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ORIGINAL RESEARCH
published: 22 November 2021
doi: 10.3389/fpls.2021.720532
Cassava Brown Streak Disease
Response and Association With
Agronomic Traits in Elite Nigerian
Cassava Cultivars
Chukwuka Ugochukwu Ano1,3, Mildred Ochwo-Ssemakula1, Angele Ibanda1,2,
Alfred Ozimati2, Paul Gibson1,4, Joseph Onyeka3, Damian Njoku3, Chiedozie Egesi3,5,6
and Robert S. Kawuki2*
Edited by: 1 College of Agricultural and Environmental Sciences, Makerere University, Kampala, Uganda, 2 National Crops Resources
Nicolas Rispail, Research Institute, Kampala, Uganda, 3 National Root Crops Research Institute, Umudike, Nigeria, 4 Makerere University
Institute for Sustainable Agriculture, Regional Center for Crop Improvement, Kampala, Uganda, 5 International Institute of Tropical Agriculture, Ibadan, Nigeria,
Spanish National Research Council 6 Cornell University Root Crops Research Institute, Ithaca, NY, United States
(CSIC), Spain
Reviewed by:
Robooni Tumuhimbise, Cassava mosaic geminiviruses (CMGs) and cassava brown streak viruses (CBSVs)
National Agricultural Research cause the highest yield losses in cassava production in Africa. In particular, cassava
Organisation, Uganda brown streak disease (CBSD) is and continues to be a significant constraint to
Prabhakaran Sambasivam,
Griffith University, Australia optimal cassava production in Eastern and Southern Africa. While CBSD has not
Clerisse Casinga, been reported in West Africa, its recent rapid spread and damage to cassava
International Institute of Tropical
Agriculture (IITA), Democratic productivity in Eastern, and Southern Africa is alarming. The aim of this study was
Republic of the Congo to evaluate Nigerian cassava genotypes in order to determine their responses to
Andy Bailey, CBSD, in the event that it invades Nigeria, the world’s largest cassava producer. The
University of Bristol, United Kingdom
study gathered information on whether useful CBSD resistance alleles are present
*Correspondence:
Robert S. Kawuki in the elite Nigerian cassava accessions. A total of 1,980 full-sib cassava seedlings
kawukisezirobert@gmail.com from 106 families were assessed in the field at the seedling stage for a year.
Specialty section: A subset of 569 clones were selected and assessed for another year at the clonal
This article was submitted to stage in Namulonge, central Uganda, a known hotspot for CBSD screening. Results
Plant Breeding, indicated that foliar and root incidences and severities varied significantly (p ≤ 0.01,
a section of the journal
Frontiers in Plant Science p ≤ 0.001) except for CBSD foliar incidence at 6 months (CBSD6i). Highest and
Received: 04 June 2021 lowest plot-based heritability estimates for CBSD were registered for CBSD root
Accepted: 18 October 2021 severity (CBSDrs) (0.71) and CBSD6i (0.5). Positive and highly significant correlations
Published: 22 November 2021 were noted between CBSD root incidence (CBSD ∗∗∗ri) and CBSDrs (r = 0.90 ).
Citation: Significant positive correlations were also noted between CBSD foliar severity at
Ano CU, Ochwo-Ssemakula M,
Ibanda A, Ozimati A, Gibson P, 3 months (CBSD3s) and CBSD foliar incidence at 6 months (CBSD ∗∗∗6i) (r = 0.77 ),
Onyeka J, Njoku D, Egesi C and CBSD and CBSD (r = 0.35∗∗∗3s rs ). Fresh root weight (FreshRW ) negatively correlated
Kawuki RS (2021) Cassava Brown
∗∗∗
Streak Disease Response with CBSDri and CBSDrs, respectively (r = −0.21 and r = −0.22∗∗∗). Similarly,
and Association With Agronomic CBSD3s correlated negatively with cassava mosaic disease severity at 3 (CMD3s)
Traits in Elite Nigerian Cassava and 6 months (CMD6s), respectively (r = −0.25∗∗∗ and r = −0.21∗∗∗). Fifteen clonesCultivars. Front. Plant Sci. 12:720532.
doi: 10.3389/fpls.2021.720532 were selected using a non-weighted summation selection index for further screening.
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
In conclusion, results revealed that the elite Nigerian accessions exhibited significant
susceptibility to CBSD within 2 years of evaluation period. It is expected that this
information will aid future breeding decisions for the improvement of CBSD resistance
among the Nigerian cassava varieties.
Keywords: breeding, cassava brown streak disease (CBSD), resistance screening, preemptive strategies, cassava
germplasm, elite genotypes, cassava brown streak virus (CBSV), Ugandan cassava brown streak virus (UCBSV)
INTRODUCTION when the rest of the plant looks healthy (Hillocks et al., 2008).
CMD is distributed across the major African cassava growing
Cassava (Manihot esculenta Crantz) is a perennial plant cultivated belt and is considered one of the most severe and widespread
as an annual crop. It originated in Latin America and is widely diseases of cassava in Nigeria. In contrast, CBSD is restricted
grown across the subtropical and tropical regions of the world. to Eastern, Central, and some parts of Southern Africa and is
It is an essential source of carbohydrate and a major staple food currently considered the world’s most dangerous threat to cassava
for over 800 million people globally (Hammond et al., 2013). production (Legg et al., 2011; Patil et al., 2014; Eni et al., 2018;
Cassava is popular because of its hardy nature and ability to adapt Tomlinson et al., 2018).
to drought and low nutrient availability in the soil. The crop is Based on complete genome sequences, CBSD is caused by
also amenable to piecemeal harvesting for a period between 8 two distinct virus species: cassava brown streak virus (CBSV)
and 24 months after planting, an attribute that makes it popular and Ugandan cassava brown streak virus (UCBSV; Mbanzibwa
among smallholder farmers. These inherent characteristics make et al., 2009; Winter et al., 2010). Both species belong to the
cassava one of the most resilient food security crops of the 21st genus Ipomovirus and family Potyviridae (Alicai et al., 2016)
century. Approximately 70% of cassava is currently grown in and can be found in low- and mid-altitude areas (Munga, 2008;
Africa and Asia, with an estimated cultivated area of more than Mrema, 2016). Symptomatically, CBSD constricts and necrotizes
22 million hectares (Food and Agricultural Organization of the cassava roots, rendering them unpalatable and unmarketable. On
United Nations [FAOSTAT], 2020). Africa accounts for 61% of most instances, blotchy yellow chlorosis or feathery chlorosis
277 million tons of cassava production worldwide, most of which appears on the minor veins of the leaves of infected plants.
comes from Nigeria with an estimated 59 million tons (Food and Brown, round, or elongated streak-like lesions can also occur
Agricultural Organization of the United Nations [FAOSTAT], on the young green portion of the infected stems. These lesions
2020). develop in severe infections to cause dieback and possibly kill the
Cassava is a basic staple food for more than 65% of the whole plant. The most prevalent viruses that are causal agents of
population in Nigeria who consume it in different forms at CMD in Africa are single-stranded DNA bipartite cassava mosaic
least once a day (Eke-okoro and Njoku, 2012). It is processed begomoviruses (CMBs), African cassava mosaic virus (ACMV),
into over 50 food forms, such as garri, lafun, bread, flakes, and and East African cassava mosaic virus (EACMV). In Nigeria,
flour (Eke-okoro and Njoku, 2012). With the increasing demand CMD reached epidemic status in the 1950s and breeding for its
for cassava for both food and non-food uses in Nigeria, efforts resistance began in 1970 (Hahn et al., 1980). Since then, CMD
must be devoted to sustain and/or increase cassava production resistance has been a backbone for all cassava varieties being
and productivity. developed and released by the national breeding program.
