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2 FiguresGenetic Map of Mango: A Tool for Mango Breeding
David N. Kuhn
Abstract
Mango (Mangifera indica) is an economically and nutritionally important tropical/subtropical tree fruit crop. Most of the current commercial cultivars are selections rather than the products of breeding programs. To improve the efficiency of mango breeding, molecular markers have been used to create a consensus genetic map that identifies all 20 linkage groups in seven mapping populations. Polyembryony is an important mango trait, used for clonal propagation of cultivars and rootstocks. In polyembryonic mango cultivars, in addition to a zygotic embryo, several apomictic embryos develop from maternal tissue surrounding the fertilized egg cell. This trait has been associated with linkage group 8 in our consensus genetic map and has been validated in two of the seven mapping populations. In addition, we have observed a significant association between trait and single nucleotide polymorphism (SNP) markers for the vegetative trait of branch habit and the fruit traits of bloom, ground skin color, blush intensity, beak shape, and pulp color.
Figures
ORIGINAL RESEARCH
published: 20 April 2017
doi: 10.3389/fpls.2017.00577
Frontiers in Plant Science | www.frontiersin.org 1April 2017 | Volume 8 | Article 577
Edited by:
Bernie Carroll,
The University of Queensland,
Australia
Reviewed by:
Zhukuan Cheng,
University of Chinese Academy of
Sciences, China
Roger Paul Hellens,
Queensland University of Technology,
Australia
*Correspondence:
David N. Kuhn
david.kuhn@ars.usda.gov
Specialty section:
This article was submitted to
Plant Genetics and Genomics,
a section of the journal
Frontiers in Plant Science
Received: 30 September 2016
Accepted: 30 March 2017
Published: 20 April 2017
Citation:
Kuhn DN, Bally ISE, Dillon NL,
Innes D, Groh AM, Rahaman J,
Ophir R, Cohen Y and Sherman A
(2017) Genetic Map of Mango: A Tool
for Mango Breeding.
Front. Plant Sci. 8:577.
doi: 10.3389/fpls.2017.00577
Genetic Map of Mango: A Tool for
Mango Breeding
David N. Kuhn 1*, Ian S. E. Bally 2, Natalie L. Dillon 2, David Innes 2, Amy M. Groh 3,
Jordon Rahaman 3, Ron Ophir 4, Yuval Cohen4and Amir Sherman 4
1Subtropical Horticulture Research Station, United States Department of Agriculture—Agriculture Research Service, Miami,
FL, USA, 2Department of Agriculture and Fisheries, Centre for Tropical Agriculture, Horticulture and Forestry Science,
Brisbane, QLD, Australia, 3International Center for Tropical Botany, Florida International University, Miami, FL, USA,
4Department of Fruit Tree Sciences, Plant Sciences Institute, Agriculture Research Organization, Rishon Letzion, Israel
Mango (Mangifera indica) is an economically and nutritionally important
tropical/subtropical tree fruit crop. Most of the current commercial cultivars are
selections rather than the products of breeding programs. To improve the efficiency of
mango breeding, molecular markers have been used to create a consensus genetic
map that identifies all 20 linkage groups in seven mapping populations. Polyembryony
is an important mango trait, used for clonal propagation of cultivars and rootstocks.
In polyembryonic mango cultivars, in addition to a zygotic embryo, several apomictic
embryos develop from maternal tissue surrounding the fertilized egg cell. This trait has
been associated with linkage group 8 in our consensus genetic map and has been
validated in two of the seven mapping populations. In addition, we have observed a
significant association between trait and single nucleotide polymorphism (SNP) markers
for the vegetative trait of branch habit and the fruit traits of bloom, ground skin color,
blush intensity, beak shape, and pulp color.
Keywords: genetic recombination map, Mangifera indica L., SNP marker, trait association, polyembryony
INTRODUCTION
Mango (Mangifera indica) is one of the most important fruit crops of the world due to its large
fruit with a soft, sweet pulp. A subtropical group in the Indian sub-continent is characterized
by monoembryonic seed and a tropical group in the south-east-Asia region is characterized by
polyembryonic seed (Mukherjee and Litz, 2009).
