horticulturae

Article
Adaptability and Stability Analyses of Improved Strawberry
Genotypes for Tropical Climate
Daniele Aparecida Nascimento 1 , Gabriella Correia Gomes 2 , Luiz Vitor Barbosa de Oliveira 2 ,
Gabriel Francisco de Paula Gomes 2 , Suzana Tiemi Ivamoto-Suzuki 2 , André Ricardo Ziest 3 ,
Keny Henrique Mariguele 4 , Sergio Ruffo Roberto 2 and Juliano Tadeu Vilela de Resende 1,2, *

1 Campus CEDETEG, State University of Centro-Oeste, Alameda Élio Antonio Dalla Vecchia, 838,
Guarapuava 85040-167, Brazil; [email protected]
2 Agricultural Research Center, State University of Londrina, Celso Garcia Cid Road, km 380,
Londrina 86057-970, Brazil; [email protected] (G.C.G.); [email protected] (L.V.B.d.O.);
[email protected] (G.F.d.P.G.); [email protected] (S.T.I.-S.); [email protected] (S.R.R.)
3 Agricultural Research Center, Federal University of Santa Catarina, R. Eng. Agronômico Andrei Cristian
Ferreira, s/n—Trindade, Florianópolis 88040-900, Brazil; [email protected]
4 Santa Catarina State Rural Extension and Agricultural Research Corporation, Admar Gonzaga Street, 1347,
Itajaí 88034-901, Brazil; [email protected]
* Correspondence: [email protected]; Tel.: +55-(43)-3376-5990

Abstract: Strawberries are grown worldwide, and the fruit is known for its flavor, pleasant aroma,
and the presence of important nutraceutical compounds. Under temperate conditions, the species is
octaploid and presents a complex inheritance. Exploring polyploidy in varietal crosses is the main
alternative to developing genotypes of high-temperature regions; thus, breeding programs must
evaluate the interaction based on parameters, such as the heritability, stability, easy propagation, and
adaptability to different soil and climate variations. To estimate the stability and temporal adapt-
ability of pre-selected triple hybrids of day-neutral strawberries, thirty-six experimental genotypes,
three commercial genotypes (‘Albion,’ ‘Monterey,’ and ‘Dover’), and four single hybrids (‘RVFS07,’
Citation: Nascimento, D.A.; Gomes, ‘RVFS06,’ ‘RVDA11,’ and ‘RVCA16’) were evaluated in a protected cultivation from August to Febru-
G.C.; de Oliveira, L.V.B.; de Paula ary under tropical climate conditions (southern hemisphere) using the mixed linear model (MLM).
Gomes, G.F.; Ivamoto-Suzuki, S.T.; The genotypes RVFS07M-34, RVFS07M-24, RCDA11M-04, RVFS07M-154, RVFS07M-36, RVFS07M-33,
Ziest, A.R.; Mariguele, K.H.; Roberto, RVFS07M-80, RVFS07M-10, RVDA11M-21, RVDA11M-13, and RVFS06AL-132 had the highest values
S.R.; de Resende, J.T.V. Adaptability of total fruit mass, adaptability, and stability. The mean predicted genotypic values of the selected
and Stability Analyses of Improved
genotypes was 138% higher than the mean of the controls. Therefore, these genotypes have the
Strawberry Genotypes for Tropical
potential to be released as cultivars.
Climate. Horticulturae 2023, 9, 643.
https://doi.org/10.3390/
Keywords: Fragaria × ananassa Duch; heritability; propagation; low cold requirement; neutral photoperiod
horticulturae9060643

Academic Editor: Yuepeng Han

Received: 19 April 2023

Revised: 23 May 2023
1. Introduction
Accepted: 25 May 2023 Strawberry production in the southern hemisphere is totally dependent on cultivars
Published: 30 May 2023 developed by breeding programs in the United States and Spain [1]. In addition to low
adaptability and stability in tropical regions, these cultivars increase production costs, since
commercial nursery plants are multiplied and imported in dollars [2]. Another recurring
problem concerns the physiological and phytosanitary quality, where several crops were
Copyright: © 2023 by the authors.
affected by pathogens that did not exist in the producing regions, and they were probably
Licensee MDPI, Basel, Switzerland.
introduced by imported nursery plants.
This article is an open access article
Climate change has promoted an increase in the temperature and in the concentration
distributed under the terms and
of carbon dioxide (CO2 ) in the atmosphere [3,4]. High temperatures limit the culture, as
conditions of the Creative Commons
strawberry plants require cold hours for floral induction. Thus, it can negatively affect
Attribution (CC BY) license (https://
the yield of cultivated plants, interfering with the balance of morphophysiological and
creativecommons.org/licenses/by/
4.0/).
hormonal processes [5,6].

