AJCS 18(07):401-407 (2024) ISSN:1835-2707
https://doi.org/10.21475/ajcs.24.18.07.p3994
Genetic diversity and population structure of a modified three-way
tomato hybrids for determining fruit size traits
Stephen I. Nnungu*
1,2
, Michael I. Uguru
2
1
Department of Botany, University of Dar es Salaam, Dar es Salaam,
Tanzania
2
Department of Crop Science, University of Nigeria, Nsukka, Nigeria
Abstract: The assessment of genetic diversity and
genetic structure of crops has a vital impact on the
plant breeding program, including the characterization,
use and conservation of genetic material. The genetic
diversity and genetic structure of a set of 94 F
3
tomato
hybrids were assessed with 25 polymorphic SNP
markers of quantitative trait loci (QTLs) underlying fruit
size in tomatoes using Sequenom Mass ARRAY system.
A total of 50 alleles were amplified and the average
polymorphic information content (PIC) was 0.2220. Nei's
genetic distance ranged from 0 to 0.62. Therefore,
single nucleotide sequence (SNP) markers detected a
significantly high degree of polymorphism in tomato
hybrids. Cluster analysis using the unweighted pair
group method with arithmetic mean methods (UPMA)
Submitted:
07/11/2023
Revised:
18/03/2024
Accepted:
24/04/2024
Full Text PDF
indicated that the tomato hybrids studied are grouped
into four main groups, which is to some extent
consistent with the size, shape and number of locules of
the tomatoes studied. Analysis of population structure
with SNP markers revealed three subpopulations.
Association mapping using 25 SNP markers detected 9
markers with a significant association with mean fruit
weight, fruit length, fruit diameter, number of locules,
and fruit shape index. The nine markers detected in this
study are recommended for the tomato fruit size
improvement breeding program.
Keywords: Genetic diversity, Population structure, SNPs markers,
Solanum lycopersicum
.
Abbreviations: BF_Beef (Florida); DNA_Deoxyribonucleic Acid;
QTL_Quantitative trait loci; PIC_polymorphic information content;
PR_Plumb (Rio grande); S_Supersteak; SNPs_Single nucleotide sequence;
UPGMA_Un-weighted Paired Group Method of Arithmetic Averages.
Introduction
Tomato (
Solanum lycopersicum
) is one of the most important local
market vegetables in Nigeria grown by small-scale farmers. Tomato
production is considered as one of the main agricultural enterprises as it
employs people in farms, processing industries and provides higher
income per hectare to small holder farmers than most staple crops
(AVRDC, 2006). However, they are many constraints affect the
productivity and quality of tomato. Some of such constraints are high
humidity and rainfall and lack of locally adapted cultivars.
The main objectives of current tomato breeding, such as increasing fruit
size, require a good understanding and management of the diversity of
cultivated genetic resources (Xu et al., 2013). Interpreting patterns of
genetic variability in cultivated landraces of economically important
crops allows breeders to reconsider this trait reservoir and, eventually,
identify new alleles to improve productivity, adaptation, fruit quality and
size, and nutritional value. To date, much of this germplasm has not
been widely characterized and most local varieties have not yet been
used in modern plant breeding (Huang et al., 2010).
The improvement of tomato with an ability to withstand the high
humidity conditions of South Eastern Nigeria impelled the initiation of a
hybridization programme. Crosses between two commercially acceptable
but poorly adapted cultivars, Roma VF and Tropica and wild variety
produced tomato hybrids with abundant fruiting (Atugwu and Uguru,
2012) and increased disease resistance (Uguru and Igili, 2002) under
high rainfall conditions. However, the average fruit size of the tomato
hybrids generated did not meet the level of acceptability in the local
market. This would necessitate further crosses between the hybrids with
exotic breeds with large fruited inbred (supersteak) which called a
modified three way crosses and the selection from the segregating
population. Successive evaluations of the progenies at different filial
generation from F
1
to F
2
showed reliable evidence of increased fruit yield
particularly in terms of fruit size. Since fruit size is quantitatively
inherited, that mean affected by environment, the molecular markers
analysis is inevitable to confirm the fruit size quantitative trait loci
incorporated in the tomato hybrids resulted from the modified three way
crosses.
