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Selection Of Tomato Landraces With High Fruit Yield and Nutritional Quality Under Elevated Temperatures

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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 selected tomato landraces. Results: Tomato landraces here analyzed in a hot climate differed in terms of yield performance, physicochemical parameters of fruit (pH, titratable acidity, °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 to identify PDVIT as the best performer in term of yield and fruit quality under high temperatures. Conclusion: The analyses here performed highlight the possibility to identify new landraces that can combine good yield performances and fruit nutritional quality at high temperatures, useful for future breeding programs. This article is protected by copyright. All rights reserved.
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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 uctuations 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 identication 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-inammatory 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, rmness), bioactive compounds (ascorbic acid, carotenoids, and polyphenols),
and anti-inammatory potential. Three of these landraces (named E30, E94, and PDVIT) showed higher fruit quality and nutri-
tional value. An estimated evaluation index allowed identication 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 uctuations 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 specicgeo-
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 signicant 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, ISPACNR, Institute of Science of Food
Production, CNR Unit of Lecce, via Provinciale Lecce-Monteroni, 73100
Lecce, Italy. E-mail: angelo.santino@ispa.cnr.it
aISPACNR, 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.
1,47
Since thermo-tolerance requires the mod-
ulation of biochemical pathways involved in reactive oxygen spe-
cies (ROS) detoxication, 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 uidity and permeability in response to tempera-
ture uctuations.
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 avonoids 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-inammatory
properties have been described following their in vitro or in vivo
administration.
1214
In particular, phenolic compounds may have
therapeutic roles in inammation-based diseases and various
type of cancers.
15
Furthermore, ascorbic acid shows signicant
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 nal
yield and fruit quality on a set of ten tomato landraces showing
good performances when grown under elevated temperatures.
Their productivity and eld performances under restrictive envi-
ronmental conditions were estimated. Moreover, the bioactive
compounds content and antioxidants/anti-inammatory proper-
ties have been evaluated in extracts from ripe fruits from different
tomato landraces, with the nal 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 eld 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 (2530 g) Ovate
E8 CRA-ORT
a
Corbarino PC05 Italy Sant'Antonio
Abate (Salerno)
Processing Small (2025 g) Elliptic
E17 CRA-ORT
a
Pantano Romanesco Italy Fondi (Latina) Fresh market Big (200250 g) Flattened
E30 CRA-ORT
a
Sel PC07 Italy Pagani (Salerno) Processing Small (1520 g) Ovate
E32 CRA-ORT
a
Sel PC16 Italy Nocera (Salerno) Fresh market Small (2050 g) Ovate
E36 Campania
Region
a
Vesuvio Foglia Riccia Italy S. Vito (Naples) Fresh market/
processing
Small (2530 g) Ovate
E53 TGRC LA0147 Honduras Tegucigalpa
mercado
Fresh market Medium (80100 g) Oblate
E76 TGRC LA4449 Black plum URSS Processing Small (2025 g) Ovate
E94 NPGS PI272890 1404 Guatemala Quetzaltenango,
Guatemala
nd Small (4050 g) Irregular
PDVIT ARCA2010
a
Caramella Italy Scafati (Salerno) Fresh market/
processing
Small (1015 g) Elliptic
MoneymakerTGRC LA2706 Moneymaker Great Britain Fresh market Medium (5060 g) Circular
a
Germplasm collections maintained at Italian public institution.
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J Sci Food Agric 2020; 100: 27912799
2792
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 rmness
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 nely 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, ltered through a
0.22 μmlter, 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 ow 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
modications reported by Rigano et al.
20
Briey, 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
UVvisible 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 (nal concentration) with an aqueous solution of 7 mmol L
1
ABTS (nal concentration) and allowed to stand in the dark at
room temperature for 1216 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 (016 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 Innite200Pro 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 humidied 5% carbon dioxide atmosphere.
BMDCs were treated with tomato methanol extracts (100 mg
lyophilized powder per milliliter, 1:25 nal 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. Signi-
cant different yields were determined by comparing mean values
through a factorial analysis of variance with Duncan post hoc test
at a signicance 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
eld 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 owering 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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2793
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 classied as good (E8, E32, E36, Moneymaker),
ve as medium (E7, E17, E53, E76, PDVIT), and two as low pro-
ducers (E30, E94) under high-temperature conditions. Indeed,
the rst 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 conrmed previous data and allowed a reli-
able classication 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 Moneymakeras 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 rmness
(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 rm, 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 benecial 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 benets and the reduc-
tion of inammatory and aging-related diseases.