Horticulturae 2023, 9, 643. https://doi.org/10.3390/horticulturae9060643 https://www.mdpi.com/journal/horticulturae

Horticulturae 2023, 9, 643 2 of 13

The development of adaptable and stable tropical cultivars can be a solution to over-
come this issue. Therefore, it is important that genetic breeding programs are stimulated
to develop productive cultivars and adapted to a wide range of latitudes, allowing cul-
tivation area expansion [7]. Several studies in tropical regions have demonstrated the
potential of new genotypes with low chilling requirements and higher yields, compared to
well-established cultivars in the market [2,8–10].
The environment interferes with agronomic characteristics [11] and the quality of the
fruit post-harvest [12]. Considering the wide latitude of strawberry cultivation worldwide,
studies of adaptability and stability should be carried out both in relation to the location
and throughout the harvest period [1].
Studying the genotype × environment interaction aims to identify the behavioral
variation that genotypes undergo when exposed to varied environmental conditions [13].
One way to measure these interaction effects is through correlation studies between the
characteristics of interest [14]. Correlations estimated among variables provide strategic
information for studies to improve adaptability and stability in strawberries [15]. In
addition, these studies allow genotype identification with predictable behavior, as well as
those responsive to environmental variations, under specific conditions [16,17].
The variability of the genus Fragaria is wide, and it is classified according to the ploidy
level, in which the basic number of chromosomes is equal to seven (x = 7) [18]. Among
the twenty-five known species, thirteen are diploid (2n = 2x = 14), five are tetraploid
(2n = 4x = 28), one is petaploid (2n = 5x = 35), one is hexaploid (2n = 6x = 42), three are octa-
ploid (2n = 8x = 56), and two are decaploids [18]. The cultivated species (Fragaria × ananassa),
classified as octaploid, is derived from immediate ancestors (F. chiloensis and F. virginiana),
considered allopolyploids [19], which, in turn, are derived from two or more
different diploid ancestors [20]. The octaploid commercial strawberry genome com-
prises 813.4 megabases (Mb) that are distributed across 28 pseudochromosomes, with
108,087 protein-coding genes and 30,703 RNA-coding genes [21]. Therefore, this wide vari-
ability generates expectations of obtaining genotypes adapted to a low chilling requirement.
Most polyploids obtained by chromosome duplication have characteristics of vigorous
plants and larger fruits [22]. Eukaryotic polyploids also show strong resistance to biotic
and abiotic factors [23].
Mixed linear models consider genotype effects as modifications to estimate adaptabil-
ity and stability, allowing a genetic effects analysis to be made using best linear unbiased
predictors (BLUPs) [24]. However, mixed linear models are routinely prone to experimental
inconstancy and the heterogeneity of environmental variations [25]. Therefore, in this
method, the genotypic values (e.g., productivity), adaptability, and genotypic stability
are analyzed simultaneously [26]. This methodology is based on the harmonic mean of
the relative performance of genotypic values (HMRPGV) method, which considers the
genotype mean and its variation in different environments.
The relationship between genotype and phenotype in different regions helps to antici-
pate more precise responses to the selection of individuals with heterogeneous habitats,
whether spatial or temporal. If the genotype has phenotypic expression for a particular
trait, depending on the environment, heritability measures can be altered according to
variations in environmental conditions [27].
Thus, the objective of this work was to estimate the adaptability and the temporal
stability, as well to select strawberry genotypes easy to propagate with lower cold require-
ments using a mixed linear model.

2. Materials and Methods

2.1. Location
The experiment was conducted at the University of Centro-Oeste, Guarapuava, Brazil
(25◦ 230 0100 S, 51◦ 290 5000 W, elevation of 1025 m a.s.l.) from August 2019 to February of 2020.
The soil was classified as typical dystroferric Latosol Bruno [28]. The climate was humid
subtropical Cfb (temperate oceanic climate, warm summer, and without a dry season),
Horticulturae 2023, 9, 643 3 of 13

which includes hot summers and frosty winters. The average annual temperature was
17 ◦ C, with maximum and minimum temperatures of 23.5 ◦ C and 12.7 ◦ C, respectively. The
average annual rainfall was 1946 mm [28].

2.2. Experimental Genotypes

In our study, 36 genotypes (Table 1) were selected from 10 populations (total of
2000 F1 plants) from crosses among genotypes pre-selected by our strawberry breeding
program and commercial cultivars with responses to neutral photoperiods (‘Albion’ and
‘Monterey’). The 36 genotypes were multiplied to produce the nursery plants for the trials.

Table 1. Genotypes pre-selected from the strawberry breeding program obtained from intravarietal crosses.