Mango has been widely cultivated in India and Southeast Asia for thousands of years. In the
fifteenth and sixteenth centuries, Portuguese and Spanish traders spread mango to other tropical
and subtropical regions of the world (Mukherjee and Litz, 2009). Early in the twentieth century,
cultivars from the Indian and Asian regions were combined in a new center of mango development
in Florida, where many cultivars were selected and disseminated. These cultivars, selected for
milder taste and aroma, colorful skin, and larger fruit size, are still the major cultivars used today
in international trade.
Mango is now grown throughout the sub-tropical and tropical world in 99 countries with a total
fruit production of 34.3 million tons of fruit per annum (Galán Saúco, 2013). The majority (76%)
of world production comes from Asia, with the Americas (12%), and Africa (11.8%) the second and
third largest producers. India is the largest producer, growing over 18 million tons (MT) primarily
for domestic consumption, followed by China (4.5 MT) Thailand (3.1 MT), Indonesia (2.6 MT),
and Mexico (1.9 MT) (Galán Saúco, 2013). Although, Mexico is fifth in production it is first in
export to the USA, which is 43% of the global import market.
Kuhn et al. Mango Genetic Map
Around the world there are hundreds and possibly thousands
of different mango cultivars and selections, most of which are
only grown and marketed locally. Relatively few cultivars are
traded internationally due to the highly specific requirements for
cultivars with favorable color, storage, and shipping traits.
Mango is suggested to have a partial allopolyploid genome
based on cytogenetics (Mukherjee, 1950). However, genetic
markers for mango have been reported to be inherited in a
disomic fashion by several authors (Duval et al., 2005; Schnell
et al., 2005, 2006; Viruel et al., 2005) suggesting that mango may
be treated as diploid. Mango has a total of 40 chromosomes,
which suggests a haploid number of chromosomes as 20 and
similarly 20 linkage groups. The haploid genome size is estimated
at ∼439 Mb (Arumuganathan and Earle, 1991).
To date the development of genetic and genomic resources
in mango have been limited and have not greatly contributed
to mango breeding around the world. An early, very limited
genetic map of mango produced by Kashkush et al. (2001) was
not sufficiently resolved to be useful for marker assisted selection
(MAS) or trait association to markers. Recently, a high resolution
map of mango has been produced by Luo et al. (2016) that may
prove more useful. Several transcriptomes from different mango
tissues have been produced (Pandit et al., 2010; Azim et al., 2014;
Luria et al., 2014; Wu et al., 2014; Dautt-Castro et al., 2015;
Sherman et al., 2015). In 2016, Kuhn et al. (2016) identified
∼400,000 single nucleotide polymorphism (SNP) markers using
a reference transcriptome from “Tommy Atkins” and sequences
of expressed mRNA from 17 genetically diverse cultivars. The
genetic diversity of mango has been explored by different
groups with a variety of markers, who all found a narrow
genetic basis among the commercial cultivars grown and traded
internationally (Schnell et al., 2006; Dillon et al., 2013; Sherman
et al., 2015). An increase in the number of unbiased markers
and a highly resolved genetic map are essential molecular tools
for mango breeders if the power of genomics is to drive future
progress of breeding for improved mango cultivars.
