Published March 2, 2017
Research
Selection of Simple Sequence Repeat Markers
Associated with Inheritance of Sweetpotato Virus
Disease Resistance in Sweetpotato
Benard Yada, Agnes Alajo, Gorrettie N. Ssemakula, Robert O.M. Mwanga,
Gina Brown-Guedira, and G. Craig Yencho*
ABSTRACT
Sweetpotato virus disease (SPVD), a complex
of Sweet potato chlorotic stunt virus (SPCSV;
Crinivirus) and Sweet potato feathery mottle
virus (SPFMV; Potyvirus) causes high yield
losses in sub-Saharan Africa (SSA). The development of resistant cultivars to SPVD has been
limited by the complex sweetpotato [Ipomoea
batatas (L.) Lam. var. batatas] genetics and
high levels of mutations in the causal viruses.
The objectives of this study were to understand
the inheritance of SPVD resistance and identify
simple-sequence repeat (SSR) markers associated with its resistance in a biparental sweetpotato mapping population. A total of 287 progeny
and parents of the ‘New Kawogo’  ‘Beauregard’ population were genotyped with 250 SSR
markers and phenotyped for SPVD resistance
at three sites and two seasons in Uganda. The
broad-sense heritability for SPVD resistance
was 0.51. Two progeny showed positive transgressive segregation for overall genotype mean
SPVD severity across sites and seasons. A total
of seven SSR markers were significantly associated with SPVD resistance in this population.
These markers and other SSRs need to be
used to fine map the quantitative trait loci (QTL)
of SPVD resistance for future implementation
of marker-assisted selection (MAS) for SPVD
resistance in sweetpotato.
B. Yada and G.C. Yencho, Dep. of Horticultural Science, North
Carolina State Univ., 214 Kilgore Hall, Box 7609, Raleigh, NC 276957609, USA; A. Alajo and G.N. Ssemakula, National Agricultural
Research Organization, National Crops Resources Research Institute,
Namulonge, P.O. Box 7084, Kampala, Uganda; R.O.M. Mwanga,
International Potato Center, Naguru Hill, Ntinda II Road, Plot 47,
Box 22274, Kampala, Uganda; G. Brown-Guedira, USDA–ARS, Dep.
of Crop Science, North Carolina State Univ., 4114 Williams Hall, Box
7620, Raleigh, NC 2769, USA. Received 22 Aug. 2016. Accepted 21
Nov. 2016. Assigned to Associate Editor Yiqun Weng. *Corresponding
author ([email protected]).
Abbreviations: AFLP, amplified fragment length polymorphism;
BLUP, best linear unbiased prediction; G  E, genotype  environment interaction; Gen(Gtype), least significant means of individual genotypes (parents and progeny) across sites and seasons; Gtype, least significant means of parents and the overall mean of the progeny; MAS,
marker-assisted selection; NaCRRI, National Crops Resources Research
Institute; NaSARRI, National Semi-Arid Resources Research Institute;
NgeZARDI, Ngetta Zonal Agricultural Research and Development
Institute; PCR, polymerase chain reaction; QTL, quantitative trait loci;
RAPD, random amplified polymorphic DNA; SNP, single-nucleotide
polymorphism; SPCSV, Sweet potato chlorotic stunt virus; SPFMV, Sweet
potato feathery mottle virus; SPVD, sweetpotato virus disease; SSA, subSaharan Africa; SSR, simple-sequence repeat.
G
lobal sweetpotato production is severely constrained by
SPVD (Valverde et al., 2007). Devastating yield losses are
particularly experienced in SSA where sweetpotato is grown for
food and nutrition security (Karyeija et al., 1998a; Tairo et al.,
2005). Sweetpotato virus disease causes yield losses of up to 98%
in SSA (Gibson et al., 1998; Karyeija et al., 1998a; Tairo et al.,
2004). Yield losses of 30 to 50% can occur in the US farmers’
sweetpotato fields if not well managed (Clark and Hoy, 2006).
Published in Crop Sci. 57:1–10 (2016).
doi: 10.2135/cropsci2016.08.0695
© Crop Science Society of America | 5585 Guilford Rd., Madison, WI 53711 USA
This is an open access article distributed under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
crop science, vol. 57, may– june 2017
www.crops.org1
Over 20% sweetpotato yield losses occur in China as a
result of SPVD (Feng et al., 2000).
Sweetpotato virus disease is a difficult to manage disease complex resulting from the synergistic dual infection by the silverleaf whitefly [Bemisia tabaci (Gennadius)]
transmitted SPCSV and the aphid [Aphis gossypii (Glover)]
transmitted SPFMV (Gibson et al., 1997; Karyeija et al.,
2000). Though many varieties are resistant to SPFMV, the
coinfection of SPCSV normally leads to break down in
putatively SPFMV-resistant varieties (Aritua et al., 1998;
Mukasa et al., 2003, 2006; Kreuze et al., 2008).