Male Genitor Cultivars Female Genitor Cultivar Genotypes

RVFS 07 (Festival × Aromas) Monterey RVFS07M-24
RVFS 07 (Festival × Aromas) Monterey RVFS07M-36
RVFS 06 (Festival × Aromas) Albion RVFS06AL-132
RVFS 07 (Festival × Aromas) Monterey RVFS07M-34
RVFS 07 (Festival × Aromas) Monterey RVFS07M-179
RVDA 11 (Dover × Aromas) Monterey RVDA11M-04
RVDA 11 (Dover × Aromas) Monterey RVDA11M-21
RVFS 07 (Festival × Aromas) Monterey RVFS07M-02
RVFS 07 (Festival × Aromas) Monterey RVFS07M-32
RVFS 07 (Festival × Aromas) Monterey RVFS07M-38
RVFS 07 (Festival × Aromas) Monterey RVFS07M-05
RVFS 07 (Festival × Aromas) Monterey RVFS07M-33
RVFS 07 (Festival × Aromas) Monterey RVFS07M-10
RVDA 11 (Dover × Aromas) Monterey RVDA11M-13
RVFS 07 (Festival × Aromas) Monterey RVFS07M-154
RVFS 07 (Festival × Aromas) Monterey RVFS07M-47
RVFS 07 (Festival × Aromas) Monterey RVFS07M-31
RVFS 07 (Festival × Aromas) Monterey RVFS07M-16
RVDA 11 (Dover × Aromas) Monterey RVDA11M-25
RVFS 07 (Festival × Aromas) Monterey RVFS07M-113
RVDA 11 (Dover × Aromas) Monterey RVDA11M-32
RVFS 07 (Festival × Aromas) Monterey RVFS07M-30
RVCA 16 (Camarosa × Aromas) Monterey RVCA16M-01
RVDA 11 (Dover × Aromas) Monterey RVDA11M-28
RVFS 07 (Festival × Aromas) Monterey RVFS07M-151
RVDA 11 (Dover × Aromas) Monterey RVDA11M-10
RVFS 07 (Festival × Aromas) Monterey RVFS07M-124
RVFS 06 (Festival × Aromas) Monterey RVFS06M-29
RVDA 11 (Dover × Aromas) Monterey RVDA11M-29
RVFS 07 (Festival × Aromas) Monterey RVFS07M-42
RVFS 07 (Festival × Aromas) Albion RVFS07AL-28
RVFS 07 (Festival × Aromas) Monterey RVFS07M-48
RVFS 07 (Festival × Aromas) Monterey RVFS07M-88
RVFS 07 (Festival × Aromas) Monterey RVFS07M-80
RVDA 11 (Dover × Aromas) Monterey RVDA11M-03
RVFS 06 (Festival × Aromas) Albion RVFS06AL-36

The mother plants were kept in a greenhouse with an average temperature of 25 ± 3 ◦ C

and a humidity of 75 ± 5%. The nursery plants were obtained from runners (stolons) and
transplanted into polypropylene trays, with 50 cells filled with substrate. After 50 days,
they were transplanted to an experimental field for evaluation in a repeat trial.

2.3. Genotype Transplantation

The nursery plants were transplanted to the field in a low tunnel cultivation system
that was spaced at 30 × 40 cm. Fertilization was composed of 1650 kg ha−1 of simple
superphosphate, 250 kg ha−1 of potassium chloride, and 295 kg ha−1 of urea and applied
Horticulturae 2023, 9, 643 4 of 13

to the soil. Irrigation was carried out by drippers with a spacing of 30 cm using two drip
lines per bed spaced at 50 cm.
The experiment was performed in a randomized block design, with three repeti-
tions and 10 plants per plot for each genotype for a total of 1320 plants. The com-
mercial genotypes ‘Albion’, ‘Monterey’, and ‘Dover,’ and the single hybrids ‘RVCA 16’
(‘Camarosa’ × ‘Aromas’), ‘RVFS07’ (‘Festival’ × Aromas), ‘RVFS06’ (Festival × Aromas),
‘RVDA 11’ (Dover × Aromas), and ‘RVDA44’ (Camarosa × ‘Sweet Charlie’) were used
as controls.
Seven topdressing fertilizations were carried out at 15-day intervals. Each fertilization
was composed of 30 kg ha−1 of ammonium sulfate, 5.5 kg ha−1 of potassium sulfate, and
7.5 kg ha−1 of potassium chloride. At the beginning of flowering, boric acid and zinc
sulfate were sprayed onto the leaves at 1 L 100 L−1 and at 1 kg 100 L−1 , respectively. In the
fruit production stage, 0.4% of calcium chloride was applied every 15 days. Phytosanitary
control was carried out with preventive spraying, according to the specific techniques
recommended for the culture. The biweekly sprays were interspersed among abamectin
(75 mL ha−1 ), thiametoxan (10 mL ha−1 ), and fipronil (250 mL ha−1 ) products. The control
of fungal diseases was carried out with alternating applications of azoxystrobin (16 g ha−1 ),
tebuconazole (75 mL ha−1 ), and mancozeb (250 g ha−1 ).

2.4. Statistical Analyses

The total fruit mass (TFM g/plant) was obtained for each harvest from August 2019 to
February 2020. Each month was considered a collection period to perform adaptability and
stability studies.
Statistical analyses were performed using a linear mixed model methodology, where
the genetic parameters were estimated using the restricted maximum likelihood method
(REML). The genetic values were predicted using the BLUP method [29].
Data were subjected to individual and joint analyses of variance. To analyze the
individual variance, the statistical model was adopted as follows:

y = Xb + Zg + e

where:
y = data vector;
b = vector of the fixed effects of the blocks added to the general mean;
g = vector of random data effects for genotypes;
e = effect of random vector errors;
and X and Z represent the incidence matrices for vectors b and g, respectively.
Data were standardized using the correction factor obtained for cases where the
coefficients of variation of heritability were verified in a broad sense according to the
following expression described by Resende (2007) [25]:
√ √
h2 ik / h2 t ,

where:
h2ik = the broad sense of individual heritability for characteristic i in the evaluation of k;
and h2t = the broad sense of individual mean heritability to evaluate k for characteristic i.
After standardizing the data, a joint analysis of variance was performed to consider
the genotypes and harvesting according to the following statistical model:

y = Xb + Za + Wc + e

where:
b = vector of the block effects (assumed as fixed) added to the general mean;
a = vector of individual genotypic effects (random);
c = vector of plot effects (randomized);
Horticulturae 2023, 9, 643 5 of 13