The current improved commercial cultivars have typically
been selected from open pollinated seedling progeny and then
vegetatively propagated to maintain genetic uniformity (Bally
et al., 2009). The continual demand for new and improved
cultivars with superior production and quality traits is a challenge
for breeders relying on traditional breeding techniques. Factors
that limit progress in traditional fruit tree breeding are the
long juvenile phase, long generation time, and large resource
requirements in field area and personnel for maintaining
and evaluating hybrid populations. In addition to these
restraints, mango breeders are faced with high heterozygosity,
polyembryony, low crossing rates (0.1%) from high numbers of
flowers per panicle, a very high level of fruitlet drop, and only a
single seed per flower resulting in a low number of fruit (0.1%
of flowers), all of which makes the task of active manual crosses
challenging (Bally et al., 2009). There is also little knowledge
of the heritability of most of the important horticultural traits
in mango (Schnell et al., 2006). Finally, the lack of genotypic
and phenotypic diversity among the current commercial cultivars
may reduce breeding efficiency if used as parents in breeding
programs. Adoption of molecular genomic tools has the potential
to estimate genetic diversity of potential parents, identify markers
associated with important horticultural traits and, in general,
improve the efficiency of mango breeding programs.
Major mango breeding/selection programs exist in India,
Australia, Brazil, and Israel, and although each program has
breeding goals specific for their industries, they share many
productivity and quality goals. Full-sib hybrid populations from
two known parents with differing horticultural traits, such as
hand pollinated populations, are more effective for breeding
progress than half-sib populations from open pollinated maternal
parents. Genetic maps that are based on segregating full-sib
hybrid populations are a powerful tool to identify linkage
between horticultural traits and molecular markers for MAS as
seen in other tree fruit crops (Ogundiwin et al., 2009; Martínez-
García et al., 2013; Harel-Beja et al., 2015).
Linking and mapping important mango traits with molecular
markers will improve the efficiency of mango breeding. One
of the traits of mango that is very distinct is polyembryony in
which multiple apomictic embryos develop from the maternal
nucellar tissues around the fertilized egg in addition to
a single zygotic embryo (Asker and Jerling, 1992). Most
mango cultivars originating in India are monoembryonic,
while cultivars originating from Southeastern Asia are usually
polyembryonic (Litz, 2009). Trees developing from the apomictic
embryos of polyembryonic mangos are genetically similar to
the maternal tree. This property provides an easy method of
clonal propagation, which may be used commercially to produce
uniform rootstocks in addition to allow commercial cultivars to
grow on their own roots. Such clonal rootstock can be well-
adapted to the local growing conditions and soils.
Although, polyembryony in mango was originally thought to
be controlled by recessive genes (Sturrock, 1968), later genetic
evidence suggested that polyembryony in mango is controlled
by a single dominant locus (Aron et al., 1998). Polyembryony
in citrus may be controlled by more than one gene as several
sequences (Nakano et al., 2012) and genes associated with
polyembryony have been identified (Nakano et al., 2013; Kumar
et al., 2014).
In this study, we generated a mango consensus genetic map,
a valuable tool that can be used to improve the efficiency and
overcome the challenges facing mango breeding programs. We
used the genetic map to identify markers and regions of the
genome that are associated with important horticultural traits
such as embryo type, branch habit, bloom, ground skin color,
blush intensity, beak shape, and pulp color.
MATERIALS AND METHODS
Mapping Populations
Seven mapping populations were used to make the consensus
map (Table 1). The four mapping populations from Australia
share a common paternal parent, Kensington Pride (KP). In
addition, the cultivar NMBP1243, the maternal parent of one
of the mapping populations, is a progeny of the Irwin (I)
×KP population. The Brazilian population Haden (H) ×
Tommy Atkins (TA) share both parents with the self-pollinated
populations of H and TA from the Subtropical Horticulture
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Kuhn et al. Mango Genetic Map
TABLE 1 | Number of progeny and the sources of seven hybrid mapping
populations used to create the consensus genetic map.