Recently, SPCSV isolates of similar strains to the ones
occurring in eastern Africa were reported in farmers’ fields
in China, posing further threat to global sweetpotato production (Qiao et al., 2011). Apart from vector transmission, clonal propagation of sweetpotato also enhances the
spread of SPVD (Karyeija et al., 1998a). The symptoms
of SPVD infection include overall stunting, leaf narrowing and distortion, chlorosis, and mosaics or vein-clearing
(Gibson et al., 1998).
The main approach for SPVD management in the
high virus pressure areas, like in SSA, has been the use
of clean planting material of moderately virus-resistant
landraces like New Kawogo and ‘Tanzania’ (Aritua et al.,
1998; Byamukama et al., 2004). Absence of a functional
formal sweetpotato seed system in SSA has made SPVD
management using clean seed lots of resistant varieties
difficult (Mukasa et al., 2003; Tairo et al., 2005). Also,
the limited sources of SPVD resistance in SSA have made
the management of SPVD challenging. However, SPVD
resistance has been demonstrated in the wild relatives of
sweetpotato (Karyeija et al., 1998b) and a few landraces
such as New Kawogo (Mwanga et al., 2001).
In eastern Africa, SPVD management was also
attempted through the transformation of some eastern
African varieties with the coat protein gene from the
russet crack strain of SPFMV, but this approach did not
succeed, as the plants succumbed to SPCSV in the field
(Okada et al., 2002; Wambugu, 2003; Tairo et al., 2005).
Recent molecular studies have provided a mechanistic
understanding of the synergistic interaction of SPCSV and
SPFMV and these may offer opportunities for future transgenic resistance work (Cuellar et al., 2009). The viral Class
1 RNase III enzyme from SPCSV has been identified as the
key factor behind SPVD and yield losses to which SPCSV
predisposes sweetpotato plants. As virus strains from various
regions are sequenced (Kreuze et al., 2002), future transformation of responsive genotypes for SPVD resistance through
the suppression of the RNase III enzyme by RNA interference method could offer a management option for SPVD.
Breeding for resistance to SPVD is difficult. Mass
selection based on observation of SPVD symptoms in the
field has been primarily employed in SSA where SPVD is
a problem (Mwanga et al., 2001). This method has relied
2
on the assembly and screening of large numbers of sweetpotato germplasm accessions and selection of parental
genotypes for use in hybridization schemes (Yada et al.,
2010b, 2011). However, this approach, like other phenotype-based screening approaches, is limited by environmental plasticity and has limited to the development of
SPVD-resistant varieties in SSA (Yada et al., 2010a).
The application of molecular markers is needed to
enhance breeding for SPVD resistance. The complex
and the polyploid nature of sweetpotato (2n = 6x = 90)
genome and limited genomic resources has slowed the
use of molecular techniques for sweetpotato improvement
over the years (Cervantes-Flores et al., 2008; Chang et al.,
2009). Another challenge to the application of molecular
markers for sweetpotato improvement is the occurrence of
high levels of self-incompatibility in sweetpotato (Martin,
1965; Gurmu et al., 2013). Self-incompatibility and polyploidy genome makes crossing difficult and complicates
the development of inbred lines for constituting the right
populations for genomic studies in sweetpotato.
As a result of the complex genome of sweetpotato, only
two QTL, spfmv1 and spcsv1, have been mapped for SPFMV
and SPCSV resistance, respectively, from a biparental cross
of Tanzania and Bikilamaliya landraces (Mwanga et al.,
2002a). These QTL were mapped with amplified fragment
length polymorphism (AFLP) and random amplified polymorphic DNA (RAPD) markers that have limited utility
for sweetpotato improvement through MAS. In a related
effort, some AFLP markers associated with SPVD resistances were identified through discriminant analysis and
logistic regression (Mcharo et al., 2005; Miano et al., 2008),
though the dominant nature of inheritance of AFLP markers has limited their use for breeding for SPVD resistance.
Another emerging method of molecular marker–trait
association in plant breeding is the regression of best linear
unbiased predictions (BLUPs) of genotype trait values
against marker profiles. This approach was developed for
predicting breeding values in animal breeding applications (Muir, 2007). Best linear unbiased prediction has
been used in several genetic studies for estimating random
effects of a mixed model (Piepho et al., 2008). One key
property of BLUP is the shrinkage toward mean, which
is a desirable property of an estimator, leads to a smaller
mean squared error, thus increasing accuracy of predictions (Robinson, 1991). Best linear unbiased prediction
additionally has the advantage of maximizing the correlation of true genetic values and predicted genetic values
and so has thus been widely used in animal breeding and
to some level in plant breeding (Schenkel et al., 2002).
