agronomy

Article
Multi-Trait Selection Indices for Identifying New Cassava
Varieties Adapted to the Caribbean Region of Colombia
Rommel León 1 , Amparo Rosero 2, * , Jorge-Luis García 2 , Julio Morelo 2 , Alfonso Orozco 1 , Gabriel Silva 1 ,
Víctor De la Ossa 2 , Ender Correa 1 , Carina Cordero 3 , Leonardo Villalba 4 , John Belalcazar 5 and
Hernán Ceballos 5

1 Centro de Investigación Caribia, Corporación Colombiana para la Investigación Agropecuaria-AGROSAVIA,

Sevilla-Zona Bananera, Magdalena 478020, Colombia; [email protected] (R.L.);
[email protected] (A.O.); [email protected] (G.S.); [email protected] (E.C.)
2 Centro de Investigación Turipana, Corporación Colombiana para la Investigación
Agropecuaria-AGROSAVIA, Kilómetro 13, Vía Montería-Cereté 230558, Colombia;
[email protected] (J.-L.G.); [email protected] (J.M.); [email protected] (V.D.l.O.)
3 Centro de Investigación Motilonia, Corporación Colombiana para la Investigación
Agropecuaria-AGROSAVIA, Kilómetro 5 vía a Becerril, Agustín Codazzi 202050, Colombia;
[email protected]
4 Centro de Investigación La Suiza, Corporación Colombiana para la Investigación Agropecuaria-AGROSAVIA,
Kilometro 32 via al mar, Rionegro 687519, Colombia; [email protected]
5 CGIAR Research Program on Roots Tubers and Bananas (RTB), The Alliance of Bioversity International and
the International Center for Tropical Agriculture (CIAT), Cali 6713, Colombia; [email protected] (J.B.);
[email protected] (H.C.)



* Correspondence: [email protected]



Citation: León, R.; Rosero, A.; García, Abstract: In Colombia, the highest cassava production comes from the semi-arid region of the Atlantic
J.-L.; Morelo, J.; Orozco, A.; Silva, G.; Coast with relatively low yield for fresh consumption (≤11 t/ha). Development of improved varieties
De la Ossa, V.; Correa, E.; Cordero, C.; is based on a plant ideotype which integrates a group of desirable traits independently measured
Villalba, L.; et al. Multi-Trait Selection
in the field. However, selecting high performance genotypes for several traits simultaneously is a
Indices for Identifying New Cassava
complex process. Sixteen genotypes were evaluated under four environmental conditions (localities)
Varieties Adapted to the Caribbean
of the Colombian Caribbean region (Cereté, Carmen de Bolivar, Agustín Codazzi, and Sevilla),
Region of Colombia. Agronomy 2021,
and two production cycles (2016/2017–2017/2018) in order to assess phenotypic expression of
11, 1694. https://doi.org/10.3390/
agronomy11091694
selected traits, their stability, and utility in genotype selection. Selection of promising genotypes
should consider both their superiority and stability. Genotypes SM3106-14, GM1692-56, CM9456-
Academic Editor: Pasquale Tripodi 12, and GM214-62 were selected based on their agronomic performance. In addition, frequency
analysis of sensorial data showed that genotypes CM9456-12, SM1127-8, SM3553-27, and SM3562-32
Received: 10 July 2021 were preferred by panelists who assessed, color, flavor, texture, and root shape. Determination of
Accepted: 13 August 2021 superiority through across-environments, multi-trait selection index allows identifying genotypes
Published: 25 August 2021 with superior performance. However, selection was improved when local multi-trait selection
indices were included—phenotypic stability determination (through Lin and Binns index and AMMI
Publisher’s Note: MDPI stays neutral model) supported an adequate selection of superior and stable cassava genotypes. The inclusion of
with regard to jurisdictional claims in
palatability response and quality features determination in cassava genotypes can be recommended
published maps and institutional affil-
to identify genotypes with higher adoption rates by farmers and consumers.
iations.

Keywords: AMMI model; fresh consumption; Lin and Binns index; phenotypic stability; varietal
adoption

Copyright: © 2021 by the authors.

Licensee MDPI, Basel, Switzerland.
This article is an open access article
1. Introduction
distributed under the terms and
conditions of the Creative Commons
Cassava is considered a staple food for more than 1 billion people worldwide. Further-
Attribution (CC BY) license (https:// more, regarding alternative sources of energy, the caloric intake from cassava is higher than
creativecommons.org/licenses/by/ that provided by different cereals and legumes. Therefore, the crop has become essential
4.0/). for the food security of developing countries, particularly in sub-Saharan Africa. In terms

Agronomy 2021, 11, 1694. https://doi.org/10.3390/agronomy11091694 https://www.mdpi.com/journal/agronomy

Agronomy 2021, 11, 1694 2 of 23

of per capita consumption, Colombia occupies the tenth place worldwide reporting an
average of 38.5 kg per person per year [1]. In Latin America, approximately 45% of the
area cultivated with cassava corresponds to regions with limited water availability or
sporadic rainfall cycles [2]. Cassava is cultivated in all the regions of Colombia, finding in
the semiarid environments the highest yields.
The genetic improvement in crops has generated the highest rates of returns in agri-
cultural research. Cassava breeding programs date back to the year 1930 initially in African
countries and in Brazil, but these efforts were discontinuous throughout the years. Only
after the 1960s, there was a rapid expansion in the use of cassava genetic resources from
Asia, Africa, and Latin America thanks to the creation of the International Institute of
Tropical Agriculture (IITA) and the International Center for Tropical Agriculture (CIAT) [3].
National cassava programs also became very active during the 1970s.
Selection in multi-environmental conditions such as contrasting seasons, either at the
same location or at different sites, has been used to expose materials to a broad range of
potential production environments. Therefore, although crop cultivars are bred in and for
specific regions, they need to be adapted to weather variability within those regions, both
within and across years [4]. This is especially the case where production areas have different
edapho-climatic conditions, are susceptible to suffer the effects of large-scale climatic events
and planting time is defined by seasonality and rainfall availability [5]. In cassava, uniform
yield trials are planted for 2 consecutive years in 5–10 locations, this typically to identify
and select superior, stable and high-yielding cultivars with high potential commercial
use [3]. Farmer and end user criteria are used during each step of selection, and they are
invited to participate for more intensive input and interaction with breeders during the
harvest [3].
Several economically relevant traits in cassava are inherited quantitatively, and the
phenotypic variance is influenced by the effects of the joint action of the genotype, the envi-
ronment and the genotype by environment interaction (G × E), as described by [6]. Single
environment results are ineffective improving quantitative traits, since the identification
of superior cultivars should take into consideration and be based on an G × E interaction
analysis as well as in their phenotypic stability [7]. Phenotypic stability is desirable during
cultivar selection for a predictable behavior in varying environmental conditions. Among
the methodologies commonly used for this purpose, the ones published by [8–11] and
recently the AMMI model [12–14] could be highlighted.
In addition to appropriate consideration of G × E interaction, breeders need to con-
sider several traits simultaneously. The use of multi-trait selection indices facilitates the
integration of several desirable attributes determined by the breeder cultivar ideotypes
can then be selected according to their genetic superiority and phenotypic stability [15,16].
The application of accurated indices promote the efficiency of the selection [17,18]. The
integration of several characteristics in a selection index favors the identification of superior
genotypes that are expected to have a positive impact on the value chain of a crop, hence,
enhancing the adoption rate of the released varieties [17,19]. In cassava, [3] reported the
use of a selection index considering agronomic aspects of the crop, such as total fresh root
yield, dry matter content, plant type, response to diseases and harvest index.
This study shows the potential of integrating different tools and calculations of se-
lection indices that allows the identification of promising cassava genotypes with high
potential for fresh consumption evaluated in multi-location trials.