e = error vector (aleatory);

and X, Z, and W represent the incidence matrices for the said effects (b, a, and
c, respectively).
Analysis of deviance (ANADEV) was performed to test the significance of the variance
components according to the random effects of the model. The likelihood ratio test (LRT)
was used to implement the variance components, in which the significance of the model
was evaluated using the chi-square test with one degree of freedom [25].
The classification of genotypes simultaneously considering productivity and stabil-
ity was performed using the harmonic mean of the genetic values (HMGV), which was
obtained as follows:
HMGVi = n/ Σn j = 1 1/GV ij
where:
n = the number of months/harvests (n = 7) for which genotype i was evaluated;
and GVij = the genetic value of genotype i in month/harvest j expressed by the ratio
of the mean in the month/harvest.
The genotypes, considering productivity and adaptability, were selected simultane-
ously by the performance of their genotypic values (RPGV) during the months/harvest
obtained by the formula:
∑nj=1 GVij
!
RPGVi = 1/n
Mj

where:
Mj = fruit productivity means during the month/harvest j.
Strawberry genotypes were simultaneously classified in terms of productivity, stability,
and adaptability through the harmonic mean of the relative performance of genotypic
values (HMRPGV), obtained according to the following expression:
n
HMRPGVi =
∑nj=1 RPGV
1
ij

The values of RPGVµ and HMRPGVµ were obtained by multiplying RPGV and HMRPGV
by the general mean of each characteristic and then considering all months/harvests. Thus,
the mean values of the genotype were provided, penalized for instability, and capitalized
by adaptability. Selective precision and selection gains were obtained according to Re-
sende [29]. Statistical model 20 was adopted for individual analyses, which refers to the
evaluation of unrelated genotypes obtained from randomized blocks containing five plants
per plot. In addition, model 55 was used in the conjoint analysis for genotypes in an RBD,
with stability and temporal adaptability for one place and seven months/harvests using the
Selegen REML/BLUP program [29]. From the HMRPGVµ values, a box plot was generated
using the R software with the ggplot2 package.

3. Results
A desirable strawberry cultivar should have good productivity, post-harvest char-
acteristics, disease and pest tolerance, adaptability, and temporal stability, distributing
production uniformly throughout the cultivation period. Adapted and stable genotypes
are typically identified during the final selection cycles, and only those that demonstrate
superiority are tested.
The climate conditions for the experiment cultivation period are shown in Figure 1. The
minimum temperature (daily average) varied from 8.26 ◦ C in July to 17.8 ◦ C in March 2019.
The maximum temperatures varied on a daily average from 20.11 ◦ C in July 2019 to 28.4 ◦ C
in March 2020. The lowest rainfall value was observed in July (0.63 mm as the mean per
day), and the highest was in December (5.04 mm per day). The monthly mean temperatures
gradually increased during the cultivation period, ranging from 14.17 ◦ C at the time of
 The climate conditions for the experiment cultivation period are shown in Figure
The minimum temperature (daily average) varied from 8.26 °C in July to 17.8 °C in Mar
2019. The maximum temperatures varied on a daily average from 20.11 °C in July 2019
28.4 °C in March 2020. The lowest rainfall value was observed in July (0.63 mm as
Horticulturae 2023, 9, 643 mean per day), and the highest was in December (5.04 mm per day). The 6monthly of 13 me
temperatures gradually increased during the cultivation period, ranging from 14.17 °C
the time of transplantation (July 2019) to 21 °C in February 2020 at the end of the harv
transplantation
period (July 2019) to 21 ◦ C in February 2020 at the end of the harvest period
(Figure 1).
(Figure 1).