Systematic future application of molecular markers
for SPVD resistance breeding will need the identification
and fine mapping of QTL of SPVD resistance based on
codominant SSR and single-nucleotide polymorphism
(SNP) markers from high-density linkage maps. This will
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crop science, vol. 57, may– june 2017
enable the implementation of MAS for SPVD resistance
for variety development. However, there are currently
limited numbers of sweetpotato SSRs (Buteler et al.,
1999; Hu et al., 2004; Schafleitner et al., 2010; Wang et
al., 2011) and no SNPs to enhance sweetpotato improvement for SPVD resistance through MAS.
The present study used regression analysis to associate
SSR markers with SPVD resistance in the ‘New Kawogo’
 ‘Beauregard’ mapping population segregating for SPVD
resistance. The association of SSR markers with SPVD resistance in sweetpotato will provide knowledge on the utility
of SSR markers for mapping SPVD resistance in sweetpotato as core genomic tools for sweetpotato are developed.
MATERIALS AND METHODS
Plant Material
A population of 287 F1 progeny from a biparental cross between
New Kawogo (NK) and Beauregard (B) was developed and
planted at National Crops Resources Research Institute
(NaCRRI), Kampala, Uganda (032 N, 3235 E, 1150 m asl)
in 2010. New Kawogo (female) is a sweetpotato weevil– and
SPVD-resistant, high dry matter content, and white-fleshed
(very low -carotene content) released landrace in Uganda
(Mwanga et al., 2001; Stevenson et al., 2009). Beauregard
(male) is a weevil- and SPVD-susceptible, low dry matter content, and orange-fleshed (high -carotene content) popular US
cultivar (Rolston et al., 1987).
Genomic DNA Extraction and SimpleSequence Repeat Genotyping
Genomic DNA was extracted from young leaves of each progeny at
NaCRRI Biosciences laboratory using a modified C-TAB method
(Doyle and Doyle, 1990). Details of the protocol are described in
Yada et al. (2015). DNA concentrations were measured using a
NanoDrop ND-1000 spectrophotometer (NanoDrop Technologies). The DNA samples were shipped to North Carolina State
University through DHL Express Courier for genotyping.
Briefly, a total of 405 published expressed sequence tags SSR
primers (Buteler et al., 1999; Hu et al., 2004; Schafleitner et al.,
2010; Wang et al., 2011) were redesigned by addition of M13
tail universal primer sequence (TGTAAAACGACGGCCAGT)
to the 5 end of the forward primer sequence. The primers were
synthesized by Eurofins Genomics (Huntsville, Alabama). The
complementary M13 sequence was labeled with fluorescent tags as
follows; VIC (green), 6FAM (blue), NED (yellow), and PET (red)
from Applied Biosystems (Foster City, California) for automated
detection of polymerase chain reaction (PCR) products.
The PCR was performed in a 10-L reaction volume consisting of 3.0 L (20–40 ng L−1) DNA template, 1.0 L of 10
PCR buffer, 1.0 L of 15 mM MgCl2, 0.8 L of 10 mM DNTPs
mix, 0.2 L forward primer (1.0 µM), 1.0 L reverse primer (1.0
µM), 0.5 L M13 primer (1.0 µM), 0.1 L Taq polymerase (50
U L−1), and 2.4 L PCR water. The PCR conditions were as
follows: one hold at 94.0C for 4 min, followed by first 15 cycles
of 94.0C denaturation for 30 s, 55.0C annealing for 30 s, and
72.0C extension for 1 min, also followed by 25 cycles of 94.0C
for 30 s, 50.0C annealing for 30 s, and 72.0C extension for 1
crop science, vol. 57, may– june 2017
min, followed by two holds at 72.0C for 7 min and at 4.0C for
infinite time. The PCR amplifications were performed using an
Eppendorf Mastercycler (Eppendorf AG).
The sizing of PCR products was done by capillary electrophoresis using an ABI3730xl Genetic Analyzer (Applied Biosystems).
The allele data were then analyzed using GeneMarker 2.2.0 (SoftGenetics, State College, Pennsylvania). The allele scores were later
converted to binary data, that is, 1 (allele present) and 0 (allele
absent) for subsequent analyses.
Field Trials and Sweetpotato Virus Disease
Resistance Screening
The 287 progeny and their parents were phenotyped for SPVD
resistance at three sites during two seasons in Uganda in 2012.
The experiments were conducted in a randomized complete
block design with three replications per clone at each site. Each
experimental plot consisted of five plants spaced 30 cm apart.
The plots were separated by 1.0 m.
The trials were conducted at the National Semi-Arid
Resources Research Institute (NaSARRI) (132 N, 3327 E),
Ngetta Zonal Agricultural Research and Development Institute (NgeZARDI) (2202 N, 3362 E), and NaCRRI. The
trials in the first season (2012A) were planted in June 2012 and
harvested in November 2012. The second season trials (2012B)
were planted in November 2012 and harvested in May 2013.
The trials were harvested at 5 to 6 mo after planting to allow for
more exposure of plant materials to SPVD pressure.