2527
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
Moneymaker4.85 ±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 signicantly 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
Moneymaker4.47 + 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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J Sci Food Agric 2020; 100: 27912799
2794
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 signi-
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.
3032
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 signicant 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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chlorogenic acid among the ten landraces and the commercial cv
Moneymaker (Fig. 3). However, signicantly 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 sunscreenfunction 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 avonoids.
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). Quantication 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). Quantication 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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J Sci Food Agric 2020; 100: 27912799
2796
Antioxidant/anti-inammatory 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 signicant 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-inammatory 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
inammatory stimulant. Figure 5(b) shows the effects of the
administration of tomato extracts on the production of pro-
inammatory IL-6 and IL-12. Signicantly 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-inammatory activity
of IL-6. E8, together with E94 and PDVIT extracts, was also able
to decrease the secretion of the pro-inammatory IL-12 (Fig. 5
(c)) even though the differences observed were not signicant.
Some studies have reported the reduction of pro-inammatory
interleukins in dendritic cells mediated by the aglycone querce-
tin, thus demonstrating an anti-inammatory activity for this
phytochemical.
4042
In this context, rutin, which is the most
abundant phenolic compound in our quantication, could be
responsible, at least in part, for the anti-inammatory activity
detected in the tomato extracts. However, our data did not
establish a clear correlation between the content in phenolic
compounds and the anti-inammatory activity in all the land-
races tested. Indeed, the role of avonoids has been generally
described using chemically pure standards, only partially reect-
ing the real anti-inammatory 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, signicant in some cases, were found among
the secondary metabolites analyzed (AsA, carotenoids, phenolic
acids, and avonoids), 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 rmness, indicating an association between
secondary metabolites and traits inuencing 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 (classied
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-inammatory activities of tomato extracts
from different landraces. (a) Antioxidant capacity proles measured by
TEAC. Data are mean μmol TE ±SD (n=3), *P<0.05 (Student's t-test).
Levels of pro-inammatory (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
J Sci Food Agric 2020; 100: 27912799 © 2020 The Authors.
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 conict of interest.
SUPPORTING INFORMATION
Supporting information may be found in the online version of this
article.
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... We assessed the post-harvest properties of these 41 accessions, such as the duration of fruit shelf life and fungal susceptibility, under normal and high temperature regimes. These genotypes have been extensively characterised for their responses to elevated temperature and/or drought growth conditions using Qualitative Trait Loci analysis, high-throughput geno-and phenotyping, assessment of flowering, fruit set, yield, fruit nutritional composition, antioxidant and antiinflammatory activities, as well as by screening for photosynthetic efficiency [23][24][25][26][27][28][29][30][31][32][33][34]. In addition, several candidate genes regulating heat stress tolerance were recently identified in varieties from this collection [24,29]. ...
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... Plant productivity under environmental stress is a highly complex process, integrating multiple physiological traits and molecular pathways. In tomato, fruit production under heat stress conditions results in reduced fruit set which translates to yield loss [22]. In order to cope with this environmental sensitivity and allow normal fruit production under heat stress conditions, we need to understand the regulatory network that underlies the stress response. ...
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Heat stress is a major environmental factor limiting crop productivity, thus presenting a food security challenge. Various approaches are taken in an effort to develop crop species with enhanced tolerance to heat stress conditions. Since epigenetic mechanisms were shown to play a regulatory role in mediating plants' responses to their environment, we investigated the role of DNA methylation in response to heat stress in tomato (Solanum lycopersicum), an important vegetable crop. To meet this aim, we tested a DNA methylation-deficient tomato mutant, Slddm1b. In this short communication paper, we report phenotypic and transcriptomic preliminary findings, implying that the tomato ddm1b mutant is significantly less sensitive to heat stress compared with the background tomato line, M82. Under conditions of heat stress, this mutant line presented higher fruit set and seed set rates, as well as a higher survival rate at the seedling stage. On the transcriptional level, we observed differences in the expression of heat stress-related genes, suggesting an altered response of the ddm1b mutant to this stress. Following these preliminary results, further research would shed light on the specific genes that may contribute to the observed thermotolerance of ddm1b and their possibly altered DNA methylation status.
... One of the most important microclimate parameters affecting tomato production and quality is air temperature [20]. Jun et al. [21] reported that the best temperature regime for net photosynthesis on greenhouse-grown tomatoes is 28/20 • C (day/night), while higher or lower temperatures can negatively affect fruit sets [22]. ...