Figure 1. Rainfall and temperature data of the strawberry experimental location from March 2019 to
Figure 1. Rainfall and temperature data of the strawberry experimental location from March 2
February 2020.
to February 2020.
For the analyses of adaptability and stability of the genotypes, the total mass of fruit
was For
usedthe
for analyses ofof
the analysis adaptability and stability of the genotypes, the total mass of fr
the mixed models.
Significant differences were observed
was used for the analysis of the mixed models. for total fruit mass in the sources of varia-
tion,Significant
genotypes, differences
genotype interactions by harvest
were observed for total time,fruit
and mass
permanent
in theeffects using
sources of variati
deviance analysis based on the likelihood ratio test (Table 2). The interaction between
genotypes, genotype interactions by harvest time, and permanent effects using devian
genotype (G) and environment (E) showed variations in performance among different
analysis based on
harvest periods the likelihood ratio test (Table 2). The interaction between genotype (
(months).
and environment (E) showed variations in performance among different harvest perio
(months).
Table 2. Deviance analysis (ANADEV) for total fruit mass in strawberry genotypes evaluated for
seven months.
From the estimates of the variance components obtained using REML/BLUP, for
total mass of fruit
Variation of the genotypes, heritability
Source Deviance in the broad LRTsense(X2was
) 33%. The me
heritability Genotypes
of the genotypes (79%) was8512.40
superior to broad-sense63.73 heritability.
**
The data p
sented Genotypes
an accuracy of 0.89, which was9019.45
× Months considered high, and 570.78the repeatability
** was 3
Permanent
(Table 3). effect G × E 8492.63 43.96 **
Complete model 8448.67 -
Table 2. Deviance
** significant analysis
at 1% of probability (ANADEV)
by deviance analysisfor total
based on thefruit mass
LRT test (X2 ) with
in strawberry genotypes
1 degree of freedom evaluated
(ttable = 6.63).
seven months.
From the estimates of the variance components obtained using REML/BLUP, for the total
mass ofVariation Source heritability in the broad Deviance LRT (X of )
2
fruit of the genotypes, sense was 33%. The mean heritability
the genotypes Genotypes 8512.40 The data presented an accuracy
(79%) was superior to broad-sense heritability. 63.73 **
of 0.89, which was
Genotypes × Months considered high, and the repeatability
9019.45was 36% (Table 3). 570.78 **
Among the 44 genotypes evaluated, 17 showed positive genetic effects, and their
Permanent effect G × E 8492.63
predicted genotypic values ranged from 128.16 (RVDA11M-25) up to 278.02 (RVFS07M-34)
43.96 **
(Table Complete
4). Throughmodel the analyses based on mixed8448.67 models, the genotypic values were -con-
**sidered
significant at 1% ofthe
to evaluate probability
strawberry bygenotypes
deviance analysis based on
for the general the LRT test
performance in (X
all2) seven
with 1 degree
harvests(tanalyzed
freedom and for the individual performance for each harvest. The 11 best geno-
table = 6.63).
types selected for each harvest period are presented in Table 5. As for overall perfor-
mance, the mean genotypic values ranged from 158.18 g/plant (RVDA11M-13) up to
311.86 g/plant (RVFS07M-34). In general, considering every harvest, genotypes RVFS07M-
34 and RVFS07M-24 were among those selected with the highest values of total fruit mass.
Among the evaluated controls, Monterey, RVCA44, and RVFS07 were selected only in some
specific harvests. Monterey was a unique commercial cultivar (control) ranked among the
Horticulturae 2023, 9, 643 7 of 13

11 most productive genotypes but only in the last harvest (February), whereas, RVCA44
was selected in harvest 1 (August) and harvest 2 (September), and RVFS07 was selected in
harvest 5 (December).

Table 3. Estimation of variance components for total fruit mass in strawberry genotypes evaluated
for seven months of cultivation.

Individual REML Value

Genotypic variance (g2 ) 3483.54
Genotype month variance (gm2 ) 5334.64
Permanent effects variance (perm2) 337.04
Temporary residual variance (e2) 1422.48
Phenotypic variance (f2) 10,577.70
Heritability in the broad sense in the plot (hp2) 0.33
Repeatability (r) 0.36
Mean heritability of genotypes (ahg2) 0.79
Accuracy (A) 0.89
General mean 123.33

Table 4. Predicted genotypic values for total fruit mass obtained from 44 strawberry genotypes.

Genotype u+g1 CI 2
RVFS07M-34 278.02 [222.45; 333.59]
RVFS07M-24 244.71 [189.14; 300.28]
RVDA11M-04 239.54 [183.97; 295.12]
RVFS07M-36 191.39 [135.83; 246.97]
RVFS07M-33 183.14 [127.57; 238.71]
RVFS07M-05 182.46 [126.89; 238.03]
RVFS07M-154 180.29 [124.72; 235.86]
RVFS07M-31 167.46 [111.89; 223.03]
RVFS07M-80 155.91 [100.34; 211.48]
RVFS06AL-132 153.04 [97.47; 208.61]
RVDA11M-13 151.92 [96.35; 207.50]
RVDA11M-21 151.47 [95.90; 207.04]
RVCA16M-01 151.30 [95.73; 206.87]
RVFS07M-32 148.63 [93.06; 204.20]
RVFS07M-10 147.01 [91.44; 202.58]
RVDA11M-03 139.66 [84.09; 195.23]
RVDA11M-25 128.16 [72.59; 183.73]
RVFS07M-124 122.98 [67.41; 178.55]
RVDA11M-32 119.52 [63.95; 175.09]
RVFS07M-16 116.20 [60.63; 171.77]
RVCA16 115.89 [60.32; 171.46]
RVDA11M-10 115.69 [60.12;171.26]
RVFS07M-179 112.89 [57.32; 168.46]
RVFS07M-113 102.96 [47.38; 158.53]
RVCA44 101.42 [45.85; 156.99]
RVFS07M-38 98.73 [43.16; 154.3]
RVFS07 97.12 [41.55; 152.69]
RVFS06 94.68 [39.12; 150.26]
RVFS07M-47 94.41 [38.84; 149.98]
Monterey 93.23 [37.66; 148.80]
RVDA11M-29 91.97 [36.39; 147.54]
RVFS07M-02 91.76 [36.19; 147.33]
RVFS07M-88 91.36 [35.79; 146.93]
RVDA11M-28 90.90 [35.33; 146.47]
Albion 90.58 [35.01; 146.15]
RVFS06AL-36 89.62 [34.05; 146.19]
Horticulturae 2023, 9, 643 8 of 13

Table 4. Cont.