Sweetpotato virus disease resistance was measured by scoring the severity of damage using the disease symptoms on leaves
and stems at 6 wk after planting and at harvest. A disease rating
of 1 to 9 was used as in Grüneberg et al. (2010).
Data Analysis
Statistical analyses were done using only 284 progeny and the two
parents; three progeny had missing data and were excluded from
the analysis. The ANOVA for SPVD severity was done using the
generalized linear mixed model procedure, PROC GLIMMIX
(SAS 9.4; SAS Institute, 2013) with genotypes as fixed effects,
while block, site, and season were treated as random effects. We
used the Turkey–Kramer grouping ( = 0.05) for comparing the
overall SPVD least significant means of parents and the overall
mean of the progeny (Gtype) and the individual parent and progeny means across sites and seasons [Gen(Gtype)]. The genotype
least significant means were plotted to assess the level of transgressive segregation for SPVD resistance in the population. The
phenotypic and genotypic variances for SPVD severity in the
population were analyzed by PROC MIXED and PROC IML
and then used to calculate the broad-sense heritability estimate
for SPVD resistance in the population.
Marker–trait association was done using regression analysis of BLUPs of genotype SPVD severities against SSR allele
profiles. The mean SPVD severity BLUPs of genotypes was
analyzed using PROC MIXED (SAS 9.4; SAS Institute, 2013).
The mean genotype SPVD severity BLUPs were associated
with the SSR marker loci by regression implemented by PROC
GLIMMIX (SAS 9.4; SAS Institute, 2013) with genotypes as
fixed effects. We used the probability level ( = 0.05) for selecting markers highly associated with SPVD resistance.
www.crops.org3
Table 1. ANOVA of sweetpotato virus disease resistance in the progeny and parents of the ‘New Kawogo’  ‘Beauregard’
mapping population. Trials were planted at three sites (NaCRRI, NgeZARDI, and NaSARRI) and two seasons in a randomized
complete block design with three replicates in Uganda in 2012.
Source
Site†
Season‡
Site  season
Gtype§
Site  Gtype¶
Season  Gtype
Site  season  Gtype
Gen(Gtype)#
Site  Gen(Gtype)††
Season  Gen(Gtype)
Site  season  Gen(Gtype)
Block(site  season)
Residual‡‡
Sum of squares (SS)
Mean sum of
squares (SS/df)
F-value
2
1
2
1
2
1
2
284
567
284
562
441.0
24.2
19.3
0.4
27.8
4.2
2.2
1660.3
2275.1
646.6
1228.3
220.5
24.2
9.6
0.4
13.9
4.2
1.1
5.8
4.0
2.3
2.2
88.9
9.8
3.9
0.2
6.1
1.8
0.5
2.6
1.8
1.0
1.0
<0.0001
0.0018
0.021
0.6885
0.0023
0.1774
0.6162
<0.0001
<0.0001
0.5144
0.7562
12
3137
80.6
7180.1
6.7
2.3
2.9
–
0.0005
–
df
Pr > F
† Mean squares tests the significant effect of sites.
‡ Mean squares tests the significant effects of seasons.
§ Tests the significant effect of overall least significant mean of the parents vs. that of the progeny across sites and seasons.
¶ Tests the significant effect of site on overall parent and progeny least significant means.
# Tests the significant effect of least significant means of individual genotypes (parents and progeny) across sites and seasons.
†† Test the significant effect of genotype  environment interaction.
‡‡ Used in ANOVA to test significant effect of extraneous factors.
RESULTS
Analysis of Variance of Sweetpotato
Virus Disease
Both sites and seasons had significant effects on mean
SPVD severity of the genotypes (Table 1). The overall
mean genotype SPVD severity for NaCRRI, NgeZARDI,
and NaSARRI were 6.8, 3.4, and 3.8, respectively. The
overall mean genotype SPVD severity for Seasons 1 and 2
were 4.4 and 5.2, respectively. The mean SPVD severity
of parents compared with that of progeny (Gtype) was not
significantly different.
However, the mean SPVD severity for individual
progeny and parents across sites and seasons [Gen(Gtype)]
were significantly different (P < 0.0001) and ranged from
2.0 to 8.0 in progeny NKB216 and NKB225, respectively.
The overall mean SPVD severity for New Kawogo and
Beauregard were 3.2 and 7.5, respectively. Significant
genotype by site interaction for SPVD was observed in
this population (P < 0.0001), though the other interaction
effects were not significant.
Heritability and Transgressive
Segregation Analysis
The broad-sense heritability estimate for SPVD resistance
in this population was moderately high (H 2 = 0.51 
0.046). The distribution of genotype mean SPVD severity across seasons at NaCRRI was skewed to the left,
meaning that most genotypes succumbed to SPVD at
this location (Fig. 1A). Mean genotype SPVD severity at
this site ranged from 2.0 to 9.0 and the severities for New
4
Kawogo and Beauregard were 3.2 and 9.0, respectively.
