Selection of tomato landraces with high fruit yield and nutritional quality under elevated temperatures

Abstract

BACKGROUND
Global warming and extreme or adverse events induced by climatic fluctuations are an important threat for plants growth and agricultural production. Adaptability to environmental changes prevalently derives from a large set of genetic traits affecting physiological and agronomic parameters. Therefore, the identification of genotypes that are good yield performer at high temperatures is becoming increasingly necessary for future breeding programs. Here, we analyzed the performances of different tomato landraces grown under elevated temperatures in terms of yield and nutritional quality of the fruit. Finally, we evaluated the antioxidant and anti‐inflammatory activities of fruit extracts from the tomato landraces selected.

RESULTS
The tomato landraces analyzed here in a hot climate differed in terms of yield performance, physicochemical parameters of fruit (pH, titratable acidity, degrees Brix, firmness), bioactive compounds (ascorbic acid, carotenoids, and polyphenols), and anti‐inflammatory potential. Three of these landraces (named E30, E94, and PDVIT) showed higher fruit quality and nutritional value. An estimated evaluation index allowed identification of PDVIT as the best performer in terms of yield and fruit quality under high temperatures.

CONCLUSION
The analyses performed here highlight the possibility to identify new landraces that can combine good yield performances and fruit nutritional quality at high temperatures, information that is useful for future breeding programs. © 2020 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Full text

Research Article
Received: 31 October 2019 Revised: 30 January 2020 Accepted article published: 5 February 2020 Published online in Wiley Online Library: 29 February 2020
(wileyonlinelibrary.com) DOI 10.1002/jsfa.10312
Selection of tomato landraces with high fruit
yield and nutritional quality under elevated
temperatures
Aurelia Scarano,aFabrizio Olivieri,bCarmela Gerardi,aMarina Liso,c
Maurizio Chiesa,dMarcello Chieppa,c,e Luigi Frusciante,bAmalia Barone,b
Angelo Santinoa
*
and Maria Manuela Riganob
Abstract
BACKGROUND: Global warming and extreme or adverse events induced by climatic fluctuations are an important threat for
plants growth and agricultural production. Adaptability to environmental changes prevalently derives from a large set of
genetic traits affecting physiological and agronomic parameters. Therefore, the identification of genotypes that are good yield
performer at high temperatures is becoming increasingly necessary for future breeding programs. Here, we analyzed the per-
formances of different tomato landraces grown under elevated temperatures in terms of yield and nutritional quality of the
fruit. Finally, we evaluated the antioxidant and anti-inflammatory activities of fruit extracts from the tomato landraces selected.
RESULTS: The tomato landraces analyzed here in a hot climate differed in terms of yield performance, physicochemical param-
eters of fruit (pH, titratable acidity, degrees Brix, firmness), bioactive compounds (ascorbic acid, carotenoids, and polyphenols),
and anti-inflammatory potential. Three of these landraces (named E30, E94, and PDVIT) showed higher fruit quality and nutri-
tional value. An estimated evaluation index allowed identification of PDVIT as the best performer in terms of yield and fruit
quality under high temperatures.
CONCLUSION: The analyses performed here highlight the possibility to identify new landraces that can combine good yield per-
formances and fruit nutritional quality at high temperatures, information that is useful for future breeding programs.
© 2020 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of
Chemical Industry.
Supporting information may be found in the online version of this article.
Keywords: tomato; high temperature tolerance; yield performance; fruit quality; nutritional value
INTRODUCTION
One of the most important challenges facing us today is deal-
ing with global warming, which can greatly impact on crop
production and food accessibility. Together with water stress
and high salinity, temperatures and light fluctuations during
plant growth are the most important abiotic stresses that
plants have to face.
1
Tomato is one of the major cultivated crops worldwide and a
model system to study plant response to the changing environmen-
tal conditions. The optimal range of temperatures for tomato cultiva-
tion is between 25 and 30 °C during the day and 20 °Cduringthe
night.
2
However, tomato varieties or landraces can exhibit individual
differences in terms of yield performances, depending on the genetic
background and the adaptation to the environment in specificgeo-
graphic areas. In this context, the exploration of the natural variation
and the screening of genotypes and landraces that are good yield
performers at high temperatures may help to understand the mech-
anisms underlying high-temperature tolerance and can provide
agronomic traits and genetic diversity useful for breeding.