Population name Number of
individuals
Source of population
Tommy Atkins ×Tommy Atkins
(TA ×TA) (Self-pollinated)
60 USDA-ARS, SHRS, USAa
Tommy Atkins ×Kensington
Pride (TA ×KP)
100 DAFQ, Australiab
Haden ×Tommy Atkins (H ×TA) 225 Embrapa, Brazilc
Haden ×Haden (H ×H)
(Self-pollinated)
40 USDA-ARS, SHRS, USAa
Irwin ×Kensington Pride (I ×KP) 180 DAFQ, Australiab
NMBP1243 ×Kensington Pride
(NMBP1243 ×KP)
100 DAFQ, Australiab
Creeper ×Kensington Pride
(Cr ×KP)
70 DAFQ, Australiab
Populations were named maternal parent ×paternal parent.
aUnited States Department of Agriculture-Agricultural Research Service, Subtropical
Horticulture Research Station, United States of America.
bDepartment of Agriculture and Fisheries, Queensland, Australia.
cBrazilian Agricultural Research Corporation (Embrapa), Pernambuco, Brazil.
Research Station (SHRS). The TA self-pollinated population
was generated by germinating and genotyping fruit from a
commercial grove planted with only TA. The H self-pollinated
population was generated by germinating and genotyping fruit
from an isolated tree at SHRS.
SNP Containing Sequences
SNP containing sequences came from three different sources:
Department of Agriculture and Fisheries, Queensland (DAFQ),
Australia, SHRS, USA and the Agriculture Research Organization
(ARO), Israel (Table 2). The SHRS SNP markers were identified
as described in Kuhn et al. (2016). The ARO SNP markers were
identified as described in Sherman et al. (2015). The DAFQ SNP
markers were identified from sequence data described in Hoang
et al. (2015).
DNA Isolation
DNA for genotyping was isolated from the leaves of individual
progeny in the mapping populations as in Kuhn et al. (2016).
Once isolated the DNA was quantified by fluorescence on a
fluorescence plate reader (BioMark, Inc.) and normalized to
10 ng/uL on a liquid handling robot (Hamilton, Inc., Reno, NV,
USA).
SNP Assays
All 1,054 SNP assays were produced from SNP containing
sequences by Fluidigm (South San Francisco, CA, USA) and
assayed on a Fluidigm EP-1 platform.
Data Reformatting
Perl scripts (available on request) were written to reformat
data from all 1,054 markers generated by the Fluidigm EP-
1 platform. Data from all mapping populations for all 1,054
markers were appended into a single file. Due to the large size
of the combined data file, the initial analysis was performed
on a 32 core Linux cluster followed by data reformatting and
analyzing with scripts that produced csv files for export to Excel.
Off type individuals, i.e., not hybrid progeny of the parents
of the population, were identified by multiple occurrence of
genotypes that could not have been inherited from the parents
and were removed from the dataset. Markers with >5% missing
data were also removed from the dataset. In the resulting
edited dataset, individual progeny with >5% missing data were
then removed. SNP markers that were homozygous for both
parents in a population were removed because they would not
be informative for finding recombination events. Selection was
made for markers with disomic inheritance segregation ratios.
SNP markers with segregation ratios differing by more than
20% from the expected disomic genotypic frequency or allelic
frequency were removed from the dataset. Such markers had
either aberrant segregation ratios based on the parental genotypes
or segregation ratios indicative of tetraploid inheritance.
Genetic Mapping
Two mapping programs, JoinMap4 (Kyazma B.V. R
,
Wageningen, Netherlands) and OneMap (Margarido et al.,
2007) were used to create genetic maps for each of the seven
mapping populations (Table 1). Each program has advantages
and they were used in conjunction as follows. OneMap was
used to identify 20 groups because it could be run recursively to
identify a predetermined number of groups. OneMap was run
individually for all seven mapping populations with recursive
runs that increased the acceptable likelihood of the odds (LOD)
threshold (increasing by increments of 0.1) until 20 linkage
groups (LGs) were achieved with a minimum of 10 markers per
LG.
The TA ×KP population analysis in OneMap produced a
map with the most markers per LG (480 markers total were
grouped with at least 20 per LG). These individual LGs were
used to force the initial marker grouping in JoinMap4. All
calculations in JoinMap4 were conducted with default parameter
settings for the population, grouping, and Maximum Likelihood
(ML) mapping. JoinMap4 has a function that allows ungrouped
markers to be added to groups based on an association score,
the Strongest Cross Link value (SCL value). Any marker with an
SCL value ≥5.0 was added to its SCL group. This was repeated
until no markers had SCL values >5.0. Loci that were marked
as identical to another locus were also included in groups.