Interestingly, three genotypes, NKB216, NKB104, and
NKB32, performed better than New Kawogo for SPVD
resistance at this site. The top 10 most SPVD-resistant
clones at NaCRRI were NKB216, NKB32, NKB252,
NKB249, NKB215, NKB104, NKB135, NKB230,
NKB255, and NKB37. The five least-resistant clones to
SPVD at NaCRRI were NKB24, NKB271, NKB88,
NKB232, and NKB212.
On the other hand, the means across seasons’ genotype SPVD severity at NgeZARDI and NaSARRI were
slightly right skewed. Mean genotype SPVD severity
at NgeZARDI ranged from 2.0 to 8.0 (Fig. 1B). New
Kawogo and Beauregard had mean severities of 2.3 and
7.6, respectively. A total of 19 progeny exhibited positive transgressive segregation for SPVD resistance at
NgeZARDI. The top 10 most SPVD-resistant progeny
at this site were NKB18, NKB55, KNB168, NKB91,
NKB249, NKB96, NKB116, NKB259, NKB52, and
NKB67, but the least five SPVD-resistant progeny were
NKB265, NKB31, NKB84, NKB170, and NKB256.
At NaSARRI, mean genotype SPVD severities across
seasons ranged from 2.0 to 7.0 (Fig. 1C) and the mean
SPVD severities of the parents were 2.1 and 6.5 for New
Kawogo and Beauregard, respectively. At this site, two
progeny, NKB195 and NKB204, exhibited positive transgressive segregation for SPVD resistance. The top 10
best-performing progeny for SPVD resistance at this site
were NKB195, NKB204, NKB277, NKB191, NKB241,
NKB277, NKB90, NKB210, NKB11, and NKB278. The
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crop science, vol. 57, may– june 2017
Fig. 1. Distribution of mean sweetpotato virus disease (SPVD) severity in the progeny and parents of the ‘New Kawogo’ (NK)  ‘Beauregard’ (B) mapping population at (A) NaCRRI, (B) NgeZARDI, (C) NaSARRI, and (D) overall mean across sites and seasons. Bars represent
the number of clones in each class of mean SPVD severity scores averaged over seasons for sites and averaged over sites and seasons
for the overall mean
five worst-performing progeny for SPVD resistance here
were NKB35, NKB196, NKB38, NKB45 and NKB5.
The overall mean genotype SPVD severity across sites
and seasons ranged from 2.0 to 8.0 (Fig. 1D). New Kawogo
and Beauregard had overall mean SPVD severities of 2.5
and 7.7, respectively. The top 10 best-performing progeny
for overall mean SPVD resistance across sites and seasons
were NKB216, NKB104, NKB32, NKB249, NKB55,
NKB90, NKB277, NKB252, NKB135, and NKB116.
The five worst-performing genotypes for overall SPVD
resistance across sites and seasons were NKB265, NKB130,
NKB31, NKB5, and NKB170.
None of the top 10 best-performing progeny for
SPVD resistance had consistent high performance across
the three sites. In the same way, none of the five worstperforming clones had consistent performance across the
three sites. However, progeny NKB249 and NKB252 performed well for mean SPVD resistance at both NaCRRI
and NgeZARDI but did not perform well at NaSARRI.
The highest-yielding (48.4 t ha−1) genotype, NKB216,
was the most SPVD-resistant genotype in this population.
However, 15 of the top 16 high-yielding genotypes with
cultivar release potential had relatively high SPVD damage
ranging from 3.8 to 5.4 (Table 2). The high-yielding and
high--carotene content genotypes from our study, such
as NKB254 and NKB135, suffered high SPVD damage
and could be used as parents for population improvement
for yield and -carotene content and to improve on their
dry matter content and SPVD resistance.
crop science, vol. 57, may– june 2017
Marker–Trait Association
Out of the 405 SSR markers screened, 250 were polymorphic on the parents and selected progeny. However, after
genotyping the whole population with the polymorphic
markers, 133 SSR markers were identified to be useful for
association of SPVD resistance. Details on the markers,
including the polymorphic information, are described in
Yada et al. (2015).
The number of SSR markers significantly associated
with mean SPVD resistance at the three sites and with
the overall mean SPVD resistance is shown in Table 3.
A total of seven SSR markers were significantly associated with overall mean genotype SPVD resistance.
Three SSR markers were associated with SPVD resistance at NaSARRI and NgeZARDI, respectively, while
five SSR markers were associated with SPVD resistance
at NaCRRI. However, most of these markers were not
highly significantly associated with SPVD resistance (P
= 0.05). The amount of total variance in mean overall
genotype SPVD resistance in the population explained by
the six selected markers was 24.6%. Marker IBS166 was
the most significantly associated SSR marker with mean
genotype SPVD resistance in this population.