2. Materials and Methods

2.1. Plant Material
Fourteen improved experimental clones (CM9456-12, CMB8527, GM1692-56, GM214-
62, GM3766-5, GM3790-2, SM1127-8, SM2773-32, SM3106-14, SM3385-55, SM3386-49,
SM3387-73, SM3474-139 and SM3553-27) developed at International Center for Tropical
Agriculture (CIAT) and two commercial checks (CORPOICA CAISELI and ICA-COSTEÑA)
were evaluated through uniform yield trials (UYT). The nomenclature used to identify each
Agronomy 2021, 11, 1694 3 of 23

genotype indicates that CM, GM or CMB clones come from controlled pollinations with
known male and female progenitors. On the other hand, SM indicates materials derived
from open pollination nurseries and thus only the female progenitor is known.

2.2. Study Area

The study was conducted in four locations of the Colombian Caribbean region cor-
responding to four locations: Agustín Codazzi (Codazzi), Carmen de Bolivar (CarmenB),
Cereté (Cerete), and the Zona Bananera (Sevilla), corresponding to the departments Cesar,
Bolívar, Córdoba and Magdalena (Figure 1), respectively, during two production cycles
(2016/2017-2017/2018), except in Coddazi, where it was not established in 2016 due to
administrative issues. Soil fertility and other characteristics of the study area are described
in Table 1.

Figure 1. Study area showing locations with geographical and altitudinal information.
Agronomy 2021, 11, 1694 4 of 23

Table 1. Locations description and soil fertility.

Features * Units Codazzi Cerete Carmen B Sevilla

10◦ 000 01.200 N, 8◦ 500 27.4700 N, 9◦ 420 50.800 N, 10◦ 470 35.400 N
Coordinates
73◦ 150 22.400 W 75◦ 480 27.5600 W 75◦ 060 26.900 W 74◦ 100 49.900 W
Mountains and
Topography Piedmont Plain Plain
Piedmont
Mean temperature (◦ C) 28.1 27.7 26.9 28
Annual rainfall (mm) 1560 1264 1179 1280
Relative humidity (%) 89 82 80 82
Altitude (m.a.s.l.) 135 12 197 18
Soil characteristics Texture Sandy-loam Clayed Clay-loam Plain
pH 7.84 6.99 7.18 6.39–6.4
OM % 1.66 2.87 2.55 0.77–1.55
P mg/kg 150.30 10.09 28.83 14.5–30
Ca cmol(+)/kg 13.04 14.79 21.74 9.97–7.51
Mg cmol(+)/kg 1.14 6.11 6.69 1.36–1.19
K cmol(+)/kg 0.31 0.50 0.20 0.14–0.10
EC dS/m 0.61 0.92 0.20 0.20–0.21
* pH water: Soil 2.5: 1.0, organic matter (OM), phosphorus (P) [Bray II], calcium (Ca), magnesium (Mg), potassium (K), electrical conductivity
(CE) relation 2.5:1.0.

2.3. Experimental Design and Management

The study was conducted during two crop cycles: (i) July 2016–April 2017 and (ii) June
2017–March 2018. The experiment employed a completely randomized block design
(CRBD) with three replicates. The experimental unit per genotype was a plot of 25 m2
with a conventional spatial arrangement of five rows of 5 m spaced at 0.9 m with the
same distance between plants (25 plants per genotype per block). Soil preparation and
planting were carried out according to the edaphological and agroclimatic conditions
of each zone. Weed management included the application of pre-emergent herbicides,
graminicides, and with a screen for herbicides that can cause phytotoxicity to the crop.
The fertilization was done according to the results of the soil analysis of each location
and considering the management that the farmer conventionally offers to the crop. All
parameters were evaluated using the central plants from each plot (nine plants). Plant type
was evaluated using a scale: (1) Clearly better than the average; (2) Slightly better than
the average; (3) Average; (4) Slightly worse than the average; (5) Clearly worse than the
average [3]. Total and commercial fresh root yield was calculated from parameters taken
per plot (commercial and total root weight), dry matter content was calculated according
to the gravimetric method [20].

2.4. Cooking and Sensory Test

After agronomic evaluation and cyanide estimation, a preliminary selection was done
to establish a trial during crop cycle 2018–2019 to produce roots for sensory evaluation.
Cassava roots of uniform shape and weight were randomly selected, carefully washed, and
left to dry in open air. Sections with length and diameter of approximately 5 cm extracted
from the middle of three roots were peeled and cooked. After 10 min of boiling and every
5 min thereafter, softness was evaluated using a toothpick. The time required to soften
the root was registered and used to prepare a sample for sensory test (approximately 20 g
samples). A hedonic scale was used to sensorially assess the cooking quality of roots
from different genotypes. The scale had five categories ranging from “extremely dislike”
to “extremely like”. It was used to produce preference evaluation based on a 9-point
hedonic scale [21]. Cassava consumers (n = 90) were recruited to evaluate roots from
Agronomy 2021, 11, 1694 5 of 23

11 of the experimental clones (CM9456-12, CMB8527, GM1692-56, GM3790-2, SM1127-8,

SM3106-14, SM3387-73, SM3386-49, SM3474-139, SM3553-27, and SM3562-32) and three
commercial checks (Corpoica Caiseli, ICA-Costeña, and Venezolana). Venezolana variety
was introduced in this experiment due to its high culinary attributes and preference by
consumers. Roots from GM214-62, GM3766-5, and SM3385-55 were not evaluated. The
order of sample presentation was randomized. The consumers were briefed on the hedonic
scale and its use prior to sample testing, and also received a glass with ambient temperature
water to cleanse their mouth between sample testing. Participants were asked to evaluate
the color, flavor, and texture for each sample. Finally, a whole representative root from each
genotype was exhibited to be evaluated and scored according to the root shape and other
morphological traits that end users take into consideration.

2.5. Quantification of Cyanide Content

Cyanide content was determined by the methodology described by [22]. Orthophos-
phoric acid, ethanol, sodium hydroxide, hydrogen cyanide were obtained from Merck
(Billerica MA, 01821 USA) and chloramine T, 1,3-dimethyl barbituric acid and isonicotinic
acid were obtained from Sigma-Aldrich (St. Louis, MO 68178 USA). Forty grams of grated
pulp from fresh roots was homogenized in a blender (Osterizer, model 4655, Ciudad de
Mexico, Mexico) with 50 mL of an extracting solution consisting of 0.1 M orthophosphoric
acid in a 25% (v/v) ethanol-water mixture for 2 min. The resulting mixture was centrifuged
(Eppendorf 5804R, Hamburg, Germany) at 6000 RPM for 10 min at room temperature, then
filtered with Whatman No. 1 paper. In addition, 0.1 mL was taken and added to a test
tube containing 0.4 mL of a phosphate buffer solution (0.1 M, pH 7.0) and then, 0.1 mL
of the enzyme Linamarase (isolated and prepared according to Cooke’s (1978) method)
was added. The tube was incubated at 30 ◦ C for 15 min, when 0.6 mL of 0.2 M NaOH was
added and was left for 5 min at room temperature. Then, 2.8 mL of pH 6.0 buffer solution
was added and 0.1 mL of chloramine T was incubated for 5 min at room temperature. In
addition, 0.6 mL of reactive color (solution of 1,3-dimethyl barbituric acid and isonicotinic
acid) was added, homogenized in a vortex, and allowed to react for 10 min. Absorbance
was observed in a spectrophotometer at 605 nm at room temperature. The total HCN
content was quantified with 5 points on a calibration curve (0.015–0.363 µg HCN/mL),
where the result is expressed in µg HCN/g fresh root.