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Light qualities are considered to affect many plant physiological processes during growth and development. To investigate how light qualities make an influence on tomato seedlings under greenhouse conditions, the growth and morphological parameters of tomato seedlings (Fortizia F1RC hybrid) were studied under three supplemental light irradiations such as light-emitting diodes with nanoparticle coating (LED 1—Red light-emitting diodes); Blue, Green, Yellow, Red light-emitting diodes (LED 2), and traditional high-pressure sodium (HPS) lamps with different photosynthetic photon flux density and the same irradiation time for 33 days. Morphological appearances of three groups of tomato seedlings were different between light treatments, that is, the plants under LED-1 and LED-2 were shorter than those under HPS, while stem diameter, leaf area, dry and fresh weights, and health indices of tomato seedlings grown under alternative light sources were higher than of those cultivated under traditional HPS lights. However, the higher plant height was in plants containing traditional high-pressure sodium lamps treatment. Photosynthetic pigments were shown to have a significant difference under respective light irradiations of LEDs. The levels of photosynthetic pigments were higher in the leaves of seedlings under LED 1 and LED 2, and lower in those that underwent HPS control treatment. Based on the data of morphological and statistical analysis, LEDs with nanoparticle coating proved to be beneficial factors for the growth of tomato seedlings under greenhouse conditions.
... A total of 41 accessions were analyzed under heat conditions, 31 from the candidate 76 tolerant genotypes selected in the FCCV_2016 experiment (8 wild accessions, 5 S. lycopersicum var. cerasiforme, 12 traditional cultivars including 7 "de penjar or "da serbo" tomatoes, 6 modern cultivars and commercial hybrids), seven heat tolerant Italian landraces [44,45], belonging to a collection available at the University of Naples Federico II, Department of Agricultural Sciences which showed heat tolerance in parallel field experiments (details hosted at LabArchive repository http:// dx. doi. ...
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Background Due to global warming, the search for new sources for heat tolerance and the identification of genes involved in this process has become an important challenge as of today. The main objective of the current research was to verify whether the heat tolerance determined in controlled greenhouse experiments could be a good predictor of the agronomic performance in field cultivation under climatic high temperature stress. Results Tomato accessions were grown in greenhouse under three temperature regimes: control (T1), moderate (T2) and extreme heat stress (T3). Reproductive traits (flower and fruit number and fruit set) were used to define heat tolerance. In a first screening, heat tolerance was evaluated in 219 tomato accessions. A total of 51 accessions were identified as being potentially heat tolerant. Among those, 28 accessions, together with 10 accessions from Italy (7) and Bulgaria (3), selected for their heat tolerance in the field in parallel experiments, were re-evaluated at three temperature treatments. Sixteen tomato accessions showed a significant heat tolerance at T3, including five wild species, two traditional cultivars and four commercial varieties, one accession from Bulgaria and four from Italy. The 15 most promising accessions for heat tolerance were assayed in field trials in Italy and Bulgaria, confirming the good performance of most of them at high temperatures. Finally, a differential gene expression analysis in pre-anthesis (ovary) and post-anthesis (developing fruit) under heat stress among pairs of contrasting genotypes (tolerant and sensitive from traditional and modern groups) showed that the major differential responses were produced in post-anthesis fruit. The response of the sensitive genotypes included the induction of HSP genes, whereas the tolerant genotype response included the induction of genes involved in the regulation of hormones or enzymes such as abscisic acid and transferases. Conclusions The high temperature tolerance of fifteen tomato accessions observed in controlled greenhouse experiments were confirmed in agronomic field experiments providing new sources of heat tolerance that could be incorporated into breeding programs. A DEG analysis showed the complex response of tomato to heat and deciphered the different mechanisms activated in sensitive and tolerant tomato accessions under heat stress.
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This narrative mini- review summarizes current knowledge of the role of polyphenols in health outcomes—and non-communicable diseases specifically—and discusses the implications of this evidence for public health, and for future directions for public health practice, policy, and research. The publications cited originate mainly from animal models and feeding experiments, as well as human cohort and case-control studies. Hypothesized protective effects of polyphenols in acute and chronic diseases, including obesity, neurodegenerative diseases, type 2 diabetes, and cardiovascular diseases, are evaluated. Potential harmful effects of some polyphenols are also considered, counterbalanced with the limited evidence of harm in the research literature. Recent international governmental regulations are discussed, as the safety and health claims of only a few specific polyphenolic compounds have been officially sanctioned. The implications of food processing on the bioavailability of polyphenols are also assessed, in addition to the health claims and marketing of polyphenols as a functional food. Finally, this mini-review asserts the need for increased regulation and guidelines for polyphenol consumption and supplementation in order to ensure consumers remain safe and informed about polyphenols.