DISCUSSION
Sweetpotato virus disease is the most devastating disease
of sweetpotato in SSA (Karyeija et al., 1998a; Tairo et
al., 2005). The areas around the Lake Victoria crescent
in Uganda were reported to have the highest incidence
of SPVD in SSA (Mukasa et al., 2003). Our findings are
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Table 2. Performance of the top 16 progeny with cultivar release potential across sites and seasons ranked using mean storage root yield (YLD), dry matter (DM), -carotene (BC) content, and sweetpotato virus disease (SPVD) resistance. Trials were
conducted at three sites (NaCRRI, NgeZARDI, and NaSARRI) and two seasons in a randomized complete block design (RCBD)
with three replicates in Uganda in 2012.
Mean
Rank†
YLD‡
DM§
BC¶
SPVD#
YLD
DM
BC
SPVD
NKB216
NKB9
NKB254
NKB177
NKB168
NKB93
NKB21
NKB153
NKB105
NKB114
NKB15
NKB193
NKB3
NKB201
48.4
41.0
40.4
40.1
38.8
38.5
38.3
38.1
37.9
36.8
36.5
36.4
36.1
35.9
29.0
30.4
24.3
30.6
29.1
30.9
29.4
29.5
28.5
25.2
28.1
30.3
28.0
30.4
9.7
7.4
29.1
9.3
8.7
6.2
9.7
10.0
14.0
6.8
20.7
11.5
17.8
12.0
2.0
5.4
5.3
3.8
4.3
4.6
5.1
5.1
5.4
5.2
5.4
4.7
4.4
4.6
1
2
3
4
5
6
7
8
9
10
11
12
13
14
138
63
285
55
134
44
112
105
178
282
208
69
213
60
187
250
3
200
218
272
188
175
94
263
31
131
56
122
1
223
217
7
29
62
165
173
222
187
219
195
53
75
NKB5
NKB135
35.8
35.7
29.7
25.6
5.5
20.9
6.4
3.9
15
16
100
277
280
29
279
10
Genotype
† Ranking of 286 genotypes (284 progeny and two parents) in descending order for storage root yield, dry matter, -carotene content, and sweetpotato virus disease resistance.
‡ YLD, genotype least significant mean storage root yield (t ha−1) averaged over three sites and two seasons.
§ DM, genotype least significant mean storage root dry matter content (%) averaged over three sites and two seasons.
¶ BC, genotype least significant mean storage root -carotene content (mg 100 g−1) averaged over three sites and two seasons.
d SPVD, genotype least significant mean sweetpotato virus disease resistance averaged over three sites and two seasons.
Table 3. Association of simple-sequence repeat (SSR) markers with the best linear unbiased predictions of across-sites and
seasons sweetpotato virus (SPVD) disease severity of genotypes at sites and overall mean across sites and seasons.
Site
Marker†
Alleles‡
Most significant allele§
R2 ¶
SPVD Mean
ProbF
NaCRRI
IbU22
IbY59
IBS166
IbL20
IBS82
5
3
3
3
5
IbU22NK144
IbY59NK133
IBS166NKB294
IbL20NKB175
IBS82NKB139
0.037
0.026
0.025
0.019
0.017
0.001
0.001
0.001
0.001
0.001
0.021
0.030
0.011
0.044
0.046
NgeZARDI
IBS166
IbE19
IbE5
3
3
3
IBS166NKB294
IbE19NKB169
IbE5NKB227
0.028
0.016
0.012
0.002
0.001
0.001
0.011
0.041
0.049
NaSARRI
IBS45
IBS166
IbY53
4
3
3
IBS45NK177
IBS166NKB294
IbY53B274
0.029
0.024
0.022
0.000
0.002
0.001
0.039
0.042
0.049
Overall
IBS118
IBS166
IBS82
IbE5
IbL20
IbU4
IbY53
3
3
5
3
3
4
3
IBS118NK210
IBS166NKB294
IBS82NKB139
IbE5NKB227
IbL20NKB175
IbU4NKB182
IbY53B274
0.028
0.050
0.042
0.030
0.029
0.039
0.029
0.001
0.001
0.002
0.001
0.001
0.001
0.001
0.049
0.007
0.043
0.039
0.044
0.031
0.046
† SSR markers that were highly associated with SPVD resistance selected out of 133 SSRs analyzed in the study.
‡ Number of alleles per SSR marker.
§ Marker allele that had the highest significant association with SPVD resistance and also the allele within the marker that accounted for the highest variance for SPVD
resistance.
¶ R2, proportion of variance of SPVD severity explained by SSR markers.
consistent with this observation, since NaCRRI, which
is located within the Lake Victoria crescent, showed the
highest mean across season SPVD severity (6.8). On the
6
other hand, NgeZARDI and NaSARRI, located >300
km away from the Lake Victoria crescent, had lower mean
SPVD severities of 3.4 and 3.8, respectively.