3
Increases in the average temperatures and UV radiation can
have a significant impact on plant growth and, consequently, on
crop yield and fruit quality. Indeed, different biochemical mecha-
nisms, including plastid biogenesis and pigments/secondary
*Correspondence to: A Santino, ISPA–CNR, Institute of Science of Food
Production, CNR Unit of Lecce, via Provinciale Lecce-Monteroni, 73100
Lecce, Italy. E-mail: angelo.santino@ispa.cnr.it
aISPA–CNR, Institute of Science of Food Production, CNR Unit of Lecce, Lecce, Italy
bDepartment of Agricultural Sciences, University of Naples Federico II, Naples, Italy
cNational Institute of Gastroenterology ‘S. De Bellis’, Institute of Research, Bari,
Italy
dBiotecgen S.r.l., Lecce, Italy
eDepartment of Immunology and Cell Biology, European Biomedical Research
Institute of Salerno (EBRIS), Salerno, Italy
© 2020 The Authors. Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and
reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
2791

metabolites synthesis, can be activated in plant cells in response
to abiotic stresses.
1,4–7
Since thermo-tolerance requires the mod-
ulation of biochemical pathways involved in reactive oxygen spe-
cies (ROS) detoxification, antioxidant compounds, including
carotenoids, ascorbic acid (AsA) and polyphenols, are accumu-
lated in response to heat stress.
8,9
Carotenoids can also contribute
to membranes fluidity and permeability in response to tempera-
ture fluctuations.
5,6
Indeed, these molecules can exert a protec-
tive role in photosynthetic membranes and play important roles
in structural stabilization, light harvesting, and photoprotection.
5
The increase in the biosynthesis of polyphenolic compounds
and flavonoids has also been reported following the exposure of
many plant species to UV radiation, making their accumulation
one of the most evolutionarily conserved responses to this type
of abiotic stress.
10,11
Polyphenolic compounds, AsA, and carotenoids are also rele-
vant for human health, since antioxidant and anti-inflammatory
properties have been described following their in vitro or in vivo
administration.
12–14
In particular, phenolic compounds may have
therapeutic roles in inflammation-based diseases and various
type of cancers.
15
Furthermore, ascorbic acid shows significant
antioxidant and electron donor capability and is able to protect
DNA from oxidation-induced damage.
15,16
Finally, it has been
demonstrated that carotenoids possess an apoptotic-inducing
effect in cancer cells and reduce oxidized low-density lipoprotein
cholesterol levels.
17
The health-promoting properties of these
bioactive compounds contribute to the nutritional value of crops
such as tomato and represent a parameter of preference in con-
sumer choice of food products. Indeed, some of these bioactive
compounds, such as AsA and carotenoids, cannot be synthesized
by animals and thus have to be introduced with the diet.
18
For
these reasons, the daily consumption of plant-derived food
enriched in these compounds has been highly promoted in the
last decade.
In this study, we analyzed the performances, in terms of final
yield and fruit quality on a set of ten tomato landraces showing
good performances when grown under elevated temperatures.
Their productivity and field performances under restrictive envi-
ronmental conditions were estimated. Moreover, the bioactive
compounds content and antioxidants/anti-inflammatory proper-
ties have been evaluated in extracts from ripe fruits from different
tomato landraces, with the final aim of identifying the best ones in
terms of both yield and nutritional fruit quality. Altogether, this
study highlights the possibility to select tomato landraces com-
bining desirable agronomic and nutritional traits, such as good
yield performances and high nutritionally active phytonutrients
content, for future applications in breeding programs.
MATERIALS AND METHODS
Plant materials
Plant material consisted of ten tomato indeterminate landraces
(listed in Table 1) and the control variety ‘Moneymaker’. In 2017
they were grown in Apulia (Pulsano, 40°2300300 N latitude,
17°2101700 E longitude), a region of southern Italy greatly devoted
to tomato cultivation and usually characterized by high tempera-
tures during the growing season. Seeds were sown in plateau
under a plastic-house in April, and seedlings were then trans-
planted in open field in June. Plants were distributed following a
complete randomized block design, with three replicate plots
per landrace and ten plants per replicate. For fruit quality and
nutritional traits analyses, ten fruits at the red ripe stage from at
least three plants from each replicate plot were collected at the
same time and pooled. Some traits were evaluated on fresh fruit,
and others on fruit frozen in liquid nitrogen and stored at −80 °C
until analysis. For yield determination, fruits at red ripe stage were
collected on the same day from all the plants for each replicate
plot. Total fruit number and fresh weight (FW) were measured to
allow yield evaluation per plant.