Significant cassava yield gaps are commonplace in most Both CBSD and CMD are transmitted over short distances
tropical countries. For example, in Nigeria, where more than by the whitefly vector, Bemisia tabaci (Gennadius) (Maruthi
40 different varieties are grown by farmers (Bankole, 2019), et al., 2005), whereas they are transmitted over long distances
the national average yield of 13.6 metric tons per hectare through the transport of infected planting materials (Patil
reflects a shortfall of 65.9% when compared with potential yield et al., 2015). Management practices for both diseases include
estimates of 40 metric tons per hectare (Food and Agricultural planting of clean (symptomless) cassava cuttings, uprooting
Organization of the United Nations [FAOSTAT], 2020). This and destroying cassava plants showing disease symptoms,
yield gap is due to an array of biotic and abiotic constraints, sterilization of farm implements, especially when cutting cassava
notably poor agronomic practices, susceptibility to prevalent stems for multiplication, and using tolerant/resistant varieties.
pests and diseases, drought, a deficit of clean planting materials, Cultivation of tolerant/resistant varieties remains the most viable
and drudgery associated with most farm operations. Among these management practice (Munga, 2008).
constraints, diseases are by far the main impediments to optimal Previously regarded as a low-altitude disease, CBSD has
cassava production (Ntawuruhunga et al., 2013). recently been confirmed to exist in both lowland and highland
In Africa, cassava production is mostly limited by two viral areas, with the recent reports indicating a wide spread of CBSD
diseases: cassava mosaic disease (CMD) and cassava brown in Uganda, Kenya, Malawi, Burundi, Rwanda, and some parts of
streak disease (CBSD). CMD causes yield losses of up to 70% the Democratic Republic of Congo (DRC; Hillocks et al., 2002;
in susceptible varieties and can kill or stunt plants to varying Bigirimana et al., 2011; Hillocks and Maruthi, 2015; Chipeta
degrees (Tomlinson et al., 2018). CBSD causes yield losses of up et al., 2016; Koima et al., 2018; Munganyinka et al., 2018).
to 100% in susceptible varieties and destroys the edible roots even With the existence of CBSD in DRC (Mulimbi et al., 2012;
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
Casinga et al., 2021), there is a possibility of the disease spreading seeds were then shipped and planted in a seedling nursery at
towards West Africa. The potential reach of CBSD into West Namulonge. The progenies were screened in Uganda in order
Africa, a region with no previous reports of the disease, is to guide the NRCRI breeding program, Nigeria, in developing
considered disturbing. breeding strategies for CBSD resistance. A total of 1,980 botanical
Unlike the East African cassava breeding programs (Munga, seeds successfully emerged into seedlings. These 1,980 seedlings
2008; Abaca et al., 2012; Kawuki et al., 2016; Ferguson et al., represented 106 families (Supplementary Table 1).
2017), West African cassava germplasm has not been undergoing
selection for CBSD resistance because of the absence of the Seedling Evaluation Trial
disease in the region and is, thus, likely to exhibit susceptibility. In a field trial, the 1,980 seedlings were planted during the
A westward drift of CBSD (Bigirimana et al., 2011; Mulimbi second rainfall of 2018 (September/October) for an evaluation
et al., 2012; Casinga et al., 2021), as well as projected studies period of one year and was harvested during the second rainfall
indicating the presence of CBSD in West Africa by 2030 (Jarvis of 2019 (September/October). The field trial was established in
et al., 2012), is a cause for great concern. The recent surge in a completely randomized design, comprising six blocks, with
B. tabaci populations in Eastern and Central Africa, which might each block consisting of 33 ranges. Each row comprised of 10
have played a role in CBSD outbreaks in mid-altitude regions individuals (unique genotypes). Since replication of seedlings
(Legg et al., 2011, 2014), equally troubling. Preemptive breeding at a seedling trial is not possible (Barandica et al., 2016), we
strategies to avert future impact of CBSD in West Africa is, stratified the families across blocks such that sibs were planted
therefore, critical since cassava is a major staple and industry in at least three separate blocks. Seedlings were planted at
crop in the region. Thus, the objectives of this study were to a spacing of 1 m × 1 m. The clone TME 204, which is
(i) determine the reaction of elite Nigerian cassava genotypes to highly susceptible to CBSD, was planted along the experimental
CBSD in Uganda and (ii) determine the relationship between borders as spreaders to augment CBSD pressure in the evaluation
CBSD field response and other important agronomic attributes plots. The experiment was carried out under rainfed conditions,
in the Nigerian cassava genotypes assessed in Uganda. without the application of pesticides and fertilizers, and was kept
weed-free by regular hand weeding.
MATERIALS AND METHODS
Clonal Evaluation Trial
Study Site The clonal evaluation trial (CET) was established at
This study was conducted at the National Crops Resources NaCRRI, Namulonge, during the second rainfall of 2019
Research Institute (NaCRRI), Namulonge (0.5232◦N, 32.6158◦E) (September/October) for a one year evaluation period
which is located at an altitude of 1,200 m above sea level and and was harvested during the second rainfall of 2020
characterized by the bimodal rainfall distribution and an average (September/October). The clonal trial constituted 569 clones
annual temperature ranging between 24 and 30◦C (Sebuwufu advanced from the seedling stage. Advancement from seedling
et al., 2015). The soil is characterized by acidic ferralsols, with pH evaluation trial (SET) to CET was based mainly on the ability
of below 6.5–7.0 (Sebuwufu et al., 2015). NaCRRI is located 27 km of a clone to produce ample planting materials, i.e., at least 10
north of Kampala, the capital city of Uganda, and has a tropical stem cuttings. This is because 10 stem cuttings were required to
wet and mild dry climate with annual rainfall ranging between constitute a row, which would represent a single clone. Briefly,
1,000 and 1,450 mm with slight humid condition (average: 65%) the trial was established in an augmented design, comprising 24
(Sebuwufu et al., 2015). Namulonge, geographically located in blocks; each clone was planted in a single row of 10 stem cuttings,
central Uganda, is considered a hotspot for CBSD screening at a spacing of 1 m × 1 m within rows. Within each block, the
(Alicai et al., 2007; Sebuwufu et al., 2015). The site is also selected test clones were planted along with three randomized
associated with high B. tabaci populations (Kawuki et al., 2016). checks, namely, TME 204, NAROCASS 1, and Mkumba.