2.6. Determination of Total Starch and Glucose Contents

The starch content was determined according to the methodology suggested by [23],
with some modifications. The Termamyl 2X enzyme (thermostable α-amylase, Novo A/S,
Copenhagen, Denmark) was used for this analysis. Sodium acetate, glucose and sulfuric
acid were obtained from Merck (Billerica, MA 01821, USA) and amyloglucosidase, GOD-
POD reagent were obtained from Sigma-Aldrich (St. Louis, MO, USA). Five hundred
milligrams of cassava flour were weighed in a 125 mL Erlenmeyer flask, and then 30 mL
of deionized water were added, gently stirred for 10 min with the help of a magnetic
stirrer. In addition, 100 µL of Termamyl 2X was added and the suspension was stirred for
5 min. The Erlenmeyer with the mixture was taken in a thermal bath at 98 ◦ C for 20 min,
mixing every 5 min. The cold suspension was transferred to a 100 mL volumetric balloon
with deionized water, 500 µL of the above solution were taken in test tubes, and a blank
was prepared with 500 µL of deionized water. Then, 1 mL of amyloglucosidase solution
(amyloglucosidase from Aspergillus niger, lyophilized, powder, ~70 U/mg Sigma-Aldrich,
(St. Louis, MO, USA).) prepared at 0.5 mg/mL in 0.1 M sodium acetate buffer (pH 4.8) was
added to each tube. The tubes were incubated at 60 ◦ C for 30 min. Once cooled, 8.5 mL
of deionized water was added and vortexed. A 75 µL aliquot of the above solution was
obtained and transferred to another test tube, adding 1.5 mL of the GOD-POD reagent,
(4-amino-antipyrine, Ref. A4382; GO, Glucose oxidase Ref. G6125-50 KU, POD, peroxidase
Ref. P8112-25KU) incubating at 37 ◦ C for 10 min, a blank with water was prepared. The
samples were read at an absorption of 510 nm (BioTek Instruments, Inc. Highland Park,
Agronomy 2021, 11, 1694 6 of 23

IN, USA). The glucose content is quantified by means of a calibration curve prepared with
5 points (0.5–25 µg glucose/mL). In addition to this, it was necessary to determine the
content of free glucose, weighing 100 mg in a test tube to which 1 mL of sulfuric acid
(0.005 M) was added, stirring in a vortex for 1 min. Followed by centrifugation at 7000 rpm
for 3 min, the supernatant was membrane filtered (0.22 µm), 100 µL of the extract were
needed in test tubes, 200 µL of the amyloglucosidase solution were added, after 30 min of
reaction, 2.5 mL of the GOD-POD solution were obtained, and the mixture was incubated
for 20 min at room temperature. After the reaction, the absorbance reading at 510 nm is
required to determine glucose with the aid of calibration as specified above. Where: Total
starch (% w/w, db), CT is total glucose (% w/w, db), FG is free glucose (% w/w, db), and
0.9 is the factor to conversion between starch and glucose.
Total starch content was calculated using the following equation:

Total Starch = (CT − FG) × 0.9

2.7. Analysis of Variance

A combined analysis of variance (ANOVA) was performed to detect the significance of
the sources of variation for each variable, followed by a multiple comparison analysis using
the R program [24]. The statistical model used to analyze the data was with mixed effects
(genotypes fixed, and locations, seasons and blocks random). Since the individual effect of
locations and growing seasons had marginal interest for this research, the combination of
location and growing season was considered as a single environment (for a total of seven
environmental conditions in the study):

Yijk = u + αi + β j (αi ) + ik + (αi )ik + ε ijk (1)

where Yij corresponds to the response variable, u is the general average of the experiment,
αi is the effect of the ith environment, β ij corresponds to the effect of the jth block within
the ith environment, ik is the effect of the kth genotype, (αi )ik is the effect of the interaction
of the ith environment with the kth genotype, and ε ij is the experimental error in the ith
environment, in the jth block under the kth genotype.

2.8. Stability and Phenotypic Adaptability Analysis

Stability and phenotypic adaptability of the genotypes were established for yield data
and its components, using the method of [9]. The most stable varieties were those that
showed the value for the stability parameter statistic of a given cultivar (Pig) closer to zero.
Equation (2) was used to obtain the stability parameter statistic:
n
( X i ( j) − M ( j))2
Pig = ∑ Pi 2n
(2)
J =1

where Pig is the stability parameter statistic of the cultivar i, Xi(j) is the response of the
dependent variable of the ith cultivar in the jth location, Mj is the maximum observed
response among all the cultivars in location j, and n is the number of locations. These results
were contrasted with the estimation of phenotypic stability by the AMMI multi-variate
analysis method, using the routine proposed by [25,26]. This analysis allowed selecting the
best cassava genotypes adapted to the target environment (Caribbean Coast).

2.9. Selection Index

The standardized selection index (SIN) integrated relevant variables by assigning a
weight established by the breeder following the methodology proposed by [3]. A negative
weight was assigned to the plant type score (PTS), considering that high values were
Agronomy 2021, 11, 1694 7 of 23

assigned to undesirable morphotypes. Commercial fresh root yield (CFRY) and dry matter
content (DMC) were also considered. The equation was then represented as follows:

SI N = (CFRY × 10) + ( DMC × 10) − ( PTS × 5) (3)

The desirable genotypes were those that showed the highest value for the SIN.

3. Results and Discussion

The Caribbean Coast region is characterized by high temperatures. Maximum tem-
peratures ranging between 35–40 ◦ C, minimum between 20–25 ◦ C, and average around
28 ◦ C were recorded (Table 2). Cassava growth requires in its first vegetative phase at least
300 mm of water, rain fall was sufficient throughout the crop cycle in the different trials.
Cereté, Seville, and Codazzi showed an accumulated rainfall above 900 mm, Carmen de
Bolívar had the lowest rainfall values, but were still acceptable for cassava (Table 2). The
observed environmental conditions presented in all locations met the expectation for this
agroecological region and were suitable for the germplasm evaluated.

3.1. Response of Cassava Genotypes to Different Environmental Conditions

Most of the evaluated genotypes showed adequate sprouting (>80%), except SM1127-8,
which exhibited a reduced sprouting. The environmental conditions at Sevilla and Carmen
de Bolívar promoted higher sprouting, in comparison with Cereté and Codazzi. However,
averages were not below 90%. Plant height was >200 cm in all genotypes (Figure 2a).
Although this trait is not directly included in the selection index, it is an important com-
ponent of PTS. Excessively high plants are undesirable due to increased vulnerability to
lodging [27,28]. Interestingly, the tallest genotype (SM1127-8) showed the lowest sprout-
ing, possibly since an excessive plant height increases lodging which, in turn, promotes
early sprouting in pre-harvested plants. CM9456-12, CMB8527, GM3790-2, SM2773-32,
SM3106-14, SM3386-49 and SM3474-139 showed plant heights comparable to commercial
varieties (Corpoica-Caiseli and ICA-Costeña). The environmental conditions at Sevilla
and Carmen de Bolívar promoted higher plant height, whereas in Codazzi, plants showed
lower average height (Figure 2b).
The environment, genotype, and G × E interaction sources of variation were highly
significant (p < 0.01) for total root yield (TRY), CFRY, and DMC (Table 3). The environmental
effect (combination of location and season) had the highest contribution to the variance
of the model. A significant proportion of the phenotypic expression of the genotypes,
therefore, was influenced by the environmental conditions where they were evaluated.
However, the significant effect of genotype on total variation was demonstrated. CM9456-
12, GM1692-56, GM214-62, GM3766-5, SM1127-8, SM3106-14, SM3385-55, SM3386-49, and
SM 3553-27 showed higher overall averages in total root yield (Figure 3a, Table 4). In
terms of commercial yield, genotypes SM 3106-14, SM 3553-27, and SM 3386-49 stood out.
Significant differences were found between locations (Tables 3 and 4, Figure 3b). Cereté
in the year 2017 showed the highest average for the total and commercial yield of 55.3
and 34.5 t/ha, respectively, followed by Sevilla 2016 (43.9 and 26.4 t/ha, respectively) and
Carmen 2016 (30.5 and 21.3 t/ha, respectively).
Agronomy 2021, 11, 1694 8 of 23

Table 2. Climatic conditions during evaluation period in four locations in the Caribbean Coast region of Colombia.