Quality traits evaluation
Physicochemical traits were evaluated on fresh fruit. The determi-
nation of pH was carried out by using a pH meter (Mettler-Toledo,
Milan, Italy), and the total acidity was determined by titrating
Table 1. List of the plant materials tested for production, quality, and nutritional traits under high temperature
Genotype Source Accession no. Common name
Country
of origin Collection site
Product
destination Fruit size Fruit shape
E7 CRA-ORT
a
Corbarino PC04 Italy Nocera (Salerno) Processing Small (25–30 g) Ovate
E8 CRA-ORT
a
Corbarino PC05 Italy Sant'Antonio
Abate (Salerno)
Processing Small (20–25 g) Elliptic
E17 CRA-ORT
a
Pantano Romanesco Italy Fondi (Latina) Fresh market Big (200–250 g) Flattened
E30 CRA-ORT
a
Sel PC07 Italy Pagani (Salerno) Processing Small (15–20 g) Ovate
E32 CRA-ORT
a
Sel PC16 Italy Nocera (Salerno) Fresh market Small (20–50 g) Ovate
E36 Campania
Region
a
Vesuvio Foglia Riccia Italy S. Vito (Naples) Fresh market/
processing
Small (25–30 g) Ovate
E53 TGRC LA0147 —Honduras Tegucigalpa
mercado
Fresh market Medium (80–100 g) Oblate
E76 TGRC LA4449 Black plum URSS —Processing Small (20–25 g) Ovate
E94 NPGS PI272890 1404 Guatemala Quetzaltenango,
Guatemala
nd Small (40–50 g) Irregular
PDVIT ARCA2010
a
Caramella Italy Scafati (Salerno) Fresh market/
processing
Small (10–15 g) Elliptic
‘Moneymaker’TGRC LA2706 Moneymaker Great Britain —Fresh market Medium (50–60 g) Circular
a
Germplasm collections maintained at Italian public institution.
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10 mL of tomato juice with a solution of 0.1 mol L
−1
sodium
hydroxide. A few drops of tomato juice were also used to estimate
the total soluble solids (degrees Brix) by adding them to the prism
plate of a refractometer (Hanna Instruments). Finally, the firmness
was measured by a penetrometer (PCE-PTR200 penetrometer,
Capannori, Italy) using an 8 mm tip. All extracts were from three
biological replicates, and three technical assays were carried out
on each biological repetition.
Extraction and detection of polyphenols
Whole tomato fruits were cut and frozen in liquid nitrogen, freeze-
dried, and finely ground. Samples of powder (200 mg) were
extracted twice in methanol:water 80:20 (v/v). The extracts were cen-
trifuged, and the supernatants were combined, filtered through a
0.22 μmfilter, and stored at −20 °C until use. Polyphenols were
detected at 320 nm by reversed-phase high-performance liquid
chromatography with diode array detector (RP-HPLC DAD) (Agilent
1100 HPLC system). Separation was performed on a C18 column
(5 UltraSphere, 80 Å pore, 25 mm), with a linear gradient from 20%
to 60% acetonitrile, in 55 min, with a flow of 1 mL min
−1
at 25 °C.
Concentrations were obtained by referring to calibration curves,
and results were expressed in micrograms per gram or milligrams
per gram (in the case of rutin and chlorogenic acid) of dried weight.
Carotenoids content
Freeze-dried tomato powder (50 mg) was added to 2 mL of 60%
potassium hydroxide, 2 mL of absolute ethanol, 1 mL of 1%
sodium chloride (NaCl), 5 mL of 0.05% butylated hydroxytoluene
in acetone. The mix was incubated at 60 °C for 30 min. A 1% solu-
tion of NaCl (15 mL) was added to the mix, and extractions were
performed with 15 mL hexane:ethyl acetate 9:1 (v/v). Extracts
were centrifuged, evaporated using a rotary evaporator, and col-
lected in 1 mL of ethyl acetate. Analyses were performed using
RP-HPLC DAD (Agilent 1100 HPLC system) according to the
method previously described.