Successful breeding for crop improvement programmes depends on
genetic variability that arises from genetic diversity (Ranaand Bhat,
2004). Lack of genetic variability may limit breeding progress and gain
from selection (Cornelious and Sneller, 2002). So, knowledge of the
genetic diversity of any germplasm collection provides a basis for
improvement of crops and development of superior cultivars. Detailed
understanding of the population structure and diversity is also needed
for the conservation planning, management and utilization of tomato
germplasm (Hamrick and Godt, 1996; Frankham et al., 2002).
The availability of cost-effective, accurate and rapid genotyping tests
has made single nucleotide polymorphism (SNP) the most frequently
used DNA marker for high-throughput plant analysis, encouraging
sequence variation analysis in germplasm collections. In different plant
species, molecular data were used to infer the existence of a genetic
structure in the study collection or to assign individuals to genetically
differentiated groups that may be compatible with their breeding history
(Mc Nailly et al., 2009).
Single nucleotide polymorphisms (SNPs) are known as a strong class of
molecular markers that have immense significance in plant genetics and
breeding because of their excellent distribution throughout the genome
and suitability for genetic diversity analysis, evolutionary relationships
and genetic population substructure estimation (Rafalski, 2002; Garris et
al., 2003; Varshney et. al., 2008). Therefore, Single Nucleotide
Polymorphisms (SNPs) markers of the quantitative trait loci (QTL)
underlying fruit sizes in tomato were performed in this study. The
present study aimed to investigate the genetic diversity and population
structure of three way tomato hybrids with respect to fruit size
determining traits.
Results
Single Nucleotide Polymorphisms (SNPs) diversity
The results from 25 SNPs markers used for this work on tomato fruit
size detected appreciable degree of polymorphism within the set of
tomato progenies used for this work. A total of 50 SNPs alleles were
detected and the total number of allele detected per primer was 2. Most
of the loci produced a maximum of two rare alleles. Some of the alleles
may be useful as diagnostic markers for some of the assayed tomato
progenies.
Most loci were highly polymorphic as indicated by values for
polymorphism information content (PIC), expected heterozygosity or
gene diversity (H
e
) and observed heterozygosis' (H
o
). The PIC value for
each marker ranged from 0.0487 for the marker detected by Solyc2 - 2
to 0.3749 for the marker detected by Solyc4 – 1 (Table 1). The markers
PIC value greater than 0.5 were considered highly informative and
markers with 0.5 >PIC>0.2 were just considered to be informative
(Bostein et al., 1980). However, because of the bi allelic nature of the
SNPs markers, the maximum PIC value is only 0.5 while SSRs markers
can go beyond 0.5. The variation was significantly associated with the
number of alleles detected at each locus. Therefore, SNPs markers
showed a reasonable amount of variation in the tomato genotypes in this
study.
The expected heterozygosity or gene diversity (He) value per marker
ranged from 0.05 at Solyc2 - 2 to 0.499 at Solyc4-1 with the mean value
of 0.266 (Table 1). The observed heterozygosities were ranged from
0.05 at Solyc2-2 to 0.372 at Solyc4-1. Overall, the expected
heterozygosities were higher than the observed heterozygosities. The
major alleles
Figure 1. Tomato parents used in this study.
Figure 2: Variation in fruit size and shapes of the F
3
progenies develop
from S x (W x R).
frequency for each marker ranged from 0.51 to 0.97; therefore the
minor alleles were less than 0.5 in most of the markers.
The genetic distance among the tomato progenies in this study
Based on the information obtained at the 25 SNPs loci, Nei genetic
distance coefficients were estimated for all pair-wise comparison of the
tomato genotypes (F
3
) developed from modified three- way cross
between advanced generation tomato hybrids and Supersteak (Figure 2).
The average distance between individual tomato progenies was
moderate at 0.56. The genetic distance among the F
2
tomato genotypes
ranged from 0.0 to 0.6174 (Supplementary Table 3) while for F
3
ranged
from 0.000 to 0.6154 (Supplementary Table 3). This value is an
indication of the magnitude of diversity among the progenies studied.
However, some tomato genotypes in both F
2
and F
3
showed 100%
similarities.
The largest genetic distance was observed between S28 and S25
(0.6174), while the lowest one was detected between S33 and S30, S33
and S31 (0.000) for the F
2
tomato genotypes. For the F
3
tomato
genotypes, the largest distance was observed between S63 and S55
(0.6154), while the lowest was detected between S64 and S55 (0.000).
Genetic diversity among tomato progenies using UPGMA-based cluster
analysis
Tomato progenies were separated using un-weighted pair-group mean
algorithm (UPGMA) dendrogram (Sneath and
Table 1. Allelic variation of 25 SNPs loci in the tomato hybrids.