Markers were removed from linkage groups if they prevented
mapping in JoinMap4 or if they were >200 cM distance from
the next closest marker in the group. The most informative map
was from the TA ×KP population. This map was then used
in JoinMap4 to provide a starting point for the maps in the
other populations which were eventually merged using the map
integration functions in JoinMap4 to produce the consensus map.
The resulting TA ×KP map contained 600 markers and was
used to force the grouping of another population, H ×TA. More
markers were added to the H ×TA groups based on SCL values
and identity with other markers. Markers were again removed
if they prevented mapping or caused the linkage map to be an
unreasonable size, such as 5,000 cM. The TA ×KP map was
integrated with the resulting H ×TA map and this integrated
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Kuhn et al. Mango Genetic Map
TABLE 2 | Source of SNP assays used in the construction of the
consensus genetic map for mango.
SNP assay Number of SNPs Contributors and citations
Australia 144 DAFQ Hoang et al., 2015
Israel 384 ARO Sherman et al., 2015
US 526 USDA-ARS SHRS Kuhn et al., 2016
Total 1,054 –
map was used to force grouping in the next population. This
procedure was repeated for every population using the newly
integrated maps as a starting point for the forced grouping. The
order of grouping and population integration into the map was
as follows, TA ×KP, H ×TA, TA Selfs, I ×KP, NMBP1243
×KP, Creeper (Cr) ×KP, Haden Selfs. After each population
was integrated into the map once, TA ×KP and H ×TA were
grouped and integrated for a second time to see if the larger
integrated maps could bring in more associated markers and
reduce the total length of the maps of each linkage group.
Trait Association
Phenotype data for 14 qualitative traits were available for TA
×KP, Cr ×KP, and I ×KP populations. In all cases KP
was the pollen donor as it is polyembryonic. The qualitative
traits measured were: stage of fruit ripeness, fruit shape, ground
skin color, blush color, blush intensity, bloom, stem end shape,
cleavage, beak shape, pulp color, embryo type, flavor, branch
habit, tree vigor, beak shape, and cleavage (Table 3). Embryo
type was measured by visual inspection of the seed without
seed coat from the F1mapping population parent (Aron et al.,
1998).
Of the 14 traits, the twelve fruit traits were assessed on a
sample of ten randomly picked at fruit maturity from each
individual genotype within the three mapping populations. Fruit
were ripened at 26◦C and assessed at the eating ripe stage using
the criteria detailed in Table 3.
Associating traits with the mapped SNP markers was done
using MapQTL6 (Kyazma B.V. R
, Wageningen, Netherlands)
using Cross Pollinated (CP) for population type and Interval
Mapping (IM) for association statistic. All calculation parameters
were set to MapQTL6 defaults. Global thresholds were calculated
as described in MapQTL6 (permutation tests of 10,000
rounds) and only traits that showed higher association
probabilities than the global threshold were considered to be
significant.
RESULTS
Segregation of SNP Markers in the Seven
Mapping Populations
Markers were chosen that segregated in a disomic fashion
to produce our genetic map. From the 1,054 SNP markers
used to genotype the 775 individuals from the seven mapping
populations, 56 were removed due to excess missing data, 25
were removed due to aberrant segregation patterns, 19 had
two homozygous parents, and 66 were unmappable across all
TABLE 3 | Fourteen phenotypic traits and their assessment criteria used
for trait association in three mapping populations (TA ×KP, Cr ×KP, and
I×KP).