19
AsA determination
AsA determinations were carried out by a colorimetric method with
modifications reported by Rigano et al.
20
Briefly, 500 mg of frozen
powder from tomato fruits was extracted with 300 μLof6%tri-
chloroacetic acid (TCA). The mixture was vortexed, incubated on
ice for 15 min, and centrifuged at 15 700×gfor 20 min. To 20 μL
of supernatant were added 20 μLof0.4molL
−1
phosphate buffer
(pH 7.4), 10 μL of double-distilled water, and 80 μL of color reagent
solution. This last solution was prepared by mixing solution A (31%
(w/v) phosphoric acid, 4.6% (w/v) TCA, and 0.6% (w/v) ferric chlo-
ride) with solution B (4% (w/v) 2,20-dipyridyl). These mixtures were
incubated at 37 °C for 40 min and measured at 525 nm using a
UV–visible spectrophotometer (NanoPhotometer™; Implen). All
extracts were from three biological replicates, and three technical
assays were carried out on each biological repetition. The concen-
tration was expressed in micrograms per gram FW.
Determination of antioxidant activity
2,20-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammo-
nium salt (ABTS; Sigma-Aldrich) radical cations were prepared by
mixing an aqueous solution of 2.45 mmol L
−1
potassium persul-
fate (final concentration) with an aqueous solution of 7 mmol L
−1
ABTS (final concentration) and allowed to stand in the dark at
room temperature for 12–16 h before use. The ABTS radical cation
solution was diluted in phosphate-buffered saline (PBS; pH 7.4) to
an absorbance of 0.40 at 734 nm. Trolox was used to prepare a
standard calibration curve (0–16 μmol L
−1
). After the addition of
200 μL of diluted ABTS to 10 μL of Trolox standard or extracts diluted
in PBS, in each well of a 96-well plate (Costar), the absorbance was
read at 734 nm 6 min after initial mixing using an Infinite200Pro plate
reader (Tecan). All extracts were from three biological replicates, and
three technical assays were carried out on each biological repetition.
The percentage absorbance inhibition at 734 nm was calculated as a
function of concentration of Trolox, and the Trolox equivalent antiox-
idant capacity (TEAC) value was expressed as Trolox equivalent (TE,
μmol) using Magellan v7.2 software.
Culture of dendritic cells and enzyme-linked
immunosorbent assay
Bone-marrow-derived dendritic cells (BMDCs) were obtained
from C57BL/6 mice, in agreement with national and international
guidelines, approved by the authors' institutional review board
(Organism for Animal Wellbeing –OPBA).
BMDCs were harvested as previously described
19
and plated in
Roswell Park Memorial Institute 1640 medium supplemented with
fetal bovine serum, antibiotics, recombinant mouse granulocyte
macrophage stimulating factor and recombinant mouse interleu-
kin (IL)-4 at 37°C in a humidified 5% carbon dioxide atmosphere.
BMDCs were treated with tomato methanol extracts (100 mg
lyophilized powder per milliliter, 1:25 final dilution), after adminis-
tration of lipopolysaccharide (LPS; 1 μgmL
−1
) at day 8 for 24 h.
BMDCs culture media were analyzed for IL-6 and IL-12 in triplicate
using an enzyme-linked immunosorbent assay (ELISA) kit as
described by the manufacturer (R&D Systems).
Data analysis
Values are expressed as mean plus/minus standard deviation (SD).
Group differences were analyzed and compared by paired two-
tailed Student's t-tests. Yield differences among the genotypes ana-
lyzed were determined using SPSS Package 6, version 15.0. Signifi-
cant different yields were determined by comparing mean values
through a factorial analysis of variance with Duncan post hoc test
at a significance level of 0.05. Spearman correlations were calcu-
lated to analyze co-occurrence and associations among all traits
measured. The P-values obtained for multiple tests were corrected
using the Benjamini and Hochberg false discovery rate (FDR). In
order to identify the landraces with a desirable combination of
traits, an evaluation index (EI) was estimated by assigning a score
to each trait, which was a maximum of 11 to a minimum of 1 des-
cending from the highest to the lowest value for all traits except
for pH, IL-6, and IL-12, where the maximum score (11) was assigned
to the lower value and the minimum score (1) to the highest value.