These characteristics qualify NaCRRI as an optimal site for TME 204 was the most susceptible check to CBSD, whereas
CBSD and CMD resistance screening (Abaca et al., 2012). In NAROCASS 1 and Mkumba were tolerant checks, officially
this study, we, therefore, assessed the response of introduced released in Uganda and Tanzania, respectively. TME 204 also
Nigerian germplasm to CBSD infestation at NaCRRI, a known acted as a spreader to augment CBSD pressure in the field trial.
hotspot in Uganda. Similar to the seedling trial, the experiment was carried out
under rainfed conditions, without the application of pesticides
Test Materials and fertilizers, and was kept weed-free by regular hand weeding.
In response to the CBSD spread across Africa, National Root
Crops Research Institute (NRCRI), Umudike, Nigeria, took Data Collection
the initiative to screen some crosses of elite-by-elite cassava For both SET and CET trials, data were collected on CBSD and
genotypes in Uganda, a hotspot for CBSD. A total of 5,000 CMD. Foliar disease symptoms were assessed on each plant at
botanical seeds were generated from various biparental crosses three and six months after planting (MAP). For assessment of
involving 48 elite progenitors. The progenitors were part of Cycle CBSD, plants were assigned disease severity scores based on the
1 of the NRCRI cyclic population and were selected based on standard five-point scoring scale (Gondwe et al., 2003), where
their yielding ability and resistance to CMD. Accordingly, these 1 = no apparent symptoms; 2 = slight foliar feathery chlorosis and
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
no stem lesions; 3 = prominent foliar feathery chlorosis, mild- For clonal trial datasets, linear mixed model effects using
stem lesions, and no dieback; 4 = severe foliar feathery chlorosis, lme4 package in R was used to estimate variance components
severe stem lesions, and no dieback; and 5 = defoliation, severe and, thus, to enable the estimation of best linear unbiased
stem lesions, and dieback (Figure 1). predictors (BLUPs). The BLUPs were computed to enable
Similarly, CMD was assessed using the 1–5 scoring scale, genotype comparison for the unbalanced dataset (Bernardo,
where 1 = cassava plant showing no leaf symptom; 2 = mild 2010). The linear model used to generate the analysis of variance
distortion and mild chlorosis on the leaves; 3 = significant for single-site analysis was as follows:
distortion and chlorosis on one-third of most leaves; 4 = extreme
distortion and presence of mosaic patterns on two-third Yijk = µ+ Ci + Bj + Gk + εijk,
of most leaves and general reduction of leaf size; and where Yijk is the observed response of the i-th clone in the j-5 = very severe mosaic symptoms on all leaves, appearance th block for the k-th test genotype, µ is the general mean of
of distortion, twisting, misshapen, and severe leaf reduction the genotypes, Ci is the fixed effect of the checks, B is theof most leaves accompanied by severe stunting of plants jrandom effect of the block, G is the random effect of the test
(Thresh and Cooter, 2005). kgenotypes, and εijk is the random error associated with the ijk-thAt 12MAP (during harvest), individual plants (in SET) and observation. The broad-sense heritability estimates for each trait
plots (in CET) were uprooted, and roots were sliced for CBSD were calculated using the following formula:
root necrosis assessment. The CBSD root severity was assessed
on all harvested roots, from a plant, using the 1–5 scoring scale H2 σ2G/(σ2 2= G+ σ e),
(Gondwe et al., 2003), where 1 = no apparent necrosis, 2 ≤5%
of root necrosis, 3 = 6–10% of root necrosis, 4 = 11–25% of root where H2 is the broad-sense heritability, σ2G is the genotype
necrosis and mild root constrictions, and 5≥25% of root necrosis variance, and σ2e is the error variance. To extract the variance
with severe root constriction (Figure 1). components for computing broad-sense heritability, the effects
Finally, for both SET and CET, data were collected on total of the block and test genotypes were considered random, whereas
carotenoid content and fresh root weight (FRW). The total the check effects were considered fixed.
carotenoid content was assessed visually using a qualitative 1–6 A non-weighted rank summation selection index (SI) was
standard root color scoring scale developed by the International used to compare the performance of the test genotypes.
Center for Tropical Agriculture (CIAT), where 1 = white, 2 = light Briefly, genotype BLUP values generated from CBSD foliar
cream, 3 = cream, 4 = light yellow, 5 = yellow, and 6 = deep yellow. and root scores were ranked and subsequently summed up
To estimate fresh root yield (FRYD) (tons ha−1) from FRW, we to compute the SI (Mulamba and Mock, 1978).
used the formula: FRYD = [(FRW/Number of plants harvested
per plot)× 10,000]/1,000 (Tumuhimbise et al., 2014).
RESULTS
Data Analyses Field Reaction of Cassava Genotypes at
Datasets generated in the seedling trial were described using the Seedling Stage
summary statistics in R (R Core Team, 2020). Relationships A total of 1,980 genotypes were planted and evaluated in the
between CBSD severity and other evaluated key agronomic traits seedling trial. However, by the third month, 38% of the genotypes
were visualized using the ggscatter function in R (R Core Team, had succumbed to CBSD pressure (Figure 2). About 0.01%
2020). The Pearson’s correlation test was conducted, and the of genotypes were lost by the 6th month, and by the 12th
coefficient of correlation was extracted using the cor.test. All the month, an additional 15% of genotypes had succumbed to CBSD
functions mentioned above are available in ggpubr package in R. pressure. Hence, only 47% of the genotypes survived, and the root
FIGURE 1 | CBSD symptom scoring scale (1–5).
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
necrosis assessment were undertaken on them at 12MAP. For the (Figure 5). In contrast, approximately 30% of the accessions
genotypes that survived up to 3 months after planting (3MAP), had CBSD root necrosis scores ranging from 1 to 2. For CBSD
the CBSD severity ranged from 1 to 3 at 3MAP, while at 6MAP incidence, more than 90% of the genotypes exhibited incidence
and 12MAP, it ranged from 1 to 5 (Figure 3). Percentage CBSD scores between 75 and 100% at 3 and 6 months, while 25% of
root incidence ranged from 0 to 100%, with a mean score of 56.8. the genotypes registered root incidences between 75 and 100%
Mean severity scores for CBSD at 3MAP, 6MAP, and 12MAP were for CBSDri. For CMD, more than 90% of the genotypes exhibited
1.03, 1.21, and 2.30, respectively. severity scores between 1 and 2, and incidences between 0 and
A total of 1,014 (out of 1,206) genotypes had low CBSD foliar 25% at 6MAP (Figure 6).
severity score (≤1.5) at 6 months. In contrast, 330 out of 927
genotypes assessed during harvest exhibited low root necrosis Correlations Between Cassava Brown
severity score (≤1.5). Overall, 51% of the 927 accessions evaluated Streak Disease and Other Related Traits
had yellow roots. Notably, there was a gradual increase in severity
from 3MAP to 6MAP, with the highest average score at 12MAP in the Seedling Trial
(Supplementary Table 2). Foliar severity at six months had a significant but low positive
correlation with CBSD root severity (r = 0.1376∗∗) and CBSD
root incidence (0.1223∗∗) (Table 2). However, CBSD root severity
Response of Cassava Genotypes to positively correlated with CBSD root incidence (r = 0.8296∗∗∗).
