nor lycopene contents were affected by either of the two
stressed group. Therefore, photosynthetic pigments were not highly treatments (Fig. 5A and B). From all tocochromanol forms, α-tocopherol,
affected by temperature stress. γ-tocopherol and plastochromanol-8 (PC-8) were detected in tomato
In contrast, tocochromanols did show significant differences because fruits (Fig. 6) together with tocotrienols traces (data not shown). None of
the treatments had an effect on the tocochromanols contents. On the
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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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 no differences. Regarding the redox state (Fig. 7D), no significant dif
temperature treatments. The heat-stressed group presented significantly ferences were observed between the different treatments.
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 4. Discussion
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) The upcoming climate change presents a great challenge for plant
compared to the control group while the cold-stressed group presented growth and development being extremes temperatures among the major
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T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581
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, pattern of fusion of floral organs in addition to reductions in final pro
2007). Extreme temperature events, such as frost, chill and heat waves, duction both in terms of the number of fruits and total yield (Lozano
are projected to become more intense and more frequent (Hatfield and et al., 1998; Meena et al., 2018). The latter is associated with slower CO2
Prueger, 2015), thus it is of great importance to understand the possible fixation and partitioning of photosynthates of fruit (Meena et al., 2018).
impacts on plant growth and development and the mechanisms that In our study, however, no differences in yield were observed using the
plants possess to cope with and adapt to them. Previous studies using micro-Tom variety between the control group and the cold-stressed
other tomato varieties have shown their sensitivity to temperatures group. This suggests that the cold-stressed tomato plants were able to
below 12 ◦ C and above 32 ◦ C (Sato et al., 2001; Liu et al., 2012). Here, acclimate to the induced stress. Many crops of tropical or subtropical
we showed that Micro-Tom variety is particularly sensitive to temper origin, such as cotton, maize, rice and tomato, are chilling-sensitive
atures above 30 ◦ C. Heat-stressed plants suffered a decrease in produc (Barrero-Gil et al., 2016). In particular, several tomato varieties are
tion, while the cold-stressed plants showed no difference compared to very sensitive to temperatures below 10–12 ◦ C (Lyons, 1973). However,
the control group. When plants face heat stress, their reproduction is previous studies have shown that prior incubation of tomato plants at
highly affected as high temperatures cause a decrease in the number of suboptimal growth (10 ◦ C) temperatures alleviate chilling injury
fruit set, pollen viability and the number of released pollen grains (Sato symptoms via protective mechanisms such as the accumulation of
et al., 2006). In addition, with higher temperatures, there is also an compatible solutes, the activation of antioxidant systems (including
increase in flower abscission and thus a decrease in yield (Alsamir et al., enhanced flavonoids and anthocyanins contents and ascorbate peroxi
2021). Furthermore, it has been shown that high temperatures accel dase and superoxide dismutase activities) and the readjustment of the
erate ripening so that, in general, the average weight of harvested fruit is photosynthetic machinery (Barrero-Gil et al., 2016). In our study, the
usually reduced (Adams et al., 2001; Ruiz-Nieves et al., 2021). Despite acclimation was made by subjecting the plants to cold stress and re
having a decreased total yield and an accelerated ripening, in our study, covery cycles of 3 and 4 days, respectively.
the fresh weight of the ripe tomatoes of the heat stress group was higher Apart from the differences in production, the plants showed varia
than that of the control group. This, as suggested by Hernández et al. tions in their physiological state due to the different temperatures. The
(2018), may be related to the increase in flower abortion to compensate decrease of chlorophyll content may be an adaptive response to a
for the weight loss by temperature stress. Previous studies have shown decreased H in heat-stressed plants since a reduction of chlorophylls
that yield is also highly affected by low temperatures (Fernandez-Muñoz entails a decrease in energy absorption and, therefore, lower leaf heating
et al., 1995; Lozano et al., 1998). Under these conditions, tomato plants (Berova et al., 2009). Moreover, the phytol obtained from chlorophyll
produce flowers showing alterations in the number, morphology and degradation can serve as a substrate for the synthesis of tocopherols,
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T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581
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T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581
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 content were not highly affected. In contrast, plant productivity was
occurring, thus heat-stressed tomatoes may increase their vitamin C highly affected in heat-stressed plants suggesting that warmer temper
levels as a defensive mechanism to counteract enhanced ROS atures caused by climate change would have a negative effect on tomato
production. productivity. Heat stressed plants increased the contents of antioxidants,
Micro-Tom is known as a convenient model system for research on such as tocochromanols in leaves and ascorbic acid in fruits, as a
different fields such as physiology, agronomy and genetics, hence, un mechanism to confront the stress. Altogether, heat stress improved fruit
derstanding its responses against different environmental conditions is quality in terms of total soluble solids and vitamin C, while cold stress
of great importance even though it is not used as a commercial variety. improved total soluble solids contents, although to a lower extent. It is
This cultivar’s phenotype is mainly due to at least three mutations: self- suggested that temperature modulation may be used as an approach to
pruning (which produces a determinate phenotype), dwarf (responsible improve tomato quality, most particularly cold temperature, which did
for the small plant size as a result of a reduction of brassinosteroids (BR) not negatively influence production. Further studies are however
content) and a still uncharacterized mutation suggested to be on the needed to confirm the validity of this approach in commercial and non-
miniature allele (which would contribute to the small plant size) (Martí dwarf tomato varieties, including as well additional measurements
et al., 2006; Campos et al., 2010). Micro-Tom mutations have been dealing with tomato fruit volatiles and flavor.
previously presented as a concern considering their potential influence
on the different results (Campos et al., 2010). Micro-Tom is a mild BR CRediT authorship contribution statement
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., Tania Mesa: Conceptualization, Methodology, Software, Validation,
2005; Carvalho et al., 2011). However, these reduced levels of BR could Formal analysis, Investigation, Data curation, Writing – original draft,
be interfering with our main results, if we were to compare them with Writing – review & editing, Visualization, Supervision. Javier Polo:
other tomato cultivars. BRs have been previously seen to reduce the Resources, Funding acquisition, Writing – original draft, All authors
effects of thermal stresses by increasing the accumulation of heat-shock have read and agreed to the published version of the manuscript. Alba
proteins, increasing the yield due to an increase in fruit number and Arabia: Methodology, Investigation, Writing – original draft, Method
increasing the activities of antioxidant enzymes (Dhaubhadel et al., ology, Investigation, Software, Writing – original draft. Vicent Caselles:
1999, 2002; Ogweno et al., 2008). BRs are also involved in cold stress Resources, Software. Sergi Munné-Bosch: Conceptualization, Valida
responses since they have the capability to uncouple cold stress toler tion, Resources, Writing – original draft, Writing – review & editing,
ance from trade-offs in terms of growth and yield (Ramirez and Pop Supervision, Project administration, Funding acquisition, Formal anal
penberger, 2020). Thus, the thermal impact observed in our study, ysis, Data curation.
mainly on fruit yield and antioxidant response, could be overestimated if
we were to extrapolate them to other varieties with higher BRs content. Declaration of competing interest
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
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T. Mesa et al. Journal of Plant Physiology 268 (2022) 153581
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