RESULTS AND DISCUSSION
Agronomic performances of tomato landraces under harsh
temperature conditions
A group of tomato landraces was previously selected for yield per-
formances under high temperatures in two regions of southern
Italy, Campania and Apulia, in 2016.
21
In the present study, we
decided to test them again under high temperatures in an open
field in the Apulia region in 2017. Plants were transplanted with
a 1 month delay with respect to the usual agronomical practice
of the area, exposing them to higher temperatures during the crit-
ical stages of flowering and fruit setting. Figure S1 reports the
values of mean, maximum, and minimum temperatures recorded
over the growing season, together with the average relative
humidity of the whole day. As shown, more than 40 days (38.5%
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of the whole growing season, from the end of May to the begin-
ning of September) reached temperatures over 32 °C, which is
considered the critical temperature affecting the reproductive
stage of tomato, as well as of other species.
21
On 16 days
(15.4%), a temperature higher than 35°C was even recorded. In
addition, very high temperatures were also recorded in the night,
and this is considered a critical point for pollen maturation.
22
Based on the evaluation of production per plant (Table 2), four
genotypes were classified as good (E8, E32, E36, ‘Moneymaker’),
five as medium (E7, E17, E53, E76, PDVIT), and two as low pro-
ducers (E30, E94) under high-temperature conditions. Indeed,
the first group exhibited a yield per plant higher than 4 kg, the
second group yield ranged from 2 to 4 kg per plant, whereas
the third group produced less than 2 kg per plant. As a whole,
yield performances confirmed previous data and allowed a reli-
able classification of the genotypes in the aforementioned three
groups.
Assessment of main quality parameters
With the aim of identifying those landraces simultaneously exhi-
biting good productivity and good nutritional quality under high
temperatures, and thus worth proposing as resilient varieties, we
evaluated the main quality parameters of the ten landraces. As
already reported in a previous study,
23
we chose the indetermi-
nate variety ‘Moneymaker’as a control genotype, considering
that it generally exhibits stable yields and fruit quality traits under
different environmental conditions and in different years. Con-
cerning the main fruit quality traits, the pH values ranged from
4.3 (landraces PDVIT and E76) to 4.6 (E17), with a mean value of
4.4, whereas the titratable acidity ranged from 0.38 g to 0.55 g
of citric acid per 100 mL of tomato juice in E36 and E76 respec-
tively (Table 3). The soluble solid content varied from 3.6 °Bx
(E7) to 8.1 °Bx (E8). Finally, E94 showed the lowest level of firmness
(8.7 kg cm
−2
) and PDVIT the maximum (18.9 kg cm
−2
). Notewor-
thy is that the three landraces E8, E30, and E76 showed high
degrees Brix levels (>7), and two of these (E30 and E76) also had
a titratable acidity value higher than 0.5. Altogether, these traits
affect consumer taste, who generally prefer firm, sweet, and acid
tomatoes,
24
and consequently the commercial value of tomatoes.
In recent years, more attention has been paid to the nutritional
value of food products, focusing on the beneficial effects of fresh
fruit and vegetables. To verify if the selected landraces could also
provide a good nutritional value when grown under high temper-
atures, the main tomato phytonutrients contents, such as AsA,
polyphenols, and carotenoids, were determined. These com-
pounds have been associated to health benefits and the reduc-
tion of inflammatory and aging-related diseases.
25–27
Therefore,
the dietary intake of these compounds is highly recommended.
The AsA levels in the red ripe fruit of the ten tomato landraces
and in the control cv Moneymaker are reported in Fig. 1. Most
landraces exhibited values of approximately 350 μgg
−1
FW,
which was statistically different from the value recorded in ‘Mon-
eymaker’(232 μgg
−1
FW), whereas two of them (E30 and E94)
reached a mean value higher than 400 μgg
−1
FW. The landrace
PDVIT was the best performer, with a mean value over 500 μgg
−1
FW. These values are in line with the values previously reported
for tomato genotypes, where AsA ranged from 100 to 880 μgg
−1
FW, even though commercial cultivars are generally characterized
by lower contents (from 100 to 400 μgg
−1
FW), probably due to
the breeding process.