Marker
MAF
G
Availability
He
Ho
PIC
Solyc04 - 1
0.5116
3.0000
0.7167
0.4997
0.3721
0.3749
Solyc11 - 1
0.9375
3.0000
0.9333
0.1172
0.0893
0.1103
Solyc11 - 3
0.9375
3.0000
0.9333
0.1172
0.0893
0.1103
Solyc11 - 7
0.9167
2.0000
0.5000
0.1528
0.1667
0.1411
Solyc11- 8
0.9286
2.0000
0.5833
0.1327
0.1429
0.1239
Solyc11 - 9
0.8750
3.0000
0.8667
0.2188
0.2115
0.1948
Solyc11 -10
0.8729
3.0000
0.9833
0.2219
0.2203
0.1973
Solyc11 - 11
0.8878
2.0000
0.8167
0.1993
0.2245
0.1794
Solyc11 - 12
0.6098
3.0000
0.6833
0.4759
0.5366
0.3627
Solyc11 - 13
0.7045
3.0000
0.7333
0.4163
0.3182
0.3297
Solyc11 - 14
0.7586
3.0000
0.9667
0.3662
0.2759
0.2992
Solyc11 - 15
0.8298
3.0000
0.7833
0.2825
0.2553
0.2426
Solyc11 - 16
0.7128
3.0000
0.7833
0.4095
0.3191
0.3256
Solyc11 - 17
0.7364
3.0000
0.9167
0.3883
0.3091
0.3129
Solyc11 - 19
0.7586
3.0000
0.9667
0.3662
0.2759
0.2992
Solyc11 - 21
0.7800
3.0000
0.8333
0.3432
0.2400
0.2843
Solyc02 - 1
0.5488
3.0000
0.6833
0.4952
0.3171
0.3726
Solyc02 - 2
0.9744
2.0000
0.6500
0.0500
0.0513
0.0487
Solyc11 - 2
0.9500
2.0000
0.6667
0.0950
0.1000
0.0905
Solyc11 - 4
0.9386
2.0000
0.9500
0.1153
0.1228
0.1086
Solyc11 - 5
0.9286
3.0000
0.9333
0.1327
0.1071
0.1239
Solyc11 - 6
0.8600
2.0000
0.8333
0.2408
0.2800
0.2118
Solyc11- 18
0.8191
2.0000
0.7833
0.2963
0.3617
0.2524
Solyc11 -20
0.8491
2.0000
0.8833
0.2563
0.3019
0.2235
Solyc11- 22
0.8426
2.0000
0.9000
0.2653
0.3148
0.2301
Mean
0.8188
2.6000
0.8113
0.2662
0.2401
0.2220
MAF = Major allele frequency, G = Genotype number, A
o
= Number of allele, He = Expected heterozygosity/gene diversity, Ho = Observed heterozygosity, PIC = Polymorphism information content (PIC).
Figure 3. Dendrogram constructed using Nei similarity coefficient and UPGMA Clustering for the F
3
tomato genotypes.
Figure 4. Each individual sample was represented by a single row broken into three-colored segments (red, green and blue), with length
proportions to each of the two inferred population subgroups. Each individual corresponded to the samples in the dendrogram.
Sokal, 1973) to describe their genetic relationship. The similarities
between the tomato progenies hybrids reflected in the 25 SNPs alleles
were estimated and grouped into four major groups (Figure 3). The first
cluster consists of tomato progenies with large fruit size, the mean
locule number per fruit greater than 5 and the fruit shape index of less
than 1.
The members of this clusters showed a direct relationship with a
Supersteak, one of the parents used in this work.
Cluster 2 comprised tomato progenies with locule number ranged from
2 to 3 and the fruit shape index around 1. The members of this clusters
showed a direct relationship with the advanced generation hybrid that
generated from wild tomato and roma VF. Cluster 3 comprised of tomato
hybrid with locule number ranged between 3 to 5 and fruit shape index
around 1. Apart from three major groups, a number of hybrids were
scattered and distributed across the clusters.
Population structure of the tomato progenies
Genotyping data generated using the 25 polymorphic SNP markers were
used for genetic structure analysis using the Bayesian clustering model
implemented in the structure software. DK was also calculated, and the
result showed that DK reached the maximal value when K = 3. The
model used indicated that K = 3 is the best number of sub-population
(hereafter referred to as Q = 3, providing support for the existence of
the three distinct clusters in our association panel. The analysis of these
data identified accessions into three subgroups as well, and the results
were very similar to those of the clustering results (Figure 4). The Q
matrix outputs of the three subpopulations were used for the
association analysis.