Cereté Carmen B. Sevilla Codazzi

Year Month Temperature (◦ C) Rain Temperature (◦ C) Rain Temperature (◦ C) Rain Temperature (◦ C) Rain
Max Min Media (mm) Max Min Media (mm) Max Min Media (mm) Max Min Media (mm)

Cycle 1 (July 2016–April 2017)

2016 JUL 35.5 21.6 28.4 116.6 21.6 37.6 29 76.2 37.7 21.6 29 76.5 36.8 24.7 30.1 69
2016 AUG 36.5 22 28.5 160.9 21.4 37.6 28.8 173.9 37.5 21.9 29.4 130.3 35.9 24.1 29.7 186.6
2016 SEP 35.3 21.8 28 111.4 21.4 36.4 27.3 72.2 37.3 22.1 28.8 142.7 33.9 23.7 28.7 173
2016 OCT 37.5 22.2 28.7 153.3 21.6 35.2 27.4 180.2 35.2 20.8 27.9 423.9 32.5 23.2 27.1 316.8
2016 NOV 33.1 22.4 27.8 110.6 20.4 34 27 158.6 35.4 21.6 28.1 196.9 32.4 22.7 27.6 272.4
2016 DEC 37 22.2 28.6 167 19.4 35.6 27.1 9.4 34.6 20.4 27.7 1.2 34.2 22.3 28 38.7
2017 JAN 35.7 19.2 28 12.91 17.2 36.6 27 0 34.8 17.9 27.1 0 35.6 21.7 29 10.6
2017 FEB 37.4 20.6 28.7 0 18 38 28 9.7 36.8 17.9 27.8 0 36.8 22.5 29 11
2017 MAR 36.2 22.7 28.8 47.5 20.6 39 28.7 51.1 36.4 21.1 28.7 0 35 24.1 29.6 66.4
2017 APR 40 22.4 29.1 198.6 21.6 37.4 29.1 37.2 37.8 22.4 29.4 0 35.3 24.5 29.7 153.3
Mean 36.42 21.71 28.45 1078.81 36.74 20.32 27.95 768.5 36.35 20.77 28.39 971.45 35 23.35 28.67 1297.8
Cycle 2 (June 2017–March 2018)
2017 MAY 33.9 24.8 28.5 290.2
2017 JUN 34.7 22.4 28.2 194 39.6 21.4 28.3 160.3 36.8 22.3 28.8 159.3 33.7 24.7 28.6 206.4
2017 JUL 34.9 22 28.1 254.8 35.6 21.6 28.2 175 36.2 21.5 28.6 131.3 34.5 24.1 29 231.4
2017 AUG 35 21 28.3 134.2 35.6 21.6 28 103.3 35.8 21.2 28.4 241.6 33.8 23.8 28.3 221.9
2017 SEP 35 22.2 28.1 376.8 34.6 22.2 28.2 138.45 35.3 21.8 28.1 255.2 33 23.7 27.9 187
2017 OCT 37 22.2 28.4 77.7 35.6 20.9 13.4 80.9 36.2 20.9 28.1 256.4 34 23.9 28.5 233.8
2017 NOV 35.8 22.3 28.3 60.1 35.4 17.3 27.1 131 34.7 22.1 28 339.1 33.1 23.1 27.6 304.8
2017 DIC 36 21.2 28.6 30.9 34.4 19 27.2 50.4 35.4 19 27.7 6.4 35.4 23.6 28.1 91
2018 ENE 35.5 21.6 28.5 39.6 35.4 19.1 26.9 46.3 35.2 21 27.9 30 35 23.2 28.6 35.2
2018 FEB 37 20.7 29 0 35 17.2 26.4 2.8 35.5 19.1 27.4 0.4 37.3 23.5 30.2 5.1
2018 MAR 37.6 21.6 29.5 24.4 36.4 18 28.4 7.2 36.6 19.8 28.5 0.6 37.8 24.9 30.8 37.9
Mean 35.85 21.72 28.5 1192.5 35.76 19.83 26.21 895.65 35.77 20.87 28.15 1420.17 34.81 23.9 28.88 1554.5
Agronomy 2021, 11, 1694 9 of 23

Figure 2. Sprouting and plant height of selected genotypes evaluated under several environmental conditions. (a) Plant
height in evaluated genotypes, (b) plant height in genotypes evaluated in seven environments. Different letters show
significant differences obtained by Tukey’s test (p < 0.05).

Table 3. Mean squares for total root yield (TRY), commercial root yield (CRY), and dry matter
content (DMC).

Scheme. df TRY CRY DMC

Environments 6 6643.89 ** 2374.41 ** 317.01 **
Reps/Environments 11 90.83 310.41 ** 7.73
Genotypes 15 190.51 ** 312.48 ** 36.81 **
Genotypes × Environments 90 126.76 ** 153.96 ** 12.33 **
Error 165 80.72 79.7 6.18
Total 287
** Significance for α = 0.01.
Agronomy 2021, 11, 1694 10 of 23

Figure 3. Agronomic performance of selected genotypes evaluated under several environmental conditions. (a) Total and
commercial fresh root yield in evaluated genotypes. (b) Total and commercial fresh root yield in seven environments.
(c) Dry matter content in evaluated genotypes. (d) Dry matter content of plants evaluated in seven environments. Different
letters show significant differences obtained by Tukey’s test (p < 0.05).
Differences among crop cycles were found in Cereté and Sevilla (Table 4). Despite
being a vegetative propagated crop, cassava shows high variation among plants stem-
ming from the same clone cultivated in the same plot, which is mainly due to factors
such as micro-environmental variation and lack of uniformity in the quality of planting
material [29,30]. On average, rainfall in the localities mentioned above was higher than
1.000 mm per year (Table 1). Conditions of low water availability reduce yield especially in
annual species [31,32]. The experimental clones evaluated had been previously selected for
their adaptation to the Caribbean environmental conditions and their superiority in single
row trials (SRT), followed by preliminary (PYT) and advanced (AYT) yield trials [33]. How-
ever, some of these genotypes showed average yields for total and commercial roots below
the values found in the control genotypes. This illustrates the limitation of selection in
early stages. It has been stated that genotypes need to stabilize their phenotypic responses,
and this requires several cycles of growth under the target environmental conditions [33].
Environmental conditions affect the phenotypic expression of characteristics with
low heritability. In this case, phenotypic features such as productive parameters (yield)
and plant architecture (height) are affected by the environment, for which the appropriate
selection of promising genotypes needs to be performed in multi-location evaluations
and, preferably, through several growing seasons. In cassava, characteristics such as
CFRY, DMC, and plant architecture are highly influenced by the genotype by environment
interaction [19,33–37].
Agronomy 2021, 11, 1694 11 of 23

Table 4. Average and standard error values for total root yield, commercial root yield and dry matter content for the 16 genotypes assessed per location and production cycle.