Cassava Brown Streak Disease at the There were no correlations between CBSD and CMD. However,
Clonal Stage CMD severity at six months had a low negative correlationwith root weight (r = −0.1306∗∗). Furthermore, root weight was
A total of 569 clones were selected from the seedling trial for negatively and marginally correlated with CBSD root necrosis
further evaluation at the clonal stage during the 2019–2020 incidence and root necrosis severity (−0.0946∗ and −0.1782∗∗∗,
season. Overall, 272 accessions succumbed to disease pressure respectively). There were marginal correlations between total
during the evaluation period: 92 accessions at 3 months, 6 carotenoid content and root weight (0.1894∗∗∗). There were also
accessions at 6 months, and 174 accessions at 12 months marginal negative correlations between total carotenoids and
(Figure 2). Hence, 297 accessions survived until root necrosis CBSD root severity (−0.0612).
assessment at 12MAP. CBSD severity scores ranged from 1 to
4 at 3MAP and 6MAP and 1 to 5 at 12MAP (Figure 5). The
percentage CBSD incidence ranged from 0 to 100 at 3MAP, Correlations Between Cassava Brown
6MAP, and 12MAP. Mean scores for CBSD severity at 3MAP, Streak Disease and Other Related Traits
6MAP, and 12MAP were 2.3, 2.5, and 2.5, respectively. Mean at the Clonal Evaluation
scores of 79.7 and 84.4 were also recorded for CBSD foliar Correlations between CBSD and other agronomic traits evaluated
incidence and 59.3 for root incidence (Table 1). Approximately at the clonal stage are presented in Table 3. Analyses between
80% of the genotypes had CBSD scores between 2 and 3 traits showed a significant positive relationship between CBSD
FIGURE 2 | Dieback and death inflicted by CBSD on the Nigerian germplasm evaluated in Uganda at SET and CET.
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FIGURE 3 | Distribution of CBSD foliar and root severity scores of Nigerian germplasm evaluated at SET in Namulonge, Uganda in 2018. CBSD3s, CBSD severity
assessed at three months after planting, CBSD severity assessed at six months after planting, CBSDrs, CBSD root severity at 12MAP.
root incidence and CBSD root severity (r = 0.90∗∗∗). CBSD 3 months (r = −0.25∗∗∗), CMD incidence at six months
foliar severity at 3 months and CBSD foliar incidence at (CMD6i) (r = −0.20∗∗∗), and CMD severity at six months
three months (CBSD3i) also had highly significant positive (r =−0.21∗∗∗).
correlations of r = 0.89∗∗∗. The same pattern was noted for Fresh root weight during harvest had a significant
CBSD foliar incidence at six months and CBSD foliar severity at negative correlation with CBSD foliar incidence at 3 months
six months (r = 0.89∗∗∗). CBSD foliar incidence at three months (r = 0.54∗∗∗− ), CBSD foliar severity at 3 months (r = ∗∗∗−0.49 ),
also correlated positively and significantly with CBSD foliar CBSD foliar incidence at 6 months (r = −0.52∗∗∗), CBSD foliar
incidence at six months (r = 0.86∗∗∗) and CBSD foliar severity severity at 6 months (r = 0.45∗∗∗− ), CBSD root incidence
at six months (r = 0.78∗∗∗). However, correlations were lower (r = 0.21∗∗∗− ), and CBSD root severity (r = −0.22∗∗∗).
between CBSD root incidence (r = 0.40∗∗∗) and CBSD root However, there was a significant positive correlation between
severity (r = 0.34∗∗∗). Similarly, CBSD foliar severity at 3 months FRW and harvest index (r = 0.51∗∗∗). There was a slight
correlated positively with CBSD foliar incidence at six months non-significant negative correlation between harvest index and
(r = 0.77∗∗∗) and CBSD foliar severity at six months (r = 0.78∗∗∗), CBSD root incidence (r = −0.17). CBSD root severity also had
but lower with CBSD root incidence (r = 0.40∗∗∗) and CBSD a slight negative non-significant correlation with harvest index
root severity (r = 0.35∗∗∗). In contrast, CBSD foliar severity (r = −0.17). Negative correlations were consistently observed
at three months correlated negatively with CMD incidence between harvest index and CBSD foliar incidence at 3 months
at three months (CMD3i) (r = 0.25∗∗∗− ), CMD severity at (r = 0.37∗∗∗− ), CBSD foliar severity at 3 months (r = −0.36),
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FIGURE 4 | Distribution of CMD severity scores of Nigerian germplasm evaluated at SET in Namulonge, Uganda in 2018. CMD.3MAP, CMD severity assessed at
three months after planting, CBMD severity assessed at six months after planting.
CBSD foliar incidence at six months (r = −0.38), and CBSD with CMD6s at the seedling stage and CBSD6s at the clonal
foliar severity at six months (r =−0.34). stage (r = 0.28∗∗∗). There were slightly non-significant negative
correlations between S_CMD3s and C_CBSD3s (r = −0.07),
Correlations Between Cassava Brown C_CBSD6s (r = −0.05), and C_CBSDrs (r = −0.03) (Table 4).
Streak Disease and Cassava Mosaic There were also slightly positive non-significant correlations
between S_CBSD and C_CBSD (r = 0.05), S_CBSD and
Disease at Both Seedling Evaluation Trial 3s 3s 3sC_CBSDrs (r = 0.01), and S_CBSD3s and C_CBSDri (r = 0.03).
and Clonal Evaluation Trial
Correlations between seedling and clonal evaluations are
presented in Table 4. There were significant correlations for Variation, Heritabilities for Cassava
CBSD ∗∗∗ri at both SET and CET (r = 0.48 ) (Table 4). Brown Streak Disease and Other
Correlations between CBSDrs at SET and CET were also Important Traits at the Clonal Evaluation
significant (r = 0.53∗∗∗). CMD6s score at the seedling stage was Analysis of variance (ANOVA) results showed significant
positively correlated with CMD3s at the clonal stage (r = 0.68∗∗∗) differences among test genotypes for CBSD severity at 3
and CMD6s at the clonal stage (r = 0.67∗∗∗). Negative correlations (p ≤ 0.001), 6 (p ≤ 0.01), and 12 months (p ≤ 0.001) (Table 1).
were consistently observed between CMD6s at the seedling There were also significant differences among test genotypes for
stage and CBSD3s at the clonal stage (r = −0.36∗∗∗), and also CBSD incidence at 3 and 12 months (p ≤ 0.001) but not at
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FIGURE 5 | Distribution of CBSD foliar and root severities and incidences in Nigerian germplasm evaluated in clonal trial Uganda in 2019. CBSD3s, CBSD severity
3MAP; CBSD6s, CBSD severity 6MAP; CBSD12s, CBSD root severity at 12MAP; CBSD3i , CBSD incidence 3MAP; CBSD6i , CBSD incidence 6MAP; CBSD12i ,
CBSD root incidence at 12MAP. Analysis based on 297 genotypes.