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Constant global warming is one of the most detrimental environmental factors for agriculture causing significant losses in productivity as heat stress (HS) conditions damage plant growth and reproduction. In flowering plants such as tomato, HS has drastic repercussions on development and functionality of male reproductive organs and pollen. Response mechanisms to HS in tomato anthers and pollen have been widely investigated by transcriptomics; on the contrary, exhaustive proteomic evidences are still lacking. In this context, a differential proteomic study was performed on tomato anthers collected from two genotypes (thermo-tolerant and thermo-sensitive) to explore stress response mechanisms and identify proteins possibly associated to thermo-tolerance. Results showed that HS mainly affected energy and amino acid metabolism and nitrogen assimilation and modulated the expression of proteins involved in assuring protein quality and ROS detoxification. Moreover, proteins potentially associated to thermo-tolerant features, such as glutamine synthetase, S-adenosylmethionine synthase and polyphenol oxidase, were identified.
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Climate change has become a serious threat for crop productivity worldwide. The increased frequency of heat waves strongly affects reproductive success and thus yield for many crop species, implying that breeding for thermotolerant cultivars is critical for food security. Insight into the genetic architecture of reproductive heat tolerance contributes to our fundamental understanding of the stress sensitivity of this process and at the same time may have applied value. In the case of tomato (Solanum lycopersicum), germplasm screenings for thermotolerance have often used yield as the main measured trait. However, due to the complex nature of yield and the relatively narrow genetic variation present in the cultivated germplasm screened, there has been limited progress in understanding the genetic basis of reproductive heat tolerance. Extending the screening to wild accessions of related species that cover a range of climatic conditions might be an effective approach to find novel, more tolerant genetic resources. The purpose of this study was to provide insight into the sensitivity of individual reproductive key traits (i.e. the number of pollen per flower, pollen viability and style protrusion) to heat-wave like long-term mild heat (LTMH), and determine the extent to which genetic variation exists for these traits among wild tomato species. We found that these traits were highly variable among the screened accessions. Although no overall thermotolerant species were identified, several S. pimpinellifolium individuals outperformed the best performing cultivar in terms of pollen viability under LTMH. Furthermore, we reveal that there has been local adaptation of reproductive heat tolerance, as accessions from lower elevations and higher annual temperature are more likely to show high pollen viability under LTMH.
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Dietary polyphenols are associated with a wide range of health benefits, protecting against chronic diseases and promoting healthy aging. Dietary polyphenols offer a complementary approach to the treatment of inflammatory bowel diseases (IBDs), a group of common chronic intestinal inflammation syndromes for which there is no cure. Tomato is widely consumed but its content of polyphenols is low. We developed a tomato variety, Bronze, enriched in three distinct classes of polyphenols: flavonols, anthocyanins, and stilbenoids. Using Bronze tomatoes as a dietary supplement as well as Indigo (high anthocyanins and flavonols), ResTom (high stilbenoids) and wild-type tomatoes, we examined the effects of the different polyphenols on the host gut microbiota, inflammatory responses, and the symptoms of chronic IBD, in a mouse model. Bronze tomatoes significantly impacted the symptoms of IBD. A similar result was observed using diets supplemented with red grape skin containing flavonols, anthocyanins, and stilbenoids, suggesting that effective protection is provided by different classes of polyphenols acting synergistically.
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The increase of L-Ascorbic Acid (AsA) content in tomato (Solanum lycopersicum) is a common goal in breeding programs due to its beneficial effect on human health. To shed light into the regulation of fruit AsA content, we exploited a Solanum pennellii introgression line (IL12-4-SL) harbouring one quantitative trait locus that increases the content of total AsA in the fruit. Biochemical and transcriptomic analyses were carried out in fruits of IL12-4-SL in comparison with the cultivated line M82 at different stages of ripening. AsA content was studied in relation with pectin methylesterase (PME) activity and the degree of pectin methylesterification (DME). Our results indicated that the increase of AsA content in IL12-4-SL fruits was related with pectin de-methylesterification/degradation. Specific PME, polygalacturonase (PG) and UDP-D-glucuronic-acid-4-epimerase (UGlcAE) isoforms were proposed as components of the D-galacturonate pathway leading to AsA biosynthesis. The relationship between AsA content and PME activity was also exploited in PMEI tobacco plants expressing a specific PME inhibitor (PMEI). Here we report that tobacco PMEI plants, altered in PME activity and degree of pectin methylesterification, showed a reduction in low methylesterified pectic domains and exhibited a reduced AsA content. Overall, our results provide novel biochemical and genetic traits for increasing antioxidant content by marker-assisted selection in the Solanaceae family.