Genotypes Carmen B_ CARMEN_B_ CERETE_ CERETE_ CODAZZI_ SEVILLA_ SEVILLA_

2016 2017 2016 2017 2017 2016 2017
Total root yield (T/ha)
CAISELI * 24.7 ± 8.2 31.3 ± 5.2 ab 17.5 ± 11.2 53.7 ± 6.7 ab 25.7 ± 7.5 b 34.9 ± 2.6 23.7 ± 8.6
CM9456-12 34.2 ± 12.1 31.9 ± 9.6 ab 7.3 ± 6.5 47.2 ± 24.1 ab 26 ± 11 b 48.4 ± 31.4 32.5 ± 8
CMB8527 17.4 ± 1.8 20 ± 9.6 ab 9.3 ± 0.5 74.4 ± 19.2 a 23.8 ± 5.7 b 38.5 ± 36.4 17.6 ± 6.6
GM1692-56 40.6 ± 0.8 31.6 ± 13.3 ab 26.2 ± 2.7 53.9 ± 14.3 ab 28.2 ± 7.3 b 47.4 ± 19.3 29.4 ± 5.6
GM214-62 38.1 ± 12.2 32.8 ± 25.1 ab 9.1 ± 4.8 58.5 ± 7.5 ab 28 ± 2.9 b 40.6 ± 2.2 22.5 ± 3.3
GM3766-5 32.3 ± 17.8 22.2 ± 8.8 ab 15.7 ± 14.6 61.4 ± 8.6 ab 28.2 ± 8.3 b 61.5 ± 12.2 29.4 ± 8
GM3790-2 32.8 ± 23.3 30.5 ± 9.2 ab 12.8 ± 7.3 48.2 ± 16.9 ab 23.1 ± 5.9 b 43.6 ± 7.3 24.7 ± 0.6
COSTEÑA * 40.5 ± 3.6 14.6 ± 8.5 ab 26.6 ± 10.2 60.6 ± 7.2 ab 28.3 ± 5 b 41.1 ± 3.3 31.7 ± 11.6
SM1127-8 18.9 ± 5.5 44.8 ± 0.6 a 17.1 ± 4.6 53.5 ± 14.2 ab 29.8 ± 0.8 b 52.1 ± 22.4 27.8 ± 6.5
SM2773-32 23.2 ± 6.2 20.9 ± 7.5 ab 6.1 ± 0 44.3 ± 15.9 ab 17.9 ± 5.1 b 26.7 ± 6.8 24.2 ± 9.2
SM3106-14 41 ± 3.8 39.2 ± 11.7 ab 30.8 ± 4 60.8 ± 17.4 ab 33.9 ± 9.8 b 43.8 ± 22.1 33.1 ± 8.3
SM3385-55 25.1 ± 1.3 18.1 ± 7.6 ab 18.3 ± 5.4 60.2 ± 10 ab 18.7 ± 3.5 b 45 ± 21.8 15.6 ± 5.3
SM3386-49 38.9 ± 0.5 45.1 ± 15 a 16.3 ± 6.7 73,7 ± 9.5 a 29.4 ± 11.6 b 42.6 ± 1.4 27.4 ± 5.5
SM3387-73 18 ± 4.6 9.9 ± 3.7 b 18.7 ± 0.4 55.2 ± 5.8 ab 27.2 ± 10,2 b 32.6 ± 0.4 18.9 ± 7.8
SM3474-139 29 ± 3 17.5 ± 3.8 ab 10.1 ± 1.5 51.5 ± 8.8 ab 26 ± 1.8 b 56.6 ± 9.8 24.6 ± 6.5
SM3553-27 33.1 ± 3.0 38.2 ± 3.8 ab 14.9 ± 1.2 28.2 ± 3.2 b 63 ± 2.08 a 47.7 ± 7.4 27.4 ± 11.1
Mean 30.5 ± 10.7 c 28 ± 13.6 c 16 ± 8.4 d 55.3 ± 15.3 a 28.6 ± 12.1 c 43.9 ± 14.9 b 25.7 ± 8 c
Commercial root yield (T/ha)
CAISELI * 13.9 ± 8 23.4 ± 7.4 abc 8.8 ± 4.8 30.1 ± 2.9 ab 18.1 ± 7.1 ab 13.9 ± 10.9 10.8 ± 7.9
CM9456-12 19.2 ± 2.6 15.3 ± 5.9 abc 4.1 ± 3.4 25.4 ± 18.5 ab 14.8 ± 7.2 b 38.9 ± 30.9 20.6 ± 9.8
CMB8527 10.6 ± 2.9 9.9 ± 7.6 abc 6.8 ± 1.1 51.6 ± 8.9 a 16.1 ± 3.4 b 5.4 ± 7.6 7±6
GM1692-56 27.6 ± 6.5 17.6 ± 10 abc 14.4 ± 4.5 28.1 ± 4.9 ab 13.5 ± 6.8 b 27 ± 8.9 14 ± 5.1
GM214-62 30.5 ± 12.9 16.2 ± 11.9 abc 3.6 ± 0.3 37.6 ± 7.6 ab 17.1 ± 1.2 b 24.7 ± 0.7 11.8 ± 2.7
GM3766-5 14.4 ± 8.9 9.6 ± 5.1 abc 12.6 ± 12.3 43.4 ± 11.8 ab 13.3 ± 6.2 b 49.1 ± 15.6 14.1 ± 7.9
Agronomy 2021, 11, 1694 12 of 23

Table 4. Cont.

Genotypes Carmen B_ CARMEN_B_ CERETE_ CERETE_ CODAZZI_ SEVILLA_ SEVILLA_

2016 2017 2016 2017 2017 2016 2017
GM3790-2 29 ± 22.3 20.3 ± 6.4 abc 4.2 ± 3 32.6 ± 14.1 ab 15.5 ± 1.9 b 20.6 ± 6.6 11.4 ± 2.5
COSTEÑA * 31.7 ± 0.4 7 ± 6.9 bc 15 ± 3 38.6 ± 7.1 ab 15.8 ± 4.3 b 28 ± 1.6 17.1 ± 12.3
SM1127-8 12.6 ± 2.1 26.8 ± 3.4 ab 12 ± 7 33 ± 14.4 ab 19.2 ± 2.7 ab 16.7 ± 2.9 14.7 ± 3
SM2773-32 15.2 ± 4.9 8.7 ± 6.2 bc 3 ± 0.1 25.2 ± 6.5 ab 8 ± 2.5 b 11.2 ± 0.5 10.7 ± 6
SM3106-14 34 ± 5 21.4 ± 6.4 abc 18.5 ± 0.2 34.4 ± 17 ab 20.7 ± 10.9 ab 36.5 ± 28.7 15.9 ± 3.6
SM3385-55 14.7 ± 0.2 10 ± 6.6 abc 10.1 ± 7.4 38.7 ± 2.9 ab 7.9 ± 4.2 b 23.9 ± 22.2 5.3 ± 2.8
SM3386-49 32.9 ± 0.4 30.8 ± 11.8 a 8.9 ± 2.4 49.4 ± 10.4 a 18.3 ± 8.1 ab 21 ± 0.2 12.7 ± 3.2
SM3387-73 11.3 ± 3.4 4.8 ± 3.2 c 12.5 ± 2.6 37.1 ± 3 ab 17.9 ± 8.7 ab 25.5 ± 4.2 9.8 ± 6.6
SM3474-139 19.8 ± 2 8 ± 2.8 bc 5.6 ± 1.1 28.4 ± 6.7 ab 12.9 ± 2.7 b 40.3 ± 11.3 10.9 ± 3.6
SM3553-27 26.8 ± 2.4 21.1 ± 3.1 abc 11.6 ± 1.9 17.8 ± 1.2 b 43 ± 25.1 a 39.3 ± 10.2 19.4 ± 6.9
Mean 21.3 ± 10.2 bc 15.7 ± 9.6 cde 9.5 ± 5.7 e 34.5 ± 12 a 17 ± 10,3 cd 26.4 ± 15.4 b 12.9 ± 6.5 de
Dry matter content (%)
CAISELI * 33.8 ± 1.3 36.4 ± 2.4 a 40.5 ± 0.3 37.4 ± 1 ab 40.3 ± 1.1 a 38 ± 0.6 34.2 ± 2.5
CM9456-12 30.8 ± 2.9 35.9 ± 2.7 ab 38.5 ± 2.9 34.8 ± 0.8 ab 36.4 ± 2.4 ab 37.6 ± 1.5 31.8 ± 0.7
CMB8527 31.9 ± 3.7 36 ± 3.1 ab 39.8 ± 2.4 37.6 ± 2.1 ab 42.3 ± 0.7 a 40.7 ± 3.1 33.5 ± 2.8
GM1692-56 34.3 ± 4.6 33.7 ± 4.2 ab 37.7 ± 1.1 34.7 ± 1 ab 40.2 ± 1.1 a 37.4 ± 2.4 32.6 ± 0.4
GM214-62 29.4 ± 0.5 35 ± 5.3 ab 41.9 ± 4.3 30.2 ± 8.4 bc 39.9 ± 1 a 34.6 ± 3.7 32.1 ± 0.9
GM3766-5 27.9 ± 0.4 30.8 ± 2 ab 38.8 ± 0.4 31 ± 3.3 abc 37.5 ± 2.8 ab 37.1 ± 4 31.4 ± 1.1
GM3790-2 30.4 ± 0.4 37.7 ± 3.3 a 40.9 ± 3.5 37.4 ± 1 ab 37.6 ± 3.4 ab 37.4 ± 2 35.1 ± 0.8
COSTEÑA * 29.5 ± 0.9 27.3 ± 2.3 b 35.2 ± 4.1 32.2 ± 2.1 abc 40.1 ± 0.5 a 36.3 ± 0.8 31.2 ± 3.7
SM1127-8 28.7 ± 0.8 37 ± 1.3 a 34.4 ± 2.8 25.9 ± 5.1 c 38.3 ± 0.8 ab 36.6 ± 1.8 32.3 ± 0.9
SM2773-32 34.3 ± 0.7 37.3 ± 1.2 a 40.7 ± 1 39.5 ± 1.2 a 36.9 ± 6.5 ab 41 ± 1.9 35.4 ± 09
SM3106-14 32.9 ± 3.9 30.2 ± 2.7 ab 40.1 ± 0.8 34.5 ± 2.1 abc 40.1 ± 0.9 a 37.7 ± 0.6 34 ± 11
SM3385-55 30.5 ± 2.7 33 ± 3.9 ab 37.9 ± 1.6 35.4 ± 2 ab 35.7 ± 2.8 ab 37.7 ± 2.9 32.2 ± 1.5
Agronomy 2021, 11, 1694 13 of 23

Table 4. Cont.