Genotype u+g1 CI 2
RVDA11 87.49 [31.92; 143.06]
RVFS07M-30 85.03 [29.46; 140.60]
RVFS07AL-28 69.84 [14.27; 125.41]
Dover 62.30 [6.73; 117.87]
RVFS07M-151 60.44 [4.87; 116.01]
RVFS06M-29 52.15 [−3.43; 107.72]
RVVFS07M-48 44.64 [−10.93; 100.21]
RVFS07M-42 38.72 [−16.85; 94.29]
1 Predicted genotypic value; 2 confidence interval.

Table 5. Genotype selection in all harvests and in each harvest based on predicted genotypic values
for the total fruit mass obtained from 44 strawberry genotypes.

General Harvest 1 1 Harvest 2 Harvest 3

Genotype u + g + gem 2 Genotype u + g + ge 3 Genotype u + g + ge Genotype u + g + ge
RVFS07M-34 311.86 RVFS07M-47 53.38 RVFS07M-80 119.64 RVFS07M-34 698.39
RVFS07M-24 271.27 RVFS07M-34 38.59 RVFS07M-24 89.84 RVFS07M-05 414.05
RVDA11M-04 264.97 RVDA11M-04 31.38 RVFS07M-36 88.04 RVFS07M-36 379.57
RVFS07M-36 206.28 RVFS07M-24 29.96 RVFS07M-34 85.09 RVFS07M-124 350.38
RVFS07M-33 196.22 RVCA44 29.35 RVFS07M-154 84.26 RVFS07M-179 334.93
RVFS07M-05 195.40 RVFS07M-154 28.26 RVCA16M-01 75.27 RVFS07M-154 302.40
RVFS07M-154 192.75 RVFS07M-80 27.30 RVDA11M-28 65.80 RVDA11M-04 293.37
RVFS07M-31 177.11 RVFS06AL-132 25.62 RVDA11M-03 60.20 RVFS07M-10 263.49
RVFS07M-10 163.04 RVFS07M-36 24.46 RVFS07M-32 58.46 RVDA11N-03 250.05
RVFS06AL-132 159.54 RVFS07M-33 24.00 RVDA11M-21 54.19 RVFS07M-31 250.04
RVDA11M-13 158.18 RVFS07M-113 21.23 RVCA44 50.91 RVFS07M-24 247.47
Harvest 4 Harvest 5 Harvest 6 Harvest 7
Genotype u + g + ge Genotype u + g + ge Genotype u + g + ge Genotype u + g + ge
RVFS07M-34 413.91 RVFS07M-34 563.86 RVDA11M-04 462.95 RVFS07M-24 400.41
RVFS07M-31 405.00 RVFS07M-05 484.49 RVFS07M-24 340.98 RVFS07M-32 334.98
RVDA11M-04 400.64 RVFS06AL-132 442.21 RVFS07M-33 264.74 RVDA11M-04 218.63
RVFS07M-05 393.19 RVFS07M-24 416.42 RVDA11M-13 237.73 RVFS07M-80 200.98
RVFS07M-24 373.76 RVDA11M-04 403.48 RVDA11M-21 218.94 RVFS07M-33 185.94
RVFS07M-33 356.12 RVFS07M-31 397.62 RVFS07M-36 216.65 RVFS07M-34 172.44
RVFS07M-36 332.83 RVCA16M-01 373.02 RVFS07M-34 210.74 RVFS07M-16 154.77
RVFS07M-80 321.29 RVFS07M-36 349.95 RVCA16M-01 202.61 RVFS07M-154 153.83
RVFS07M-154 312.29 RVFS07M-154 341.10 RVDA11M-25 186.88 Monterey 152.35
RVDA11M-13 294.86 RVFS07M-33 331.10 RVDA11M-10 152.20 RVDA11M-21 128.65
RVDA11M-21 289.38 RVFS07 317.73 RVDA11M-03 151.93 RVDA11M-25 125.97
1 Harvest 1 = August; harvest 2 = September; harvest 3 = October; harvest 4 = November; harvest 5 = December;
harvest 6 = January; harvest 7 = February; 2 mean genotypic value in 7 harvests that capitalizes the mean
interaction with all evaluated harvests; 3 predicted genotypic value in each harvest, i.e., the genotypic values
capitalizing the interaction with the harvests.

Mean genotypic values penalized by instability and capitalized by adaptability were

obtained. Data dispersion showed the 11 genotypes that stood out from the others
(Figure 2). They had the highest yields and were the most stable and adaptable: RVFS07M-
34, RVFS07M-24, RCDA11M-04, RVFS07M-154, RVFS07M-36, RVFS07M-33, RVFS07M-80,
RVFS07M-10, RVDA11M-21, RVDA11M-13, and RVFS06AL-132. This demonstrated the
potential of theses genotypes as commercial cultivars.
When considering the means of each harvest separately, the RVFS07M-34 (Figure 3)
genotype stood out as always being among the seven best in all harvests. It had the
highest predicted genotypic value (278.02 g/plant) and the highest mean genotypic value
(311.86 g/plant) (Table 4 and Table 5, respectively). The RVFS07M-24 hybrid also showed
high performance in almost all harvests, except in harvest 3 (October) (Table 5). In ad-
dition, RVFS07M-24 had the highest production stability in several harvesting periods,
such as harvests 4 (November, 373.76 g/plant), 5 (December, 416.42 g/plant), 6 (January,
340.98 g/plant), and 7 (February, 400.41 g/plant).
 RVFS07M-80 321.29 RVFS07M-36 349.95 RVCA16M-01 202.61 RVFS07M-154 153.83
RVFS07M-154 312.29 RVFS07M-154 341.10 RVDA11M-25 186.88 Monterey 152.35
RVDA11M-13 294.86 RVFS07M-33 331.10 RVDA11M-10 152.20 RVDA11M-21 128.65
RVDA11M-21 289.38 RVFS07 317.73 RVDA11M-03 151.93 RVDA11M-25 125.97
1 Harvest 1 = August; harvest 2 = September; harvest 3 = October; harvest 4 = November; harvest 5 =