28
However, the AsA content in fresh tomato
fruits is also dependent on genotype, climatic conditions, fruit
development, and maturation.
16
Carotenoids accumulation has been reported following abiotic
stresses, such as high or low temperature and high light, upon
which the homeostasis of ROS metabolism is challenged. For
Table 2. Yield (kg) per plant measured on ten landraces and the
control cv Moneymaker during 2017
Genotype Yield (kg)/plant Production level
E7 3.43 ±0.57
abc
Medium
E8 4.15 ±1.12
c
High
E17 2.71 ±0.29
ab
Medium
E30 1.70 ±039
a
Low
E32 4.93 ±0.83
c
High
E36 5.67 ±0.58
d
High
E53 3.67 ±0.25
bc
Medium
E76 2.59 ±0.41
ab
Medium
E94 1.67 ±0.71
a
Low
PDVIT 2.98 ±0.51
abc
Medium
‘Moneymaker’4.85 ±0.60
c
High
Following Duncan's post hoc test, the level of production under high
temperature was also reported. Values followed by the same letters
are not significantly different.
Table 3. Qualitative traits (mean and standard error) parameters measured on red ripe fruit. Statistical analysis was carried out by comparing values
with those recorded in the cv Moneymaker (M)
Genotype pH Soluble solid content (°Bx) Titratable acidity (g citric acid/100 mL juice) Firmness (kg cm
−2
)
E7 4.45 ±0.05 3.62 + 0.26** 0.43 + 0.01 14.31 + 1.11
E8 4.41 ±0.02 8.13 ±0.01** 0.46 + 0.01 15.16 + 0.12
E17 4.65 + 0.01* 4.29 + 0.17** 0.49 + 0,02 14.02 + 2.10
E30 4.42 + 0.04 7.88 + 0.21** 0.53 + 0.04 13.21 + 1.34
E32 4.49 + 0.02 6.58 + 0.24 0.39 + 0.01 15.03 + 0.18
E36 4.40 + 0.05 3.60 + 0.45** 0.38 + 0.03 14.05 + 2.51
E53 4.40 + 0.04 5.92 + 0.20 0.47 + 0.02 11.17 + 1.45
E76 4.32 + 0.02* 7.74 + 0.26* 0.55 + 0.03* 10.91 + 0.98*
E94 4.36 + 0.04 6.78 + 0.12 0.48 + 0.03 8.68 + 0.01**
PDVIT 4.31 + 0.06 5.92 + 0.01 0.50 + 0.02 18.90 + 1.50
‘Moneymaker’4.47 + 0.04 6.17 + 0.27 0.43 + 0.02 15.18 + 1.05
*P<0.05, **P<0.01 (Student's t-test).
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these reasons, carotenoids are implicated in the thermo-tolerance
of different plant species, including tomato.
2,29
Therefore, herein,
we analyzed the carotenoids content in the fruits of the tomato
landraces considered here. Concerning the main carotenoids
(i.e. lycopene, ⊎-carotene, and lutein), our data showed signifi-
cantly higher levels for these compounds in E30, E36, and E94
compared with cv Moneymaker (Fig. 2). Noteworthy is that a
higher ⊎-carotene content compared with the control cultivar
was also evidenced in PDVIT. This compound is considered a pro-
vitamin, which can be converted into retinol, a phytochemical
essential for vision. ⊎-Carotene is also known to act as a strong
antioxidant and is the best quencher of singlet oxygen.
16
The ⊎-carotene/lycopene ratio (Fig. S2) showed a different trend
among the landraces tested, with higher levels recorded in E17,
E30, and E32 (0.76, 0.68, and 1.16 respectively) compared with
cv Moneymaker (0.27) and other landraces. The differences in
the ⊎-carotene/lycopene ratio can be attributable to a possible
different genetic background of the landraces tested, which
might affect either the ⊎-carotene or lycopene biosynthesis.
Regarding this point, further molecular analyses are needed to
better elucidate possible genetic variations, which could explain
the differences in the amounts of these phytochemicals. In addi-
tion, harsh environmental conditions, such as high temperature,
can also impact lycopene accumulation in tomato fruits.
30–32
Brandt et al.,
30
for example, reported decreased lycopene biosyn-
thesis under high temperatures in the tomato F
1
variety
‘Lemance’.