Genotypes Carmen B_ CARMEN_B_ CERETE_ CERETE_ CODAZZI_ SEVILLA_ SEVILLA_

2016 2017 2016 2017 2017 2016 2017
SM3386-49 31.2 ± 2.1 37.1 ± 2.7 a 38.6 ± 1.2 35.7 ± 0.9 ab 38.7 ± 0.4 ab 36.5 ± 0.9 32.1 ± 1.7
SM3387-73 29.7 ± 1.7 30.8 ± 3.4 ab 40.4 ± 0.6 37.4 ± 1.2 ab 40.4 ± 1 a 35.4 ± 4.5 34.4 ± 1.4
SM3474-139 31.5 ± 0.6 35 ± 1.8 ab 37.6 ± 5.8 34.7 ± 1.5 ab 41.3 ± 0.7 a 37.1 ± 3.7 34.2 ± 1.6
SM3553-27 33.2 ± 3 33.7 ± 1.1 ab 38 ± 1 38.4 ± 0.8 ab 32.4 ± 1.3 b 39.3 ± 0.5 34.2 ± 1.8
Mean 31.2 ± 2.6 c 34.2 ± 3.8 b 38.8 ± 2.8 a 34.8 ± 4.2 b 38.6 ± 3.1 a 37.5 ± 2.4 a 33.2 ± 1.9 bc
Group of means with the same letter are not significant for α = 0.05 according to Tukey’s test. * Commercial genotypes (checks).
Agronomy 2021, 11, 1694 14 of 23

DMC averages across environments ranged between 25–40%, which were positive
since the minimum established to carry out the selection of promising genotypes was
35.17%. In this sense, 64% of the evaluated genotypes stood out for showing high DMC
averages (Figure 3c, Table 4). High and stable DMC is one of the objectives pursued by
cassava breeding programs. Furthermore, varieties with mealy texture must have dry
matter (and starch) content above 33–35%. Starch in fresh cassava roots represents around
85–90% of the DMC. Starch, after water, is the most abundant component in cassava
roots [38]. For fresh consumption, the market requires materials with good culinary
quality, low cyanogenic potential and high dry matter content [30,39]. However, the results
showed significant environmental effects on DMC (p > 0.05) (Figure 3d, Tables 3 and 4).
Codazzi 2017 presented the highest overall average among environments. Environmental
and cultural practices have strong influence on DMC in roots. For example, sprouting
before harvest, drastically reduces DMC in roots [3]. DMC of each genotype in specific
environmental conditions represent an expression of G × E interaction. Many studies have
identified a differential adaptation for genotypes in diverse environmental conditions and
significant G × E effects [32,40–42]. In those cases, a stability analysis must be performed
to identify genotypes showing stable performance across seasons and locations.

3.2. Use of Selection Indices and Analysis of Phenotypic Stability to Identify Promising Genotypes
The multi-trait selection index (SIN) considered variables such as CRY, DMC and
PTS as previously mentioned. SINs were obtained for both local (individual) and across-
locations performances. The results of the analysis by environment (combination of location
and season) showed that the genotypes CMB8527, GM1692-56, GM3790-2, SM3106-14,
SM3386-49, and SM3553-27 had large positive SIN values in more than three different envi-
ronments (Figure 4a. CM9456-12, SM1127-8 and SM3387-73 had desirable performances
in at least three environments, but also negative SIN values (of similar magnitude) in at
least three environments, indicating that these were genotypes with good adaptation only
to particular environments. Finally, genotypes GM214-62, ICA-COSTEÑA, SM2773-32,
SM3385-55, and SM3474-139 showed negative values in more than four environments
(Figure 4a).
The analysis combined across locations showed that genotypes with positive SIN, as
expected, had good agronomic performance in most environments. However, selecting
genotypes based on average SIN across environments may not be adequate since perfor-
mances of some genotype(s) in some environment(s) may result in undesirable biases. For
example, SM 3386-49, SM 3553-27, SM 3106-14, and GM 3790-2 were the genotypes with
positive average performances (Figure 4b, Table 5), which would indicate their superiority.
However, some of those genotypes exhibited a negative performance in some environ-
ments, and the average hid this response. The average SIN, for example, may be strongly
affected by unrealistically high yields in certain environments. It is important, therefore, to
assess the stability and regularity of performance across environments. This is ultimately
what defines an outstanding variety and defines if farmers will adopt a variety or not.
 mances in at least three environments, but also negative SIN values (of similar magnitude)
in at least three environments, indicating that these were genotypes with good adaptation
only to particular environments. Finally, genotypes GM214-62, ICA-COSTEÑA, SM2773-
Agronomy 2021, 11, 1694 32, SM3385-55, and SM3474-139 showed negative values in more than four environments
15 of 23
(Figure 4a).

Figure
Figure 4. Multi-factorialresponse
4. Multi-factorial response of
of genotypes
genotypesevaluated
evaluatedin multiple Caribbean
in multiple conditions.
Caribbean (a) Geno-
conditions. (a)
type selection index in the environment. (b) General selection index of genotypes evaluated
Genotype selection index in the environment. (b) General selection index of genotypes evaluated in
multiple environments.
in multiple environments. (c) (c)Lin
Linand
andBinns superiority
Binns index
superiority for the
index fortotal
the and
totalcommercial yields and
and commercial yields
dry matter content.
and dry matter content.
Agronomy 2021, 11, 1694 16 of 23

Table 5. Classification of 16 cassava genotypes using the selection index (SIN) evaluated in seven environments of the Colombian Caribbean region.

Carmen-B Carmen-B Cerete Cerete Codazzi Sevilla Sevilla

Genotypes
2016 2017 2016 2017 2017 2016 2017
GM1692-56 8.91 −1 −6.14 −9 9.04 −2 −4.75 −13 6.05 −11 16.43 −9 −13.69 −10
SM3106-14 6.87 −2 −21.88 −13 20.02 −1 2.65 −9 19.52 −1 24.28 −4 −5.29 −3
SM3386-49 4.78 −3 13.95 −2 −1.34 −11 15.05 −1 10.01 −9 11.24 −11 −16.63 −12
GM3790-2 −0.7 −4 12.51 −3 0.57 −8 8 −5 6.77 −10 16.84 −7 −7.15 −5
ICA-COST * −0.81 −5 −44.43 −16 −4.69 −13 −4.32 −12 14.18 −6 18.44 −6 −13.88 −11
SM2773-32 −1.76 −6 −12.3 −11 −8.57 −15 5.68 −7 −9.37 −15 5.31 −15 −7.71 −6
GM214-62 −5.94 −7 −3.85 −7 2.74 −6 −17.16 −15 11.71 −8 9.94 −12 −16.64 −13
SM3553-27 −6.45 −8 −0.2 −6 −0.16 −10 10.03 −4 −6.24 −14 24.64 −3 −0.78 −1
SM3474-139 −9.34 −9 −12.09 −10 −10.99 −16 −2.64 −11 11.88 −7 23.23 −5 −10.33 −9
CAISELI * −11.44 −10 12.13 −4 3.93 −4 7.5 −6 16.91 −4 7.31 −13 −8.85 −7
CMB8527 −12.3 −11 −5.03 −8 0.12 −9 12.74 −2 15.55 −5 −5.74 −16 −17.31 −15
SM3385-55 −12.8 −12 −18.24 −12 1.8 −7 4.76 −8 −9.4 −16 13.98 −10 −22.31 −16
CM9456-12 −15.37 −13 5.01 −5 −6.22 −14 −8.48 −14 −0.4 −13 34.2 −2 −3.7 −2
SM3387-73 −18.08 −14 −27.14 −15 7.52 −3 10.28 −3 17.36 −3 16.77 −8 −9.29 −8
SM1127-8 −19.59 −15 19.58 −1 −2.42 −12 −39.31 −16 17.67 −2 6.42 −14 −5.46 −4
GM3766-5 −20.46 −16 −22.24 −14 3.13 −5 −1.38 −10 1.8 −12 40.55 −1 −17.11 −14
* Commercial genotypes (checks).
Agronomy 2021, 11, 1694 17 of 23