TABLE 1 | Field response of elite Nigerian clones in Uganda.
Mean squares
SOV Df Severity Incidence HI
CBSD3s CBSD6s CBSDrs CMD3s CMD6s CBSD3i CBSD6i CBSDri CMD3i CMD6i
Genotype 292 0.209*** 0.197** 1.371*** 0.263*** 0.408*** 296*** 218ns 1181*** 748.1*** 881.1*** 0.027**
Check 2 21.440*** 22.206*** 68.053*** 0.046*** 0.012* 62369*** 50893*** 43000*** 320.9** 95.6** 0.196***
Check vs. Genotype 1 44.463*** 42.187*** 1.240* 1.611*** 3.109*** 167756*** 140320*** 10866*** 4243.1*** 6803.1*** 1.145***
Block 23 0.057ns 0.105ns 0.225ns 0.005ns 0.005ns 149ns 370ns 317ns 41.4ns 28.5 0.012ns
Residual 46 0.05 0.096 0.193 0.006 0.003 118 340 237 45.5 18.3 0.123
mean 2.306 2.478 2.498 1.383 1.499 79.76 84.41 59.32 20.35 22.42 0.28
CV (%) 9.4 12.2 17.5 6.5 4.8 13.1 21.4 25.8 72.7 42.2 40.5
H2 0.69 0.6 0.71 0.76 0.81 0.68 0.5 0.66 0.79 0.81 0.55
SOV, source of variation; Df, degrees of freedom; CBSD3s, CBSD severity at 3 months after planting (MAP); CBSD6s, CBSD severity at 6MAP; CBSD3i , CBSD incidence
at 3MAP; CBSD6i , CBSD incidence at 6MAP; CMD3s, CMD severity at 3MAP; CMD6s, CMD severity at 6MAP; CMD3i , CMD incidence at 3MAP; CMD6i , CMD incidence
at 6MAP; CBSDrs, CBSD root severity; CBSDri , CBSD root incidence; HI, harvest index; CV, coefficient of variation; H2, entry mean broad-sense heritability; ns, non-
significant at alpha = 0.05; *p ≤ 0.05; **p ≤ 0.01; ***p ≤ 0.00.
6 months. Comparisons between test genotype means and means 12 months varied from moderate to high (CBSD3i H2 = 0.68,
of the checks also showed significant differences (p ≤ 0.05 and CBSD6i H2 = 0.50, CBSD H2ri = 0.66, and CBSD H23s = 0.79,
p ≤ 0.001) for both CBSD incidence and severity, except CBSDrs CBSD H26s = 0.60, CBSD H2rs = 0.71).
(p ≤ 0.05), which exhibited significant marginal differences.
Entry mean-based broad-sense heritability estimates ranged
from moderate to high (Table 1). Overall, disease traits had Comparisons and Ranking of Cassava
higher heritability estimates than agronomic traits. For disease Clones Based on the Selection Index
traits, CBSD6i and CBSD6s had the lowest heritability estimates Genotype ranking based on the non-weighted rank summation
with moderate H2 of 0.50 and 0.60, respectively. CMD severity SI revealed the overall best performer as UGIN181367, a
and incidence at 6 months had the highest estimates of yellow-fleshed clone (Table 5). Other top nine performing
heritability with H2 = 0.81 and 0.81, respectively. Heritability genotypes included UGIN180528, UGIN181535, UGIN180247,
estimates for CBSD (incidence and severity) at 3, 6, and UGIN181791, UGIN181326, UGIN181154, UGIN181371,
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TABLE 2 | Relationship between CBSD and other related traits in Nigerian genotypes evaluated in seedling trial at Namulonge in 2018.
Variables CBSDri CBSDrs CBSD3s CBSD6s CMD3s CMD6s FreshRW ttl_caro
CBSDri –
CBSDrs 0.8296*** –
CBSD3s −0.0365ns −0.019ns –
CBSD6s 0.1223** 0.1376** −0.0222ns –
CMD3s 0.0766ns 0.0594ns 0.0199ns 0.0214ns –
CMD6s 0.0277ns 0.0718ns −0.0316ns −0.0331ns 0.0334ns –
FreshRW −0.0946* −0.1782*** −0.0119ns 0.0076ns 0.0066ns −0.1306** –
Total_Caro 0.0294ns −0.0612ns −0.0465ns 0.0217ns 0.0065ns 0.0588ns 0.1894*** –
***Significant (p < 0.001); **significant (p < 0.01); *significant (p < 0.05); CBSD3s, CBSD foliar severity at 3MAP; CBSD6s, CBSD foliar severity at 6MAP; CBSDri , CBSD
root incidence at 12MAP; CBSDrs, CBSD root severity at 12MAP; CMD3s, CMD severity at 3MAP; CMD6s, CMD severity at 6MAP; FreshRW , fresh root weight; ttl_caro,
total carotenoid content; ns, Not significant.
TABLE 3 | Relationship between CBSD and other related traits in Nigerian genotypes evaluated in the clonal trial at Namulonge in 2019.
Variables CBSDri CBSDrs CBSD3i CBSD3s CBSD6i CBSD6s CMD3i CMD3s CMD6i CMD6s FreshRW HI ttl_caro
CBSDri –
CBSDrs 0.897*** –
CBSD3i 0.4007*** 0.3406*** –
CBSD3s 0.3989*** 0.3449*** 0.8872*** –
CBSD6i 0.3775*** 0.3322*** 0.8567*** 0.7702*** –
CBSD6s 0.4175*** 0.3851*** 0.7797*** 0.7768*** 0.8912*** –
CMD3i −0.1287ns −0.0836ns −0.1551ns −0.2539*** −0.0087ns −0.119ns –
CMD3s −0.1279ns −0.0875ns −0.1578ns −0.2501*** −0.0161ns −0.116ns 0.9747*** –
CMD6i −0.1185ns −0.0977ns −0.1055ns −0.2001*** 0.0211ns −0.0859ns 0.9257*** 0.9076*** –
CMD6s −0.1127ns −0.0899ns −0.1181ns −0.2081*** 0.013ns −0.0907ns 0.9073*** 0.9235*** 0.9695*** –
FreshRW −0.2084*** −0.2189*** −0.5432*** −0.4915*** −0.5182*** −0.452*** −0.1031ns −0.1185ns −0.1218ns −0.1355ns –
HI −0.1699ns −0.1672ns −0.3658*** −0.352*** −0.3764*** −0.3367*** −0.0695ns −0.0749ns −0.0995ns −0.1112ns 0.5092*** –
ttl_caro 0.0337ns 0.0118ns 0.2067*** 0.1533ns 0.17ns 0.1194ns 0.1006ns 0.1092ns 0.1077ns 0.1139ns −0.078ns −0.0015ns –
***Significant (p < 0.001); CBSD3s, CBSD severity at 3MAP; CBSD6s, CBSD severity at 6MAP; CBSD3i , CBSD incidence at 3MAP; CBSD6i , CBSD incidence at 6MAP;
CMD3s, CMD severity at 3MAP; CMD6s, CMD severity at 6MAP; CMD3i , CMD incidence at 3MAP; CMD6i , CMD incidence at 6MAP; CBSDrs, CBSD root severity;
CBSDri , CBSD root incidence; HI, harvest index; FreshRW , fresh root weight during harvest; ttl_caro, total carotenoid content; ns, Not significant.