Discussion
SNP-based polymorphism and genetic diversity
Average Nei's gene diversity and Polymorphism Information Content
(PICs) values revealed by SNP markers in this study were 0.2662 and
0.2220, respectively. This level of genetic diversity is similar to the
report of Corrado et al. (2013) who also used SNP genotyping for the
genetic diversity and detected the gene diversity and PIC values of 0.215
and 0.177, respectively. On the other hand, most of the researches
involving SSR markers for genetic diversity detected high gene diversity
and PICs values (Maccaferri et al., 2003 and Moragues et al., 2007).
However, the relative lower genetic variation revealed by SNP markers is
expected. This is because SNP markers are mainly bi-allelic; and
therefore, the gene diversity and PICs cannot exceed 0.5 while the multi-
allelic markers such as SSR can approach the maximum of 1. Similarly,
Chen et al. (2009) and Todorovska et al. (2015) observed the overall
genetic variation of 19.16% and 23.2% respectively across 47 SSRs and
SNPs loci in 216 hybrids and elite breeding lines of tomato originating
from four breeding centres in China.
The number of alleles per locus in this study was 2 alleles, although this
value was expected due to the bi-allelic nature of the SNPs markers.
Benor et al. (2008) reported 4.3 alleles per locus and PIC value of 0.31 in
tomato varieties. He et al. (2003) identified 2.7 alleles per locus on
average and PIC value of 0.37 in the study of relationships among 17
varieties and two parental lines of tomato with 60 SSR markers. Limited
allelic variation was also observed in a study of tomato populations
consisting of a total of 216 genotypes from four breeding centres in
China using 12 SSRs and 35 SNPs markers.
The present study revealed the genetic diversity within the F
3
tomato
genotypes. The relative high polymorphism (61.7%) recorded in this
study for the fruit size characters was due to the occurrence of the null
allele's segregation. The genetic similarity estimated in this study
according to SNPs data was scaled up to 100%, thus suggesting the
potential of SNPs markers in discriminating among tomato genotypes of
close or distant genetic background.
Furthermore, it was reported that solanaceaus plants have a low
frequency of polymorphism among cultivars (Nunome et al., 2003 and
Stagel et al., 2008). It was also documented that cultivated tomatoes are
highly monophorphic at the molecular level, although they are
phenotypically very diverse (Labate and Roberts, 2002).
Population structure
A prerequisite for the association studies is a good estimation of the
true population structure. The result on the population structure was
highly similar to the neighbour-joining dendrogram and fruit
characteristics. Both neighbour-joining dendrogram and the population
structure segmented the tomato genotypes into three main groups. The
result validates the findings of Ruggieri et al. (2014) who also
segmented tomato genotypes into three major groups by using both
joining dendrogram and the population structure. The number of sub-
populations obtained in this study was also similar to the number of
clusters observed by Mazzucato et al. (2007) in 61 accessions of the
cultivated tomato. On the other hand, Ranc et al. (2012) detected only
two sub-populations for the genetic structure of 90 tomato accessions
using 20 SSR markers.
Materials and Methods
Plant materials and population development
The experimental materials comprised advanced hybrids raised from
inter-specific crosses between cultivated tomatoes (Roma VF and
Tropica) and the wild tomato relative,
Solanum pimpinefollium
(W x R, R
xW and W x T). The advanced hybrids were crossed with a large fruited
inbred tomato variety Supersteak (S) imported from the United States of
America (USA), Beef (Florida) (BF) and Plumb (Rio grande) (PR) varieties in
a modified three - way cross to produce F
1
hybrids (Figure 1). The
advanced hybrids served as the pollen parent while the Supersteak, Beef
and Plumb were the seed parents. The F
1
hybrids were selfed to produce
the F
2
populations as a segregating population.
The experiments were carried out in the Department of Crop Science
screenhouse, University of Nigeria, Nsukka, located in the derived
savannah zone (Latitude 0.6
o
52N, longitude 07
o
24E with an altitude of
447.26 m above sea level) in 2013 and 2014. The seeds were raised in
nursery boxes filled with sterilized soil, well cured poultry manure and
river sand mixed at a ratio of 3:2:1 by volume. The seedlings were
transplanted into polythene bags arranged in the screen house four
weeks after planting.