The general performance of the genotypes, according to the [9] index, is defined as the
mean square of the distance between the average value of the cultivar and the maximum
average response for all locations. Genotypes with lower index values correspond to
those with higher phenotypic stability. The most stable genotypes obtained through this
analysis mostly coincide with the genotypes considered as stable according to the AMMI
analysis [43]. Although Lin and Binns index is useful for the stability analysis, it can
be affected by atypical data, and result in selecting genotypes that adapt very well to a
particular environment(s). That is, genotypes SM3386-49, SM3106-14, GM1692-56, and
CAISELI were selected for their total root yield (TRY), genotypes CAISELI, SM2773-32,
SM3474-139, and GM214-62 for their CRY, and genotypes SM3386-49, SM3553-27, SM3106-
14, and CAISELI for their DMC in almost all the environments (Figure 4c and Table 5).
The analysis of variance quantified the effects attributable to the genotypes (G), en-
vironment (E), and their interaction (G×E) on the expression of CRY and DMC (Table 6).
The AMMI analysis, showed that the first component explained 65.8 and 65% of the vari-
ance contained in the G × E interaction for CRY and DMC, while the second component
explained 28.9 and 30.9% of them, respectively. Therefore, the selection of a single mul-
tiplicative term of the AMMI model was sufficient to explain a large proportion of the
relevant data [44]. The AMMI biplot obtained from the main genotypes and environments
effects, the general mean and the first multiplicative term of the AMMI model (PC1) for
CRY and DMC is shown in Figure 5. Figure 5a shows that 70% of the sum of squares
of the G × E interaction for TRY was decomposed into two main components (PC1 and
PC2). The genotypes closest to the origin point were those with little contribution to the
interaction effects and, therefore, can be considered more stable. Genotypes GM214-62,
SM3106-14, and GM1692-56 were stable. Meanwhile, SM3474-139 and CM9456-12 were
located close to the Sevilla environment during 2016 and 2017, SM3387-73, SM3385-55, and
CM85-27 showed an interaction with the environment in Cereté during 2016 and 2017,
and genotypes SM1127-8 and GM3790-2 in Carmen de Bolívar during 2016. SM3553-27
and GM3766-5 showed the lower stability and high interaction with the environmental
conditions found in Codazzi-2017 and Sevilla-2016, respectively (Figure 5b). Comparing
the averaged CRY and PC1), the genotypes GM1692-56, GM214-62, SM3106-14, SM3553-27,
and SM3386-49 showed a CRY up to 20 tn/ha and they were closest to the origin point
of PC1. The last two genotypes were outstanding for yield variables, and had a higher
selection index and were more stable according to Lin and Binns (Figure 5c).

Table 6. Mean squares and significance of commercial root yield (CFRY) and dry matter content
(DMC) according to the AMMI model.

Source of Variation df CFRY DMC

ENV 6 3,164,400 *** 317,020 ***
REP(ENV) 11 247,100 *** 7630 ns
GEN 15 238,700 *** 36,880 ***
ENV*GEN 90 136,000 *** 12,330 ***
Residuals 163 63,500 6170
Mean 19,755 35,420
CV 40,337 7015
PC1 20 312,705 (41.2%) 24,277 (40.4%)
PC2 18 243,648 (28.9%) 20,660 (30.9%)
*** significance for α = 0.001; ns: No significance; ENV: Environment; REP: Repetition; GEN: Genotype; CV:
Coefficient of variation; PC: Principal component.
Agronomy 2021, 11, 1694 18 of 23

Figure 5. Biplot of AMMI analysis of the total yield and dry matter content. (a) Biplot obtained between PC1 and PC2 for
total yield. (b) Biplot between PC1 and total commercial yield. (c) Biplot obtained between PC1 and PC2 for dry matter
content. (d) Biplot between PC1 with the dry matter content.

In terms of DMC, GM3790-2, SM2773-32 and CMB8527 showed values above 35% and
comparable with the best commercial control, Caiseli (Figure 5d); the last two genotypes
were also the most stable according to the Lin and Binns index. Cereté-2016, Codazzi-2017,
and Sevilla-2016 showed the highest DMC values for most of the genotypes (Figure 5c).
Several authors have reported significant interactions between the environment and
cassava cultivars [45,46], representing an opportunity to identify the best discriminating
environments and select stable genotypes in different environmental conditions [47,48].
Alternatively, it may be desirable to select clones adapted to specific environments [49].
AMMI allows an adequate selection of stable genotypes across environments as well as
genotypes adapted to specific environments [12–14,41,42,50]. The AMMI analysis allows a
straightforward interpretation of the results using biplot graphics. According to [12], the
AMMI tool is powerful to improve the precision of the genotype by environment interac-
tion. It allows eliminating the error of the estimators of phenotypic stability parameters
generated by the effect of some environments in particular genotypes.
Ref. [51] pointed out that those treatments that exhibit an angle close to 90◦ are not
related to each other, and those that have an angle close to 180◦ tend to have an opposite
Agronomy 2021, 11, 1694 19 of 23

behavior, as was the case between the four locations assessed. These were very different
from each other, and seven macro environments for the locations of El Carmen de Bolívar,
Cereté, Agustín Codazzi, and Sevilla were generated during 2 years (except for Codazzi).
Genotypes and environments with high coordinates on PC1 considered in absolute value,
contributed more to the G × E interaction. Meanwhile, genotypes and environments with
PC1 close to zero had little participation in this effect [52].
The correlation coefficient between genotypes, environments or the genotype by
environment interaction is given approximately by the cosine of the angle formed between
the vectors. Thus, if the angle between the vectors is 180◦ the correlation coefficient is −1,
if the angle is 0◦ the coefficient is +1, and if it is 90◦ the coefficient is 0. However, the AMMI
analysis does not provide a quantitative measure of stability. For this reason, Ref. [53]
proposed an average stability value (ASV) measure to quantify and classify genotypes
according to their yield stability in that ASV is the distance of the varieties from point zero
of the scatter diagram (PC1 vs. PC2). The genotypes with the lower scores were more
stable (Table 7). According to the ranking using several indexes, SM214-64, GM1692-56,
SM2773-32, CM9456-12 and SM3106-14 resulted in the best ASV values. Genotypes that
were previously selected as superior, SM3553-27, GM3766-5 and SM3386-49, showed lower
ASV values, suggesting lower stability. However, the selection of promising genotypes
should consider both their superiority and stability. Therefore, SM3106-14, GM1692-56,
CM9456-12 and GM214-62 were recommended for the next evaluation cycle.

Table 7. Ranking and correlation for the commercial fresh root yield (CFRY), the selection index
(SIN), and the phenotypic stability (Pig and ASV) of 16 cassava genotypes.

Genotype SIN CRY Pig CFRY ASV CFRY

SM3106-14 6.60 1 1 1 5
SM3553-27 2.98 5 2 2 16
GM3766-5 −2.24 11 4 3 14
SM3386-49 5.29 2 3 4 13
GM1692-56 2.26 6 6 5 3
COSTEÑA −5.07 15 5 6 2
CM9456-12 0.72 7 8 7 11
SM3474-139 −1.47 9 11 8 12
GM214-62 −2.74 12 7 9 1
GM3790-2 5.26 3 10 10 7
SM3387-73 −0.37 8 13 11 6
CAISELI * 3.93 4 12 12 10
SM3385-55 −6.03 16 15 13 8
SM1127-8 −3.30 13 9 14 9
SM2773-32 −4.10 14 16 15 4
CMB8527 −1.71 10 14 16 15
Ranking coefficient CRY Pig CRY ASV CRY
SIN 0.465 0.503 −0.253
CRY 0.900 −0.076
Pig CRY −0.088
PIG: Stability parameter statistic of a given genotype; * commercial varieties (control); ASV: AMMI stability value.