UGIN180602, and UGIN181346. Notably, 8 out of the best progenies surviving until harvest at 12MAP. Only two families
15 clones were yellow clones. Families of the best and worst had higher CBSD root severity means than that of the susceptible
performers in terms of CBSD resistance are presented in Table 6. check TME 204 (4.33) at 12 months, with F040 being the most
Only family F036 had 2 progenies in the best 15 categories, and susceptible with a mean score of 5.0. Progenies per family for
other families, such as F001, F004, F014, and F018, had one the seedling trial ranged from 10 to 130. In contrast, progenies
progeny each in the best performing category. advanced to CET after selection ranged from 1 to 18, averaging
Comparison of checks and test genotypes is shown in four progenies per family. Overall, 30 families succumbed to
Figure 7. CBSD-resistant checks (Mkumba and NAROCASS 1) CBSD pressure during the seedling evaluation.
performed markedly better than all other test genotypes for
CBSD resistance. However, 65% of test genotypes performed
better than the susceptible check (TMEB204) in terms of CBSD DISCUSSION
resistance (Figure 7).
From the seedling to clonal evaluation stage, family Cassava brown streak disease is one of the topmost threats to food
progression with regard to CBSD is presented in Supplementary security (Patil et al., 2015), undermining any investments made
Figure 1. Mean CBSD severities at 3, 6, and 12 months in the to maximize the benefits of cassava value chains. For this reason,
seedling stage were 1.03, 1.18, and 2.28, respectively. However, concerted efforts are devoted toward finding sustainable disease
at the clonal stage, mean CBSD severities at 3, 6, and 12 months management options. Based on the lessons learned in East Africa,
were 2.50, 2.70, and 2.57, respectively. Evidently, there was a where less attention was given to CBSD until it reached epidemic
general increase in CBSD from seedling to clonal stage. The levels after several decades of existence at low altitudes of coastal
survival rate of progenies per family from seedling to clonal areas in Tanzania (Storey, 1936; Legg et al., 2011, 2015), it has
evaluation ranged from 5 to 80% (Supplementary Figure 2). become necessary to take preemptive measures to prevent the
The family F059 had the highest survival rate, with 80% of its spread of CBSD in West Africa, a major cassava-producing zone
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FIGURE 6 | Distribution of CMD severities in Nigerian germplasm evaluated in clonal trial in Uganda in 2019. CMD3s, CMD severity assessed at three months after
planting, CBMD severity assessed at six months after planting, CMD incidence assessed at three months after planting, CMD incidence assessed at six months after
planting.
in Africa, and limit its impact. Accordingly, this study aimed at Indeed, significant correlations between seedling and clonal
contributing toward development of improved cassava varieties CBSD root incidences and severities (S_CBSDri and C_CBSDri
with enhanced CBSD resistance in Nigeria. r = 0.48∗∗∗; S_CBSD and C_CBSD r = 0.53∗∗∗rs rs ) suggest viral
Consequently, 1,980 seedlings were evaluated for their inoculum buildup in the course of the evaluations. For these
responses to CBSD. Of these, 569 clones were selected for further reasons, conclusions cannot be deducted on resistance status at
evaluation at the clonal level. By the first year of field evaluation, seedling trials.
38% of the 1,980 seedlings succumbed to CBSD pressure during Progenies per family ranged from 10 to 130 in the SET,
the first three months after planting, and by the 12th month, with an average of 18 progenies per family. In CET, this
only 46% of the genotypes survived for root necrosis assessment. varied between 1 and 18, with an average of four progenies
This magnitude of CBSD severity can be attributed to a lack of per family (Supplementary Figure 1). This variation in the
CBSD resistance alleles in the Nigerian germplasm. A similar number of progenies from each progenitor is related to
outcome was noted by Elegba et al. (2020), who reported less the highly erratic flowering behavior of different cassava
than 50% survival rate for Ghanaian cassava genotypes tested genotypes (Ceballos et al., 2012). Overall, family averages at
against CBSV and UCBSV under screen-house conditions. 6 and 12 months in the CET indicated that most families
Likewise, Winter et al. (2019) reported moderate to severe foliar had considerably low resistance to CBSD owing to high
symptoms when 238 South American cassava genotypes were susceptibility scores (Supplementary Figure 1). Some families
assessed for resistance to CBSVs. Viral inoculum buildup occurs had seedlings that exhibited marginal CBSD symptoms. A good
when diseased stem cuttings are recycled (Kaweesi et al., 2014). example is family F036, which had two of its progenies
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
TABLE 4 | Relationships between CBSD and CMD for the genotypes between the seedling and clonal trial.
Variables C_CBSD3s C_CBSD6s C_CBSDri C_CBSDrs C_CMD3s C_CMD6s S_CBSD3s S_CBSD6s S_CBSDri S_CBSDrs S_CMD3s S_CMD6s
C_CBSD3s –
C_CBSD6s 0.6443*** –
C_CBSDri 0.2165 0.1245 –
C_CBSDrs 0.1346 0.0837 0.8921*** –
C_CMD3s −0.4973*** −0.3536*** −0.1537 −0.1586 –
C_CMD6s −0.4606*** −0.335*** −0.0785 −0.1149 0.922*** –
S_CBSD3s 0.0472 0.0051 0.0364 −0.0182 −0.0037 −0.021 –
S_CBSD6s 0.0538 0.1266 −0.1364 −0.1313 0.0963 0.1498 0.0057 –
S_CBSDri 0.0881 0.0839 0.475*** 0.5067*** −0.1733 −0.1527 −0.1021 0.156 –
S_CBSDrs 0.0838 0.0426 0.4326*** 0.5266*** −0.0863 −0.0609 −0.0977 0.1978 0.8591*** –
S_CMD3s −0.0659 −0.0536 0.0552 −0.0332 0.2315 0.3353*** 0.152 0.0921 −0.0491 −0.0529 –
S_CMD6s −0.3556*** −0.2803*** −0.0661 −0.0882 0.6781*** 0.6653*** −0.0638 0.0705 0.0185 0.0969 0.1991 –
***Significant (p < 0.001); S_CBSD3s, Seedling evaluation for CBSD severity at 3MAP; S_CBSD6s, Seedling evaluation for CBSD severity at 6MAP; S_CMD3s, Seedling
evaluation for CMD severity at 3MAP; S_CMD6s, Seedling evaluation for CMD severity at 6MAP; S_CBSDrs, Seedling evaluation for CBSD root severity at 12 months;
S_CBSDri , Seedling evaluation for CBSD root incidence at 12 months. C_CBSD3s, Clonal evaluation for CBSD severity at 3MAP; C_CBSD6s, Clonal evaluation for CBSD
severity at 6MAP; C_CMD3s, Clonal evaluation for CMD severity at 3MAP; C_CMD6s, Clonal evaluation for CMD severity at 6MAP; C_CBSDrs, Clonal evaluation for CBSD
root severity at 12 months; C_CBSDri , Clonal evaluation for CBSD root incidence at 12 months. Correlations were obtained using 294 genotypes with complete dataset
for CBSD and CMD at SET and CET.