DNA extraction
Leaf tissue was used to extract total genomic DNA from parents
(advanced interspecific hybrid and supersteak) and the 94 F
2
populations
arising from the crosses. The extraction of DNA followed the modified
mini preparation protocol described by Doyle and Doyle (1990) with
minor revisions. The extraction was done in the Department of
Bioscience, International Institute of Tropical Agriculture (IITA), Ibadan,
Nigeria.
Single nucleotides polymorphism (SNPs) markers
Tomato genotypes were genotyped with 45 SNP markers (Supplementary
2). The SNPs markers were downloaded from the Tomato SNPs Database
(SolCAP tomato collection) (Supplementary 1). SNPs markers selection
and assay design were performed according to the procedures of Chao
et al. (2010). The SNPs were selected mainly from chromosomes that are
related with fruit size and shape (chromosomes 2, 3 and 11). A total of
250ng of genomic DNA per genotype was used for the Illumina SNP
genotyping at the Inqaba Biotech, Pretoria, South Africa using the
Sequenom Mass Array Iplex Platform following the manufacturer's
protocol (Gabriel et al., 2009).
Data analysis
Power Marker V3.25 software was used to estimate the allele frequency
of the entire SNP markers. QTL association mapping was done using
Trait Analysis by Association, Evolution and Linkage (TASSEL 3.0 version
software). The population structure was estimated with the model-based
(Bayesian) cluster software, STRUCTURE 2.33 version.
Conclusion
The genetic studies of the modified three ways cross tomato hybrids are
necessary for the stable selection of marketable tomato fruit size. The
SNP based analysis shows that a high level of genetic diversity exists
among the modified three-way cross hybrids and population structure
analysis reveals the occurrence of three different gene pools of F
2
tomato hybrids among the examined populations.The Single Nucleotides
Polymophisms (SNPs) markers analysis implicated mean fruit weight,
number of locules per fruit, fruit length, fruit diameter and fruit shape
index in chromosome 2 and 11 as important determinants of fruit size.
These traits were very evident in the determination of the fruit size and
yield in S x (W x R), which is the most promising three- way cross.
Acknowledgements
The authors would like to acknowledge the TRECCAFRICA scholarship
program for the PhD scholarship granted the corresponding author at
University of Nigeria, Nsukka. Also they wish to acknowledge the
University of Dar es Salaam for providing research funds for the present
study.
Data availability statements
The data that support the findings of this study are available from the
corresponding author, Nnungu, Stephen Issa upon request.
References
Atugwu A, Uguru MI (2012) Tracking fruit size increase in recombinant
obtained from an interspecific cross between cultivated tomato and wild
tomato relative. Journal of Plant Breeding and Crop Science. 4(4): 62 -
71.
AVRDC, (2006) Vegetables Matter. The World Vegetable Center. Shanhua,
Taiwan.
Benor S, Zhang M, Wang Z, Zhang H (2008) Genet Genomics. 35:373–
379. Available from:
http://dx.doi.org/10.1016/S1673-8527(08)60054-5.
Bouchet S, Pot D, Deu M, Rami J-F, Billot C, Perrier X, Rivallan R, Gardes
L, Xia L, Wenzl P (2012) Genetic structure, linkage disequilibrium and
signature of selection in sorghum: lessons from physically anchored
DArT markers. PLoS One. 7:3
Chao S, Zhang W, Akhunov E, Sherman J, Ma Y, Luo MC,Dubcovsky
J(2009) Analysis of gene-derived SNP marker polymorphism in US
wheat (
Triticum aestivum
L.) cultivars. Mol Breed
.
23:23 - 33.
Chen J, Wang H, Shen H, Chai M, Li J, Qi M, Yang W (2009) Scientia
Horticulturae. 122: 616-623. Available from:
http://dx.doi.org/10.1016/j.
scienta
.2009.03.025.
Cornelious BK, Sneller CH (2002) Yield and molecular diversity of
soybean lines derived from crosses of Northern and Southern elite
parents. Crop Sci. 42:642-647.
Frankha R, Ballou JD, Briscoe DA (2002) Introduction to conservation
genetics. Cambridge University Press, Cambridge, United Kingdom
Gabriel S, Ziaugra L, Tabbaa D (2009) SNP Genotyping Using the
Sequenom Mass ARRAY iPLEX Platform. Current Protocols in Human
Genetics. 60:1-18.
Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its
effect on haplotype diversity and linkage disequilibrium surrounding
the xa5 locus of rice (
Oryza sativa
L.). Genetics. 165:759–769.
Hamrick JL, Godt MJW (1996) Effect of life history traits on genetic
diversity in plant species. Phil Trans R Soc Lond B. 351:1291-1298.
He C, Poysa V, Yu U (2003) Development and characterization of simple
sequence repeat (SSR) marker and their use in determining
relationship among
Lycopersicon esculentum
cultivars. Theor Appl
Genet
.
106:363–373.
Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T,
Zhang Z (2010) Genome-wide association studies of 14 agronomic
traits in rice landraces. Nat Genet. 42(11):961–976.
Labate J, Roberts L (2002) Genetic variation in heirloom versus modern
tomato (
Lycopersicon esculentum
) cultivars. p. 27 In: Program for the
43rd Annual Meeting of the Society for Economic Botany, NY Botanical
Garden, NYC, NY.
Maccaferri M, Sanguineti M, Donini P, Tuberosa R (2003) Microsatellite
analysis reveals progressive widening of the genetic basis in the elite
durum wheat germplasm. Theor Appl Genet
.
107:783–797.
Mazzucato A, Papa R, Bitocchi E, Mosconi P, Nanni L, Negri V, Picarella
ME,Siligato F, Soressi GP, Tiranti B (2008) Genetic diversity, structure
andmarker-trait associations in a collection of Italian tomato (
Solanum
lycopersicum
L.) landraces. Theor Appl Genet. 116(5):657–669.
Moragues M, Moralejo M, Sorrells M, Royo C (2007) Dispersal of durum
wheat [
Triticum turgidum
L. ssp.
turgidum
convar.
durum
(Desf.)
MacKey] landraces across the Mediterraneanbasin assessed by AFLPs
and microsatellites. Genet. Resour. Crop Evol. 54: 1133–1144.
Nunome T, Suwabe, K, Iketani H, Hirai M(2003) Identification and
characterization of microsatellites in eggplant. Plant Breed. 122:256-
262.
Rafalski JA (2002) Novel genetic mapping tools in plant: SNPs and LD-
based approaches. Plant Sci. 162: 329–333.
Rana MK, Bhat KV (2004) A comparison of AFLP and RAPD markers for
genetic diversity and cultivar identification in cotton. J Plant Biochem
Biotech. 13: 19- 24
Ranc N, Muños S, Xu J, Le Paslier MC, Chauveau A, Bounon R, RollandS,
Bouchet JP, Brunel, D, Causse M (2012) Genome-wide association
mapping in tomato (Solanum lycopersicum) is possible using genome
admixture of
Solanum lycopersicum
var. cerasiforme. G3: Genes
Genomes Genet
.
2(8):853–864.
Ruggieri V, Francese G, Sacco A, D'Alesandro A, Rigano M, Parisi M,
Milone M, Cardi T, Mennella G, Barone A (2014) An association mapping
approach to identify favourable alleles for tomato fruit quality breeding.
BMC Plant Biology. 14:337.
Stàgel A, Portis E, Toppino L, Rotino G (2008) Gene-based microsatellite
development for mapping and phylogeny studies in eggplant. BMC
Genomics
.
9:1-14.
Todorovska E, Ivanova A, Ganeva D, Pericharova G, Molle E, BojinorB,
Rudkova M, Danoilov Z (2014) Assessment of genetic variation in
Bulgarian tomato (
Solanum lycopersicum
L.) genotypes using
fluorescent SSR genotyping platform. Biotechnology and
Biotechnological equipments
.
28 (1): 68 - 76.
Uguru MI, Igili D (2002) Field reactions of segregating population of
interspecific hybrid of lycopersicon species to natural infection of
Xanthomonas camprestris
vesicatria (Doidge) Dye. Nigeria Journal of
horticultural science. 6 (1): 5 - 11.
Varshney RK, Thiel T, Sretenovic-Rajicic T, Baum M, Valkoun J, Guo P,
Grando S, Ceccarelli S, Graner A (2008) Identification and validation of a
core set of informative genic SSR and SNP markers for assaying
functional diversity in barley. Mol Breed. 22:1–13
Xu JX, Ranc N, Munos S, Rolland S, Bouchet JP, Desplat N, Le Paslier MC,
Liang Y, Brunel D, Causse M (2013) Phenotypic diversity and association
mapping for fruit quality traits in cultivated tomato and related species.
Theor Appl Genet. 126(3):567–581.