Flavonoids, such as quercetin-3-rutinoside (rutin), and hydroxy-
cinnamic acids (such as chlorogenic, ferulic, and caffeic acids) are
the most representative phenolic compounds of tomatoes.
33,34
These compounds are characterized by the presence of phenolics
rings and hydroxyl groups in their structure that can scavenge
free radicals,
35,36
thus inhibiting the generation of ROS. In this
study, no significant differences were detected in the amount of
Figure 2. Content of the main carotenoids in tomato fruits of different landraces and the cv Moneymaker (M). Analyses were carried out by HPLC on fruit
extracts. Statistical analysis was carried out by comparing the content of each compound with that recorded in the cv Moneymaker (M). Data are mean
plus/minus SD (n=3). *P<0.05 (Student's t-test).
Figure 1. AsA content in the red ripe fruit of the ten tomato landraces and the control variety ‘Moneymaker’. Data are showed as mean ±SD (n=3).
*P<0.05, **P<0.01 (Student's t-test).
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2795

chlorogenic acid among the ten landraces and the commercial cv
Moneymaker (Fig. 3). However, significantly higher rutin levels
were detected in E36, E94, and PDVIT, compared with the control
cultivar (Fig. 3). A lower rutin level was instead detected in E32. In
the majority of the landraces analyzed in this study, higher levels
of kaempferol-O-rutinoside, one of the most common derivatives
of kaempferol in tomato fruit, were detected in E7, E17, E30,
E32, E36, E94, and PDVIT in comparison with ‘Moneymaker’
(Fig. 4). A higher kaempferol-O-glucoside content was also
detected in E94. Low levels of other phenolic compounds, such
as naringenin, were overall detected in the majority of land-
races (Fig. 4).
The higher polyphenols levels detected in some of the
tomato landraces analyzed could also be explained as a
stronger response to abiotic stresses, including heat
stress and exposure to UV radiation. Indeed, changes in
the polyphenols content have already been reported
in tomato following UV exposure.
37
In fact, genes implicated
in polyphenol biosynthesis are activated by light exposure,
and a ‘sunscreen’function has been proposed for these phy-
tochemicals to protect the tissues from possible damage gen-
erated by UV radiation.
10
Some authors reported that high
temperatures and light exposure stimulate the production of
phenolic acids and other flavonoids.
38,39
Indeed, heat stress
positively modulates the activity of the enzyme phenylalanine
ammonia-lyase and affects the total phenols content by acti-
vating their biosynthesis and inhibiting their oxidation in
tomato plants.
38,39
Figure 4. Polyphenols content in tomato fruits from different landraces and the cv Moneymaker (M). Quantification was carried out by HPLC using
methanolic extracts of fruits. Statistical analysis was carried out by comparing the content of each compound with that recorded in the cv Moneymaker
(M). Data are mean plus/minus SD (n=3). *P<0.05, **P<0.01 (Student's t-test).
Figure 3. Chlorogenic acid and rutin content in fruits of different landraces and the cv Moneymaker (M). Quantification was carried out by HPLC using
fruit methanolic extracts. Statistical analysis was carried out by comparing the content of each compound with thatrecorded in the cv Moneymaker (M).
Data are mean plus/minus SD (n=3). *P<0.05, **P<0.01 (Student's t-test).
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Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
J Sci Food Agric 2020; 100: 2791–2799
2796

Antioxidant/anti-inflammatory properties of tomato
landraces
The antioxidant capacity of methanol extracts from fruits of
the ten tomato landraces is reported in Fig. 5(a), using the
TEAC assay. Previous studies reported that rutin and phenolic
acids can contribute to the overall antioxidant capacity of
tomato, neutralizing free radicals by acting as electron donors
or inhibiting the activity of enzymes involved in the produc-
tion of free radicals.
39
Our results indicated a slight, not signif-
icant, higher antioxidant activity in E32, followed by E17 and
E30. Conversely, a significant lower antioxidant activity was
evidenced in E53 and E76, which also showed a lower polyphe-
nols content (see Fig. 4). E76 also showed a lower AsA content
than in the other landraces. Indeed, it is well known that the
antioxidant property of a food matrix is dependent on the
presence and levels of different compounds comprising phe-
nolic species and AsA.