TABLE 5 | Rankings of the best-15 and worst-15 genotypes following CBSD evaluations at Namulonge in 2019.
Best-15 performing genotypes Worst-15 performing genotypes
Genotype CBSD3s CBSD6s CBSDrs CBSD3i CBSD6i CBSDri SI ttl_caro Genotype CBSD3s CBSD6s CBSDrs CBSD3i CBSD6i CBSDri SI ttl_caro
UG110017 1 1 1 1 1 1 6 1 UGN180552 278 296 281 296 276 224 1651 2
Mkumba 2 2 9 2 2 18 35 1 UGIN180141 294 257 284 260 261 275 1631 1
UGIN181367 8 12 32 9 13 28 102 2 UGIN181204 295 258 283 259 260 274 1629 1
UGIN180528 9 6 26 27 5 33 106 1 UGIN180263 273 282 245 289 296 207 1592 1
UGIN181535 12 61 13 20 26 10 142 1 UGIN181764 277 252 268 295 275 223 1590 1
UGIN180247 6 5 46 10 7 71 145 4 UGIN181352 289 256 248 257 258 272 1580 1
UGIN181791 5 107 3 8 62 2 187 1 UGIN181162 284 269 293 195 239 280 1560 3
UGIN181326 4 38 6 4 141 4 197 1 UGIN181784 288 270 278 194 238 279 1547 1
UGIN181154 18 11 66 52 9 50 206 2 UGIN180201 282 268 260 192 237 278 1517 1
UGIN181371 15 14 94 16 16 63 218 3 UGIN181592 292 165 266 258 259 273 1513 3
UGIN180602 17 57 4 35 102 8 223 4 UGIN180481 285 234 272 248 173 286 1498 2
UGIN181346 11 148 8 12 51 9 239 1 UGIN181454 291 235 265 247 172 285 1495 1
UGIN180416 25 45 33 105 18 29 255 1 UGIN181343 283 255 161 255 256 271 1481 1
UGIN181466 14 46 11 17 186 6 280 3 UGIN181598 221 281 218 288 295 178 1481 2
UGIN181723 23 99 61 30 37 40 290 2 UGIN181503 266 289 285 133 267 227 1467 1
UGIN181678 19 94 14 41 121 11 300 1
UGIN180342 26 19 82 26 87 60 300 3
CBSD3s, CBSD severity at 3MAP; CBSD3i , CBSD incidence at 3MAP; CBSD6s, CBSD severity at 6MAP; CBSD6i , CBSD incidence at 6MAP CBSDri , CBSD root incidence
at 12MAP; CBSDrs, CBSD root severity at 12MAP; SI, rank summation index; ttl_caro, total carotenoid content; Mkumba, CBSD resistant/tolerant check; UG110017,
resistant/tolerant check; TME 204, CBSD susceptible check. Checks were included to enable direct comparisons with test genotypes. The non-weighted rank-summation
SI was used in ranking.
(UGIN181367 and UGIN181371) among the best performers increased viral inoculum resulting from stem recycling. Escape
for CBSD at CET. This situation presents an opportunity variants underscore why the selection for CBSD resistance among
to select superior genotypes for further evaluation of traits previously untested genotypes should not focus on seedling
of interests. Similar reports suggested by Mrema (2016) evaluations alone. This is because, at SET, the viral load in stem
also highlighted on cassava families with varying number of cuttings would be low compared to that in the clonal level. Also,
seedlings that exhibited CBSD symptoms and seedlings that seedling evaluations and data collection are based on a single
were symptomless. plant, as opposed to 10 plants at the clonal stage. Thus, the
A similar phenomenon was reported by Shirima et al. evaluation at the clonal stage allows for better phenotypic data
(2019), who noted the degeneration of cassava genotypes due to computation and exposes escape variants, such as the case of
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TABLE 6 | Family based responses to CBSD of the best-15 and worst-15 Nigerian genotypes evaluated at Namulonge in 2019.
Families of the Best-15 genotypes Families of the Worst-15 genotypes
Clones Family Progenitors SI ttl_caro Clones Family Progenitors SI ttl_caro
UGIN180416 F001 F153P046 × F58P008 255 1 UGIN180141 F005 F50P003 × F58P008 1631 1
UGIN180342 F004 F153P046 × F58P008 300 3 UGIN180481 F008 F153P046 × F154P012 1498 2
UGIN180247 F014 F168P002 × F63P006 145 4 UGIN180201 F010 F154P011 × F10P008 1517 1
UGIN180528 F018 F153P053 × F58P008 106 1 UGIN180263 F015 F50P003 × F58P002 1592 1
UGIN180602 F022 F154P012 × F163P008 223 4 UGIN180552 F020 F153P014 × F63P014 1651 2
UGIN181367 F036 F152P004 × F63P006 102 2 UGIN181162 F051 F12P061 × F162P008 1560 3
UGIN181371 F036 F152P004 × F63P006 218 3 UGIN181204 F054 F77P003 × F58P008 1629 1
UGIN181154 F051 F12P061 × F162P008 206 2 UGIN181352 F064 F158P046 × F11P011 1580 1
UGIN181326 F063 F58P008 × F122P006 197 1 UGIN181343 F064 F158P046 × F11P011 1481 1
UGIN181346 F064 F158P046 × F11P011 239 1 UGIN181454 F069 F165P009 × F2P030 1495 1
UGIN181466 F070 F87P016 × F64P001 280 3 UGIN181503 F072 F58P008 × F91P001 1467 1
UGIN181535 F075 F26P004 × F10P007 142 1 UGIN181592 F079 F153P046 × F58P013 1513 3
UGIN181678 F084 F91P011 × F162P008 300 1 UGIN181598 F079 F153P046 × F58P013 1481 2
UGIN181723 F088 F124P001 × F63P014 290 2 UGIN181764 F090 F153P046 × F10P008 1590 1
UGIN181791 F093 F124P001 × F162P008 187 1 UGIN181784 F092 F165P009 × F124P001 1547 1
SI, Selection index; ttl_caro, total carotenoid content. Out of 106 families, a total of 24 had progenies among the best 30 performers. The non-weighted rank-summation
SI was used in ranking.
UGIN180447 and other accessions that exhibited marginal CBSD by mean severities and incidences of about 1.4 and 20%
symptoms in the seedling trial. respectively (Table 1).