Trait Rating Score description
Stage of ripeness 0 Hard (no give in fruit)
1 Rubbery (slight give in fruit under strong
thumb pressure)
2 Sprung (flesh deforms by 2–3 mm with
moderate thumb pressure)
3 Firm soft (whole fruit deforms with
moderate hand pressure)
4 Eating soft (whole fruit deforms with soft
hand pressure)
Fruit shape 1 Long
2 Ovate
3 Round
Ground skin color 1 Green
2 Green/yellow
3 Yellow
4 Orange
5 Pink
Blush color 1 Orange
2 Pink
3 Red
4 Burgundy
Blush intensity 1 No blush
2 Blush barely visible
3 Slight blush (similar to Kensington Pride)
4 Medium blush (similar to Haden)
5 Solid blush (similar to Tommy Atkins)
Bloom (the efflorescence of the
wax covering the fruit)
1 Heavy
2 Light
Stem end shape 1 Deep
2 Slightly depressed
3 Level
4 Slightly raised
5 Pointed
Pulp colora1 Orange group 24A
2 Yellow orange group 32A
3 Yellow group 15A
4 Yellow group 13B
5 Yellow group 6A
Embryo type 1 Monoembryonic
2 Polyembryonic
Flavor 1 Unacceptable
2 Floridian
3 Indian
4 Other
(Continued)
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Kuhn et al. Mango Genetic Map
TABLE 3 | Continued
Trait Rating Score description
5 Kensington Pride
6 South East Asian
Branch habit 1 Upright
2 Spreading
3 Intermediate
Tree vigor 1 Extreme dwarf
2 Dwarf
3 Low vigor
4 Medium vigor
5 High vigor
Beak shape (prominence of the
point at the stylar scar)
1 Absent
2 Very slight
3 Slight
4 Medium
5 Prominent
Cleavage (severity of the groove
on the ventral shoulder of the
fruit)
1 Deep
2 Shallow
3 Absent
aThe_Royal_Horticultural_Society, 2001.
populations for a combination of these reasons such as missing
data in one mapping population and aberrant segregation in
another, leaving 888 potentially mappable markers (Table 4). As
the seven mapping populations had different parents, different
sets of markers were mappable within different populations.
To merge individual maps into a consensus map required the
removal of certain markers that did not appear to be stably
inherited in the same position or order in all the mapping
populations. In general, these markers were heterozygous in
both parents and distant from markers that were heterozygous
in only one parent so that correct phasing of the markers
in each population was difficult. Thus, although addition of
map data from populations with different parents increased the
number of markers in the consensus map, it also could lead
to the removal of markers that could not be phased correctly.
Examples of markers with aberrant segregation patterns for
disomic inheritance in different populations are listed in
Table 5.
Consensus Genetic Map
To include all markers in the consensus map, we employed
the strategy detailed in Section Materials and Methods, using
the strengths of both JoinMap4 and OneMap. We produced a
consensus map with 726 SNP markers distributed across 20 LGs
shown in Figure 1. A text version of SNP markers, linkage group
and map positions is provided in Table S1. Sequences for the
SNP markers, map positions, and annotation, where possible, are
presented in Table S2 and Fluidigm assay designs are in Table S3.
TABLE 4 | Types of markers removed prior to genetic mapping.
Type of marker Number of
markers
Total markers 1,054
Aberrant segregation types in all populations −25
Homozygote ×Homozygote in all populations −19
Too much missing data in all populations −56
Unmappable in all populations because of a combination of
unmappable marker types (e.g., aberrant segregation in one
population, missing data in one population, etc.)
−66
Final mappable markers in at least one population 888
TABLE 5 | Examples of aberrant segregation types for SNP markers in a
mapping population.