3.3. Cooking and Sensory Properties in Selected Genotypes

HCN differs widely in cassava. Non-bitter roots usually have a cyanogenic glucoside
concentration < 100 mg HCN equivalents/kg fresh [54,55]. All varieties (except Tai 8) can
be considered non bitter. SM3474-139, GM3766-5, and SM2773-32 HCN contents close to
100 mg/kg, and the rest showed lower concentration values. Genotypes such as CMB8527,
GM3790-2, SM1127-8, SM3385-55, and SM3553-27 showed the HCN content <50 mg/kg, as
did the checks Venezolana and Caiseli.
Agronomy 2021, 11, 1694 20 of 23

The cooking time for most of the evaluated genotypes was in the range of 20–30 min,
however, genotypes such as GM1692-56, GM3766-5, GM3790-2, SM3387-73, SM3553-27,
and SM3562-32 showed an extended and undesirable cooking period (Table 8).

Table 8. Quality features of the evaluated cassava genotypes.

Dry Matter Content Starch Content HCN Cooking Time

Genotype
(%) (%) (µg/g P.F.) (Minutes)
CM9456-12 34.6 ± 3.1 ab 86.1 ± 8.2 57.7 ± 20.3 bcd 23 ± 3.6
CMB8527 38 ± 4.4 a 81.1 ± 1.4 36.8 ± 9.1 cd 23 ± 1.4
GM1692-56 36.2 ± 4.4 ab 77.8 ± 0.3 62.5 ± 23.2 bcd 41 ± 26.9
GM214-62 34.3 ± 5.7 ab 82 ± 2.6 70.7 ± 22.2 bcd 27 ± 1.4
GM3766-5 32.7 ± 3.6 b 86.4 ± 6.2 96 ± 38.8 b 50 ± 13.2
GM3790-2 36.8 ± 3.4 ab 82.5 ± 3.2 36.5 ± 18.4 cd 41 ± 26.9
SM1127-8 34.3 ± 4.6 ab 86 ± 4.3 26.6 ± 13.2 cd 25.3 ± 4.7
SM2773-32 37.3 ± 3.3 ab 83.4 ± 1.2 83 ± 9.6 bc 27.5 ± 0.7
SM3106-14 35.7 ± 5.3 ab 82.2 ± 3 62.6 ± 41.4 bcd 22
SM3385-55 34.1 ± 2.8 ab 82.6 ± 1.8 37.2 ± 14.5 cd 30.5 ± 0.7
SM3386-49 35.6 ± 4 ab 79.6 ± 6.9 73 ± 14 bcd 24.3 ± 2.5
SM3387-73 37.2 ± 5.1 ab 85.9 ± 5.6 56.4 ± 18 bcd 43.5 ± 23.3
SM3474-139 36.5 ± 3.5 ab 86 ± 1.5 109.4 ± 55.2 ab 24.7 ± 4
SM3553-27 34.7 ± 4.1 ab 84.1 ± 1.3 36.3 ± 8.7 cd 40.3 ± 17
SM3562-32 34.6 ± 4.1 ab 81.89 73.15 bcd 42
Caiseli 36.8 ± 4.1 ab 83.6 ± 1.8 31.5 ± 9.5 cd 29
Costeña 33.8 ± 4.8 ab 80.3 ± 6.9 55.5 ± 55 bcd 28
Venezolana 34.7 ± 4.8 ab 81 ± 0.9 24.4 ± 6.7 d 29
Tai 158.5 ± 39.9 a
Different letters show significant differences obtained by Tukey’s test (p < 0.05).

Sensorial description of cassava genotypes from untrained panelists aided to improve

the selection of promising genotypes, hedonic scale was used to qualify parameters such
color, flavor, texture, and root shape (Table 9). Frequency analysis of sensorial data showed
that CM9456-12, SM1127-8, SM3553-27, and SM3562-32 were preferred by panelists, their
color, flavor, texture, and root shape seemed to be superior to commercial varieties. Al-
though, previous reports showed that varieties with mealy texture contain higher contents
of dry matter and starch contents. Although larger starch granules were observed in mealy
varieties than those of non-mealy varieties [56], the factors related to flavor and texture
remain still poorly understood.

Table 9. Liking categories for the evaluated cassava genotypes.

Genotype Colour Flavour Texture Root shape

CM9456-12 4–5 (0.83) 4–5 (0.78) 4–5 (0.72) 4–5 (0.78)
CMB8527 4–5 (0.68) 4–5 (0.60) 4–5 (0.64) 4–5 (0.71)
GM1692-56 4–5 (0.66) 4–5 (0.47) 2–3 (0.50) 4–5 (0.64)
GM3790-2 2–3 (0.52) 2–4 (0.51) 2–4 (0.49) 4-5 (0.70)
SM1127-8 4–5 (0.85) 4–5 (0.82) 4–5 (0.86) 4–5 (0.81)
SM3106-14 4–5 (0.59) 4–5 (0.74) 4–5 (0.68) 4–5 (0.51)
SM3386-49 4–5 (0.73) 4–5 (0.63) 4–5 (0.65) 4–5 (0.67)
SM3387-73 1–3 (0.59) 1–4 (0.48) 1–5 (0.56) 4–5 (0.68)
SM3474-139 3–5 (0.54) 2–4 (0.60) 3–4 (0.58) 4–5 (0.61)
SM3553-27 4–5 (0.87) 4–5 (0.78) 4–5 (0.70) 4–5 (0.84)
SM3562-32 4–5 (0.81) 4–5 (0.63) 4–5 (0.63) 4–5 (0.69)
Caiseli 4–5 (0.58) 4–5 (0.59) 4–5 (0.55) 4–5 (0.63)
Costeña 5 (0.54) 4–5 (0.78) 4–5 (0.68) 4–5 (0.82)
Venezolana 1–5 (0.63) 4–5 (0.67) 4–5 (0.52) 4–5 (0.63)
Numbers show more frequent categories and the frequency is between parentheses, Hedonic scale 1: Dislike
extremely, 2: Dislike moderately, 3: Neither like nor dislike, 4: Like moderately, 5: Like extremely.
Agronomy 2021, 11, 1694 21 of 23

The inclusion of palatability response and quality features determination in cassava

genotypes allowed identifying genotypes with higher opportunity to be adopted by farmers
as new cassava varieties.

4. Conclusions
Environmental conditions influenced the expression of several phenotypic (polygenic)
traits related to root yield, plant architecture, and dry matter content in the evaluated genotypes.
The use of local and multi-location and multi-trait selection indexes allowed the
identification of superior genotypes with a stable performance, which can be released as
new varieties. Moreover, phenotypic stability determination through the Lin and Binns
index, ASV measurement, and AMMI model supported an adequate selection of superior
and stable cassava genotypes.
The inclusion of palatability response and quality features provides crucial information
regarding the acceptability of the roots from the consumer’s point-of-view. Therefore, it
should be considered as a participative selection process that ensures a major adoption of
new cassava varieties.
The genotypes CM9456-12 and SM3553-27 exhibited promissory agronomic perfor-
mance and good acceptance by consumers, with yields higher than the national average,
good culinary quality, and adapted to the Caribbean Region.

Author Contributions: Conceptualization, R.L., A.R., and H.C.; methodology, all authors; formal
analysis, R.L., A.R. and H.C.; investigation, all authors; writing—review and editing, all authors; su-
pervision, A.R. and R.L. All authors have read and agreed to the published version of the manuscript.
Funding: This research was funded by “Ministerio de Agricultura y Desarrollo Rural-MADR” by
TV15-16 agreements.
Acknowledgments: The authors would like to thank Jorge Iván Lenis for all his support in the
propagation of the material used in this work. Many thanks to CIAT for providing the plant material
used in this research and to Agrosavia who funded the research under the project entitled “Cassava
varieties for fresh consumption, and for the balanced feed industry and starch production”.
Conflicts of Interest: The authors declare no conflict of interest.

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