Significant differences were recorded among test genotypes A non-weighted rank summation SI, which comprised the
for all traits in the CET, except CBSD incidence at six months summation of genotype rank for CBSD incidence and severity
(Table 1). A mean score of 84.4 for CBSD6i indicates that data at three, six, and 12 months, was used to rank the
most genotypes exhibited high levels of CBSD at six months, performance of the test genotypes (Table 5). UGIN181367
explaining why there were no significant variations among the (SI = 102) was the overall best genotype in its response to
test genotypes. This reinforces the lack of resistance alleles CBSD. This genotype exhibited marginal symptoms to CBSD
in the Nigerian germplasm. Significant differences in CBSD foliar and root severity and incidence at both SET and CET.
root severity at three, six, and 12 months, however, indicate However, UGIN181367 was ranked third after NAROCASS 1
differential responses of the genotypes. Similar findings were and Mkumba, the two resistant checks. NAROCASS 1 and
reported by Abaca et al. (2012), Kaweesi et al. (2014), and Mkumba had SI values of 6 and 35, respectively. They are varieties
Pariyo et al. (2015), who identified varied resistance/susceptibility that exhibit high tolerance to CBSD (Mukiibi et al., 2019).
categorizations of foliar and root severities. This observation is in Interestingly, a few other genotypes, including UGIN180528,
accordance with earlier studies by Jennings (1960) and Hillocks UGIN181535, UGIN180247, also had a high SI ranking and
and Thresh (2000), who reported that different cultivars respond exhibited marginal symptoms for CBSD foliar and root severity
differently to CBSD. and incidence (Table 5). These identified genotypes merit for
For the clonal trial, the significant positive correlations further evaluations to confirm their CBSD responses.
between CBSD shoot severity and incidence, with CBSD Broad-sense heritability estimates ranged from moderate to
root severity and incidence (Table 3), agree with the reports high for all traits in the clonal trial (Table 1). Except for
suggested by Abaca et al. (2012) and Mrema (2016). Results CBSDrs and CBSDri, heritability estimates of CBSD incidence and
also indicated negative correlations between CBSD and severity at six and 12 months were comparable to those presented
CMD, which were largely non-significant except for CBSD3s by Kayondo et al. (2018) and Ozimati et al. (2018) (CBSDrs
(Table 3). The negative correlation suggests that the traits H2 = 0.25 and 0.26, respectively). The heritability estimates for
were under the control of different genetics. The negative CBSDrs in the clonal trial were also similar to the reports
correlations between harvest index and CBSD illustrate the suggested by Okul Valentor et al. (2018) (H2 = 0.69). Estimates
damage inflicted by CBSD, as observed in previous studies of broad-sense heritability for CBSD incidence were generally
by Nuwamanya et al. (2015) and Mrema (2016). The non- lower than those of CBSD severity in the clonal trial (Table 1).
significant negative correlation between harvest index and This contrasts with the findings suggested by Okul Valentor
CMD is likely due to high CMD resistance among the et al. (2018), who reported higher broad-sense heritability
evaluated germplasm. CMD resistance breeding has been estimates for CBSD incidence. Accordingly, heritability estimates
ongoing in Nigeria since 1932 (Hahn et al., 1980). Thus, for CBSDs and CBSDi in the clonal trials suggest that effective
most of the Nigerian germplasm was resistant as evidenced selection can be made at the clonal stage.
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
FIGURE 7 | Comparison of CBSD susceptible and resistant checks to test genotypes at 6 and 12 months. CBSD6i , CBSD incidence at 6MAP; CBSD6s, CBSD
severity at 6MAP; CBSDri , CBSD root incidence; CBSDrs, CBSD root severity; SI, Selection Index.
CONCLUSION and in diverse sites to confirm their resistance/tolerance to
CBSD. In addition, crossing the 15 identified clones with
This study was initiated on the premise of determining the field CBSD-resistant Ugandan cassava varieties would ensure the
reaction of Nigerian cassava genotypes to CBSD. Therefore, this introduction of more resistance alleles into the genome of the
could inform the extent of CBSD resistance/susceptible allele Nigerian population. The introgression of CBSD resistance from
distribution in the elite Nigerian germplasm used for cultivation East African clones is, therefore, critical as a preemptive breeding
and/or genetic improvement. Based on the generated datasets, it strategy for CBSD resistance in Nigeria. This will help the
can be concluded that most of the genotypes that constituted the Nigerian cassava breeding program to develop varieties with
Nigerian cassava population exhibited significant susceptibility to more durable resistance to the disease. Furthermore, continued
CBSD within the 2-year evaluation period. Fortunately, 15 clones screening and characterization of Nigerian cassava germplasm
have been identified to have either limited or no CBSD symptoms. for responses to CBSD infection is important to identify more
These genotypes can be re-evaluated at higher plot capacities genotypes with CBSD tolerance or resistance traits. Deploying
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Ano et al. CBSD-Evaluation of Nigerian Cassava Accessions
such tolerant or resistant cultivars can help in the effective control FUNDING
of the disease spread and reduction in losses associated with it.
The authors thank the UK’s Foreign, Commonwealth and
Development Office (FCDO) and Bill and Melinda Gates
DATA AVAILABILITY STATEMENT Foundation (Grant INV-007637, http://www.gatesfoundation.
org) for their financial support.
The original contributions presented in the study are included
in the article/Supplementary Material, further inquiries can be
directed to the corresponding author. ACKNOWLEDGMENTS
The authors thank all technicians and support staff of Root
AUTHOR CONTRIBUTIONS Crops Programme, NaCRRI, who participated in CBSD data
collection for experiments conducted during the 2018/2019
CA was involved in conceptualization, data collection, data and 2019/2020 planting period. The authors appreciate the
analysis, and manuscript writing. MO-S was involved in collaborative support with the National Root Crops Research
conceptualization, manuscript writing, manuscript editing, and Institute (NRCRI), Nigeria, where the breeding materials
supervision. AI and DN were involved in manuscript editing and originated. The authors acknowledge the contribution of
supervision. AO involved in the data collection, data analysis, Makerere University Regional Center for Crop Improvement
and manuscript editing. PG was involved in conceptualization, (MaRCCI). This study is a part of graduation study of CA at
supervision, and manuscript editing. RK was involved in Makerere University, Uganda.
conceptualization, data collection, data analysis, supervision,
manuscript writing, and manuscript editing. JO was involved
in conceptualization, manuscript editing, fund acquisition, and SUPPLEMENTARY MATERIAL
supervision. CE was involved in conceptualization, manuscript
writing, manuscript editing, fund acquisition, and supervision. The Supplementary Material for this article can be found
All authors contributed to the article and approved the online at: https://www.frontiersin.org/articles/10.3389/fpls.2021.
submitted version. 720532/full#supplementary-material
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et al. (2012). First report of Ugandan cassava brown streak virus on cassava in absence of any commercial or financial relationships that could be construed as a
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Munganyinka, E., Ateka, E. M., Kihurani, A. W., Kanyange, M. C., Tairo, F.,
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