Population Marker Segregation ratio
(XX:XY:YY:ZZ)
H×TA Mi_0299 60:26:63:76
TA ×KP Mi_0020 57:0:43:3
Mi_0171 50:1:49:3
TA Self pollinated Contig 1638_A98G 0:66:0:0
Mi_0103 50:0:16:0
I×KP Mi_0200 121:3:52:3
NMBP1243 ×KP Mi_0425 72:4:23:1
Contig 6698_C90T 16:52:32:0
Markers exhibited aberrant segregation types in one or more populations and were
removed from further analysis. Only three genotypes are distinguishable using SNP
assays: Homozygous allele 1 (XX), heterozygous (XY), and homozygous allele 2 (YY). If
alleles are inherited as in a diploid, expected segregation ratios dependent on possible
parental genotypes are: 1:1 XX:XY, 1:2:1 XX:XY:YY, and 1:1 XY:YY. In the aberrant
segregation patterns, ZZ represents either a potential null allele or missing data.
Table 6 shows the calculated length in centimorgans (cM) and
the number of markers for each of the 20 LGs. Linkage group 8
was the longest at 247.8 cM and LG 16 had the greatest number
of markers at 71. Average distance between markers for each LG
is also shown in Table 6 and the overall average distance between
markers was 4.095 cM. Greatest distance between markers was
44.775 cM on LG 13 and shortest distance was 0.001 cM on LG
8 and 13 not including identical markers (0.000 cM distance).
Although, SNP markers had been designed so that there was
only one marker per transcript/gene, several SNP markers were
mapped to the identical position in all mapping populations
suggesting that the 775 meiotic events across all the populations
were not sufficient to observe recombination between these
genes.
Assuming a haploid genome size of ∼439 Mb and 20
chromosomes per haploid genome, the average size of a
chromosome would be ∼22 Mb. The total size of the map is 2,890
cM. An estimate of the average size of a cM would be ∼150 Kb
but would be expected to vary greatly within the genome.
Associating Qualitative Traits with the Map
Qualitative phenotypic data were available for three of the
mapping populations (TA ×KP, I ×KP, and Cr ×KP). Interval
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Kuhn et al. Mango Genetic Map
FIGURE 1 | The consensus genetic map of mango. Vertical lines represent linkage groups. Horizontal lines crossing the vertical lines depict the name and position
in cM of SNP markers on the linkage group.
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Kuhn et al. Mango Genetic Map
TABLE 6 | Consensus map statistics.
LG Number of
markers per
linkage
group
Length of
each
linkage
group (cM)
Ave
distance
between
markers
(cM)
Max
distance
between
markers
(cM)
Min distance
between
markers
(cM)
1 28 111.2 4.1 14.6 0.06
2 31 135.6 4.5 22.8 0.05
3 26 79.4 3.2 19.8 0.08
4 36 223.2 6.4 41.6 0.07
5 31 126.3 4.2 19.4 0.18
6 25 80.4 3.4 17.4 0.17
7 29 151.1 5.4 25.0 0.00
8 42 247.8 6.0 32.9 0.00
9 35 143.1 4.2 25.7 0.01
10 42 186.5 4.5 28.8 0.00
11 26 77.2 3.1 14.4 0.00
12 35 148.8 4.4 26.1 0.00
13 43 154.9 3.7 44.8 0.00
14 27 114.9 4.4 22.6 0.02
15 45 166.2 3.8 18.0 0.00
16 71 228.0 3.3 17.9 0.00
17 56 156.7 2.8 26.7 0.00
18 21 76.5 3.8 21.6 0.00
19 34 126.7 3.8 20.5 0.00
20 43 156.1 3.7 20.1 0.02
Total 726 2890.6
Summary of the final consensus linkage map containing 726 markers across 20 linkage
groups. For markers in a linkage group, the minimum number was 21, the maximum
number was 71, and the average was 36. For length in cM of a linkage group, the minimum
was 76.5 cM, the maximum was 247.8cM, and the average was 144.5 cM.
mapping testing using MapQTL found seven of the 14 qualitative
traits used in the association study had significant LOD scores
in at least one of the populations. Table 7 shows the seven
qualitative traits with significant LOD scores and their position
on the map associated with the trait. Reported LOD scores are
all above the thresholds determined by permutation tests for the
trait in the respective population.