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crop science, vol. 57, may– june 2017
The relatively cool and moist environment around
the Lake Victoria crescent for the most part of the year is
favorable for enhancing the population dynamics of whiteflies that transmit SPCSV, the more damaging of the two
viruses causing SPVD (Aritua et al., 1998; Byamukama et
al., 2004). Oppositely, NaSARRI and NgeZARDI have
two hot, dry spells every year, and this impedes the reproduction and survival of whiteflies, as most sweetpotato
crops, and likely alternate hosts of whiteflies and aphids, dry
out during these dry spells. The dry spells at NgeZARDI
are not as severe as those at NaSARRI, thus the reason for
the slightly lower mean SPVD severity at NgeZARDI.
These agroecological differences were reflected in the
significant genotype  environment interaction (G  E)
results observed for SPVD resistance in the different trial
sites (Table 1). None of the genotypes, either among the
top 10 or the bottom five, showed consistent performance
across the three sites. Significant G  E for SPVD resistance in sweetpotato was also reported in multilocation
evaluation of 15 clones that included Ugandan landraces
and introductions from the International Potato Center
(Byamukama et al., 2002). In addition to environmental differences, G  E interaction for SPVD resistance is
also attributed to the diversity of sweetpotato virus strains
present in the different agroecologies. Molecular studies
showed the occurrence of different sweetpotato virus isolates in different geographical zones, and such diversity
was attributed to high mutation rates in the constituent
viruses (Ateka et al., 2007).
Genotype significantly influenced the response to
SPVD pressure in our study. Sweetpotato genotypes have
been demonstrated to show differences in response to
SPVD pressure. Beauregard is highly susceptible to sweetpotato viruses in Louisiana (Clark and Hoy, 2006), while
New Kawogo is moderately resistant to SPVD in Uganda
(Mwanga et al., 2001). Studies also demonstrated that
significant variation occurred in the level of SPVD resistance in the Ugandan sweetpotato germplasm (Bua et al.,
2006; Yada et al., 2011). The highly significant difference
among the progeny in our study is beneficial and could be
exploited for selection of sources of SPVD resistance for
use in sweetpotato population improvement in SSA.
The progeny in our New Kawogo  Beauregard population was expected to react differently to SPVD pressure as
segregation occurs at F1 in sweetpotato hybrids. This diverse
progeny performance was expected because of the diverse
gene pools from which the parents were selected. Just like
in our study, progeny from diallel families responded differently to SPVD, but at NaCRRI, most of them succumbed
to high SPVD pressure (Mwanga et al., 2002b). Future
genetic gains in SPVD resistance will need the selection and
hybridization of diverse parents for SPVD resistance.
The distribution of mean progeny SPVD severity differed with the evaluation sites. The distribution of mean
crop science, vol. 57, may– june 2017
genotype SPVD severity at NaCRRI was highly skewed
to the left, but at NgeZARDI and NaSARRI, severity
scores were slightly right skewed. The overall individual
progeny mean SPVD severities over sites and seasons were
normally distributed. The skewed distribution at NaCRRI
was attributed to the very high SPVD pressure at this site,
while SPVD pressure is much lower at NgeZARDI and
NaSaRRI. Thus, NaCRRI has been used for routine
screening of breeding lines for SPVD resistance in Uganda.
Over 100,000 clones are routinely screened at NaCRRI for
SPVD resistance before advancing of the promising clones
for yield trials (Mwanga et al., 2007).
Less than 10 genotypes exhibited transgressive segregation for SPVD resistance in this population at the three
sites. The genotypes exhibiting transgressive segregation
could be having genetic mechanisms of either restricting
infection or suppressing development of the viruses or both.
Reports have shown that certain plant genotypes suppress
virus infection by limiting virus multiplication and movement through the cells and vascular tissues (Valkonen,
1994). The genotypes exhibiting transgressive segregation
could also be expressing tolerance, which is the ability of
infected plants to offset the effects of infection so that storage root yields would not be reduced relative to a susceptible check clone (Valkonen, 1994). However, tolerance is
screened against in the NaCRRI breeding program.
Another reason for the low SPVD severity in these
superior genotypes could be recovery from infection after
the delayed harvest. Recovery is the ability of plants to
show partial or complete loss of symptoms on originally
SPVD-infected plants. Recovery was observed in New
Kawogo (Mwanga et al., 2002a), and this trait could be
segregating in the progeny. However, the genetic mechanism for this phenomenon is not understood.
The high-performing progeny may also possess morphological features, such as heavy vine and leaf pubescence, that inhibit whitefly and aphid feeding. This needs
to be confirmed through morphological characterization.
Some Ugandan sweetpotato germplasm with dense vine
and leaf pubescence had low SPVD severities, and this
resistance was attributed to antixenosis through vector
inhibition (Yada et al., 2010a, 2011). As the harvesting of
these trials was delayed, we could rule out escape as the
cause of low SPVD severity in these resistant genotypes
and consider this reaction as active and heritable SPVD
resistance to a great extent.