38
To assess the anti-inflammatory potential and the ability to trig-
ger an in vitro immune-modulating response, tomato extracts
were incubated with murine dendritic cells. LPS was used as an
inflammatory stimulant. Figure 5(b) shows the effects of the
administration of tomato extracts on the production of pro-
inflammatory IL-6 and IL-12. Significantly lower levels of IL-6
were detected in the presence of E7 and E8 extracts. Both these
landraces showed increased levels of AsA, which could be
related to the decreased levels of the pro-inflammatory activity
of IL-6. E8, together with E94 and PDVIT extracts, was also able
to decrease the secretion of the pro-inflammatory IL-12 (Fig. 5
(c)) even though the differences observed were not significant.
Some studies have reported the reduction of pro-inflammatory
interleukins in dendritic cells mediated by the aglycone querce-
tin, thus demonstrating an anti-inflammatory activity for this
phytochemical.
40–42
In this context, rutin, which is the most
abundant phenolic compound in our quantification, could be
responsible, at least in part, for the anti-inflammatory activity
detected in the tomato extracts. However, our data did not
establish a clear correlation between the content in phenolic
compounds and the anti-inflammatory activity in all the land-
races tested. Indeed, the role of flavonoids has been generally
described using chemically pure standards, only partially reflect-
ing the real anti-inflammatory activity that can be exerted by a
whole fruit or vegetable extracts.
43
Combining yield and quality parameters
To examine the possible co-occurrence of both yield and quality
features in the landraces tested, we calculated Spearman correla-
tions considering all the traits included in this study (Fig. 6(a)).
Positive correlations, significant in some cases, were found among
the secondary metabolites analyzed (AsA, carotenoids, phenolic
acids, and flavonoids), indicating that the observed changes
within the plant secondary metabolism involve the cross-talk
among different classes of phytochemicals and thus different bio-
chemical pathways. Furthermore, some of these metabolites pos-
itively correlated to physicochemical parameters such as acidity,
degrees Brix, and fruit firmness, indicating an association between
secondary metabolites and traits influencing fruit organoleptic
properties.
An estimated EI was also calculated considering the quality
and nutritional traits analyzed all together. EI varied from a
minimum of 123 for E17 to a maximum of 175 for PDVIT, with
a mean value of 141.2. The distribution of the ten landraces
according their EI value and yield is shown in Fig. 6(b). From
this analysis, it is evident that three landraces (E30, E94,
PDVIT) exhibit better performances in terms of fruit quality
(EI >160), though two of them (E30 and E94) showed low
yield (less than 2 kg per plant) under high temperatures. All
the better performing landraces in terms of yield (classified
as high or medium producers), with the exception of PDVIT,
exhibited lower EI levels, thus evidencing lower values of
quality traits.
CONCLUSION
In this paper, one landrace (PDVIT) was selected as a good com-
promise between yield performances and good fruit quality and
nutritional traits when growing under high temperature. Addi-
tional molecular and physiological analyses in other environ-
ments are in progress in order to further characterize this
selected landrace. Indeed, this landrace shows a level of adapt-
ability that can be useful in adverse conditions, making it a suit-
able candidate for breeding programs, since it can be
Figure 5. Antioxidant and anti-inflammatory activities of tomato extracts
from different landraces. (a) Antioxidant capacity profiles measured by
TEAC. Data are mean μmol TE ±SD (n=3), *P<0.05 (Student's t-test).
Levels of pro-inflammatory (b) IL-6 and (c) IL-12 in BMDCs stimulated with
LPS and treated with methanolic tomato extracts from fruits of different
tomato landraces. Concentrations of cytokines were determined by ELISA
test. Data are expressed as mean plus/minus SD (n=3); *P<0.05
(Student's t-test).
Selection of tomato landraces with high fruit yield www.soci.org
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Journal of The Science of Food and Agriculture published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.
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2797

considered as a ‘balanced landrace’
44
in terms of stress resilience
and fruit nutritional quality.
ACKNOWLEDGEMENTS
This work was in part founded by the European Union's Horizon
2020 research and innovation program through the TomGEM pro-
ject under grant agreement no. 679796 and by the Apulia region
through the SICURA project (KC3U5Y1). We acknowledge Mr
Leone D'Amico for technical assistance.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
SUPPORTING INFORMATION
Supporting information may be found in the online version of this
article.
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