Horticulturae 2023, 9, 643 December; harvest 6 = January; harvest 7 = February; 2 mean genotypic value in 7 harvests that cap- 9 of 13
italizes the mean interaction with all evaluated harvests; 3 predicted genotypic value in each harvest,
i.e., the genotypic values capitalizing the interaction with the harvests.

Horticulturae 2023, 9, x FOR PEER REVIEW 10 of 14

Figure 2. Box plot of adaptability and stability of the 44 evaluated genotypes of strawberry.
Figure 2. Box plot of adaptability and stability of the 44 evaluated genotypes of strawberry.

Figure 3. Morphoagronomic
Figure 3. Morphoagronomic aspects
aspects of
of genotype
genotype RVFS07M-34
RVFS07M-34 developed
developed with
with high
high yield, stability,
yield, stability,
and temporal adaptability. (A) Production; (B) plant size, architecture, and flowering; (C) pseudo-fruit
and temporal adaptability. (A) Production; (B) plant size, architecture, and flowering; (C) pseudo-
shape; (D) pseudo-fruit
fruit shape; internal
(D) pseudo-fruit and external
internal colors.colors.
and external

4. Discussion
4. Discussion
Currently, strawberry cultivation in the southern hemisphere is based on cultivars
Currently, strawberry cultivation in the southern hemisphere is based on cultivars
from international breeding programs, which leads to market dependence and vulnerabil-
from international breeding programs, which leads to market dependence and vulnera-
ity [11,30], since the cultivars are not well adapted to the climate, and they do not express
bility [11,30], since the cultivars are not well adapted to the climate, and they do not ex-
their maximum genetic potential. These cultivars have low productivity in tropical and
press their maximum genetic potential. These cultivars have low productivity in tropical
subtropical conditions, due to their lack of adaptability and stability throughout the year,
and subtropical conditions, due to their lack of adaptability and stability throughout the
especially during the warmest periods [1].
year, especially during the warmest periods [1].
To reduce dependence on imported cultivars and rescue the genetic sovereignty of the
To reduce dependence on imported cultivars and rescue the genetic sovereignty of
species, research has focused on the development of new strawberry genotypes classified
the species, research has focused on the development of new strawberry genotypes clas-
as day-neutral and adapted to tropical and subtropical growing conditions [2].
sified as day-neutral and adapted to tropical and subtropical growing conditions [2].
The analysis of deviance in relation to total fruit mass in strawberry genotypes was
The analysis
significant for the of deviance
effects in relationpermanent
of genotype, to total fruit mass and
effects, in strawberry genotypes
the interaction was
between
significant for the effects of genotype, permanent effects, and the interaction between gen-
otype and environment, demonstrating the presence of genetic variability among straw-
berry genotypes tested for the variable total fruit mass in response to harvest periods.
Therefore, it was possible to carry out the selection of more stable genotypes for produc-
tion throughout the year, which was also observed for strawberry genotypes with low
Horticulturae 2023, 9, 643 10 of 13