Apart from the clone NKB216, which was the highest
yielding and SPVD-resistant genotype, the rest of the highyielding genotypes had high SPVD damage. Resistance in
these higher-yielding genotypes likely was due to tolerance, since storage root yield was not significantly reduced
by severe SPVD infection. The SPVD resistance performance exhibited by the SPVD-resistant progeny is similar to that of the female parent, New Kawogo, which was
www.crops.org7
reported to have moderate SPVD field resistance (Mwanga
et al., 2001). Most of the released high-yielding and orangefleshed cultivars in Uganda are resistant to SPVD (Mwanga
et al., 2009). Some of the superior genotypes in this study
could be released for production as high-yielding cultivars
in low-SPVD-pressure SSA countries after yield trials.
Our study demonstrated SPVD resistance to be a
moderately heritable trait (H 2 = 0.51), meaning that
>50% of the observed SPVD reaction in this population was explained by genotypic variance. Mwanga et al.
(2002b) reported, using a diallel cross population, that
SPVD resistance is quantitatively inherited with a moderate-to-high broad-sense heritability (H 2 = 0.73–0.98).
In another diallel population, the broad-sense heritability
estimate for SPVD resistance was high (H 2 = 0.85–0.98),
while narrow-sense heritability estimate was low (h2 =
0.48) (Hahn et al., 1981). Therefore, substantial SPVD
resistance expressed in the transgressive segregants in this
population was inherited. This means that multiple SPVD
resistance can be incorporated into adaptable sweetpotato
genotypes to enhance resistance through breeding. The
moderately high heritability estimate for SPVD resistance
in our study also meant that it was possible to associate
SSR markers with SPVD resistance as a result of the high
genetic nature of this trait in this population.
The SSR regression analyses led to the selection of
seven SSR markers significantly associated with SPVD
resistance in this population. This SSR marker–SPVD
resistance association in sweetpotato in our study, though
successful, was limited by the low amount of variance and
significance levels of SSR loci. The amount of variation
in SPVD resistance explained by the selected SSR markers was lower than that reported with AFLP and RAPD
markers that explained over 70% of resistance to SPCSV
and SPFMV (Mwanga et al., 2002a). The low variability
in our analysis could have been due to the limitation of
the markers used in this analysis to capture the quantitative nature of the trait. This study, however, shows that
SSRs are linked to SPVD resistance loci in sweetpotato
and could be used for future mapping of SPVD resistance
to enhance breeding.
Earlier, the AFLP and RAPD markers e41m33.a and
S13.1130 were reported to be associated with SPFMV
and SPCSV resistance, respectively, through discriminant analysis (Mcharo et al., 2005). Miano et al. (2008)
also identified four AFLP markers highly associated
with SPVD resistance in sweetpotato and proposed that
they could be used for selecting SPVD resistance. However, because of the polyploid nature of the sweetpotato
genome, these AFLP-based SPVD resistance loci have not
been used for sweetpotato improvement. The AFLPs are
dominantly inherited and not suitable for differentiating
heterozygous and homozygous alleles that typically occur
in polyploid genomes.
8
The ability to identify and associate alleles within
SSR loci with SPVD resistance in our study makes SSR
markers a better alternative to AFLPs in enhancing sweetpotato genomic improvement. In the short term, the SSR
markers significantly associated SPVD resistance could be
used for genetic diversity analysis of sweetpotato germplasm for selecting diverse parents for SPVD resistance
improvement. This diversity data could be augmented
with phenotypic data to select suitable parents to ensure
better genetic gains in SPVD resistance. In the long term,
however, more SSR markers need to be developed to
facilitate sweetpotato genomic improvement. This, coupled with development of sweetpotato SNPs, will lead to
development of high-density genetic linkage maps for fine
mapping of SPVD resistance for use in MAS.
CONCLUSION
This study demonstrated that wide biparental crosses will
be useful for future improvement of SPVD resistance,
as such crosses generate progeny with high potential for
transgressive segregation for selection of SPVD resistance.
Second, SPVD resistance is a heritable trait in sweetpotato that can be mapped with codominant SSR markers
to enhance early selection of resistance. We therefore recommend that the New Kawogo  Beauregard population
be used for developing genomic resources for sweetpotato through genotyping-by-sequencing for SSR and
SNP marker development. Further phenotyping of this
population for SPVD resistance needs to be done to fine
map SPVD resistance with codominant markers for future
MAS of SPVD resistance.
Acknowledgments
This research was funded by the McKnight Foundation Collaborative Crop Research Program (CCRP) and the Norman E. Borlaug Leadership Enhancement in Agriculture Program (LEAP).
We thank Dr. Consuelo Arellano of the Department of Statistics,
NCSU, for providing assistance in statistical data analysis.
Conflict of Interest
The authors declare that there is no conflict of interest.
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