genotype and environment, demonstrating the presence of genetic variability among straw-
berry genotypes tested for the variable total fruit mass in response to harvest periods.
Therefore, it was possible to carry out the selection of more stable genotypes for pro-
duction throughout the year, which was also observed for strawberry genotypes with
low chilling requirements [2], guaranteeing market fruit all year round and reducing the
off-season period.
A significant interaction demonstrated the occurrence of a difference in the ranking of
the genotypes in the different harvest months, indicating a complex interaction between
the genotypes and the environment. According to Allard and Bradshaw [31], this type of
interaction is caused by unpredictable variations in the environment, such as precipitation,
temperature, relative humidity, the occurrence of pests and/or diseases, and even the
production system used for cultivation. The significance in the interaction was evident
when highlighting the climatic variation between the harvest months evaluated, when
they occurred in three seasons of the year (winter, spring, and summer) in the southern
hemisphere. The harvest seasons occurred from August (winter), September to December
(spring), and February (summer), when temperatures were relatively high, and the pho-
toperiod was long between the equator and the Tropic of Capricorn. Significant interaction
results between strawberry genotypes and harvest environments have already been de-
scribed in several studies [32,33]. The results underscored the importance of adaptability
and stability studies in strawberry cultivars as a basic precept for recommending a cultivar
developed by a breeding program [11,34,35].
The propagation of genetic material in a vegetative way in strawberry breeding programs
makes it possible to take advantage of genetic variance, whether of an additive, dominant, or
epistatic nature [36]. However, it is still important to consider the genotype × environment
interaction. The interaction generates uncertainties in heritability estimates, correlations
(genetic, phenotypic), and expected gains with selection, mainly for quantitative traits, such as
total fruit mass. The effect of the complex genotype × environment interaction can be reduced
by developing cultivars with greater stability and production adaptability [36], especially
when the objective is to explore strawberry cultivation in a wide range of latitudes.
The broad-sense heritability of plot (hp2) of 33% was considered high (h2 > 0.3 = high) [26],
demonstrating good genetic control of the quantitative characteristic total fruit mass. In
Table 2, the representations of additive, dominant, and epistatic h2 are observed. The
cultivated strawberry species (Fragaria × ananassa) was octaploid; most characteristics were
under polygenic control and were highly influenced by the cultivation environment [37,38].
In a study evaluating productivity and its main components in strawberry cultivated in
a subtropical climate, the authors observed heritability values in the broad sense ranging
from 0.01 to 0.63 [11]. Previous studies found broad-sense heritability values above 70% for
productivity in strawberry cultivars [14,15]. Therefore, the heritability results found in the
present research corroborate several studies already described in literature.
Repeatability tends to be greater than broad-sense heritability, reaching the maximum
value that broad-sense heritability can reach [39]. For example, one study observed her-
itability values of 74.81, 85.17, and 98.44% for the number of fruits per plant, mean fruit
mass, and productivity, respectively [15].
Our results showed a high value for accuracy, demonstrating the experimental re-
liability of this research. Accuracy is the most suitable parameter for determining the
proportions between variations of a genetic nature and residual quantitative traits [26].
Based on the harmonic mean of the relative performance of genotypic values
(HMRPGV) method, which considers the genotype means and the variation of this mean
along the environments, the 11 best genotypes were selected (Figure 2) for the variable
total fruit production, as well as stability and adaptability throughout the harvest periods.
The selected genotypes were RVFS07M-34, RVFS07M-24, RVDA11M-04, RVFS07M-154,
RVFS07M-36, RVFS07M-33, RVFS07M-80, RVFS07M-10, RVDA11M-21, RVDA11M-13, and
RVFS06AL-132 (Figure 2). Among them, only RVFS06AL-132 did not have Monterey as
Horticulturae 2023, 9, 643 11 of 13

a female parent. Furthermore, RCDA11M-04, RVDA11M-13, and RVDA11M-21 featured

Dover in the male parent’s genealogy, while the others had Festival in their genealogy.
Aromas was in the genealogy of all male parents used in this study. Camarosa
and Aromas cultivars have been described as the most adapted and stable commercial
strawberry cultivars [36]. These cultivars probably have additive alleles already fixed for
stability and adaptability characteristics, which are inherited by the progeny, since the
mean h2 of the genotypes was 79%.
Productivity is a quantitative trait of polygenic inheritance with great influence from
the environment [37], which can explain the variation in the ranking of genotypes among
harvest periods. The experimental genotypes were superior to the commercial cultivars
used in the experiment. Monterey was a unique cultivar ranked among the top 11 genotypes
and only in the last harvest. The superiority of the experimental genotypes was due to the
strawberry breeding program being developed in a soil and climate condition similar to
the cultivation area. These results indicate the importance of plant selection occurring as
closely as possible in the cultivation environment. A previous study evaluated advanced
genotypes of day-neutral strawberries, where crosses were also performed with genotypes
RVFS07, RVFS11, and Monterey. Our results agree with this study, as we obtained similar
results [2].
The RVFS07M-34 hybrid was the most productive genotype, with greater stability and
adaptability, and was classified among the five best genotypes in harvests 1–5 (August to
December). A study evaluating strawberry genotypes in two seasons with three different
environments obtained significant results for the components of environmental variations
and interactions [35]. According to the same authors, abiotic and biotic factors, such as
temperature variation, relative humidity, pests, and diseases, can interfere with the results,
and they play an important role in the environmental variation for strawberry production.
Strawberry is a microclimatic crop, and the cultivars’ behaviors can vary depending
on many agronomical and environmental factors (climate conditions and season) [39],
highlighting the importance of our study, which analyzed several harvest periods.

5. Conclusions
The use of the mixed linear model methodology to study adaptability and stability
showed the superiority of 11 genotypes that had the potential to be released as cultivars.
In addition, RVFS07M-34, being the most promising, will be chosen to follow the legal
procedures with the official cultivar registration agency.

Author Contributions: D.A.N. performed the experiments and wrote the manuscript. Field man-
agement activities, collection, and data analysis were carried out by D.A.N., G.C.G., L.V.B.d.O. and
G.F.d.P.G.; A.R.Z., S.T.I.-S. and K.H.M. helped with the experimental design, statistical analysis,
and final review of the manuscript. S.R.R. assistance in the interpretation of post-harvest data and
writing of the paper, J.T.V.d.R. was responsible for the Strawberry Breeding Program for tropical
and subtropical climates (project coordinator and research creator) and obtained funding, assisted
in writing, and reviewed the final manuscript. All authors have read and agreed to the published
version of the manuscript.
Funding: We are especially grateful to the National Research Council (CNPq), Fundação Araucária
(FA), and the Superintendence of Higher Education, Science and Technology of the State of Paraná
(SETI) for their financial support. J.T.V.R. and S.R.R. thank CNPq for the research grant.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: Not applicable.
Conflicts of Interest: The authors declare that they have no political, personal, religious, ideological,
academic, intellectual, commercial, or any other competing interests.
Horticulturae 2023, 9, 643 12 of 13

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