Embryo type was the only trait to have significant LOD scores
at the same marker (Mi_0173) across two different populations
(Figure 2). Marker Mi_0173 was unable to be mapped in the I ×
KP population, which prevented testing for a significant signal
for embryo type in that population. For trait association, only
genotype data from mapped markers in the population were
used to ensure that the phasing specific to the population was
correct.
Bloom, pulp color, and branch habit traits showed significant
association to markers in two different populations. The marker
association was on different LGs in each population (Table 7).
For example, the bloom trait showed a significant association to a
marker on LG 9 in I ×KP and on LG 13 in TA ×KP (Figure 3).
The ground skin color, blush intensity, and beak shape traits
showed a significant association to markers on a single LG in only
one population (Table 7).
DISCUSSION
A Genetic Map of Mango from SNP
Markers
MAS provides a means to improve the efficiency of tree breeding.
A genetic map provides a means to improve the strength of the
association between traits and markers for MAS. We chose to
produce a genetic map from SNP markers for several reasons:
SNP markers are more abundant than microsatellite markers,
easier to identify, easier to score and, as unambiguous markers,
are appropriate for international databases as they show no
platform bias, which means they can be assayed by any method
and produce the same genotype. For mango, ∼500,000 SNP
markers were identified from RNA sequencing and alignment to
a consensus transcriptome (Hoang et al., 2015; Sherman et al.,
2015; Kuhn et al., 2016). From these SNPs, 1,054 were selected,
converted into assays and used to genotype seven different extant
mapping populations of mango comprising 775 individuals. Of
the 1,054 SNP markers, 726 segregated in a disomic (Mendelian)
fashion, showed normal segregation ratios in at least one of
the mapping populations, and could be placed on the genetic
map. We also found markers whose segregation could best be
explained with a tetrasomic inheritance model, which provides
evidence for at least a partial allopolyploid nature of mango.
Some markers had aberrant segregation patterns that could not
be explained by either a diploid or polyploid model. Not all the
markers that showed disomic segregation were able to be assigned
to a linkage group. This occurred most frequently when both
parents were heterozygous for the marker. In a diploid, when
both parents are heterozygous, the phase of the marker must be
determined by relating it to the inheritance of the nearest markers
where only one parent is heterozygous. In essence, the haplotypes
of the parental chromosome pairs are being inferred. However,
in a polyploid, there are many more potential combinations
of parental haplotypes and, thus, the phase of each haplotype
may not be correctly identified. In this situation, the position
of the marker on the map may vary dramatically from one
population to the next and the marker may also cause significant
distortion of the map. In such cases, the marker was removed
from the consensus map, unless, in at least one of the mapping
populations, only one of the parents was heterozygous for the
marker and phase calculation was unnecessary.
Mango has 40 chromosomes with the diploid number being
20. The markers we used for the map were inherited in a
disomic fashion, leading to an expectation that we would
find 20 identifiable LGs. This suggests that if mango is an
allopolyploid, the two ancestral genomes are different enough to
be distinguished by our markers.
We used a strategy to make the map that took advantage
of the strengths of two different mapping programs, JoinMap4
and OneMap. Using OneMap we set the group size and group
number parameters to artificially identify 20 LGs with at least
10 markers per LG. We then used these groups to force group
formation using JoinMap4 and to identify a SCL value of markers
that were not in the group identified by OneMap. Groups were
expanded by setting a minimum SCL value for inclusion into
the group and recursively applying this rule until all possible
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Kuhn et al. Mango Genetic Map
TABLE 7 | Trait association in three mapping populations.
Trait LG Marker Position (cM) TA ×KP LOD Cr ×KP LOD I ×KP LOD
Embryo type 8 Mi_0173 46.1 4.96 8.82
8 mango_rep_c6716 74.8 7.70
8 Contig1936 78.3 7.40
8 mango_rep_c886 80.2 7.23
8 Mi_0102 85.3 6.65
Ground skin color 17 Mi_0135 0.0 5.61
17 SSKP009C1_A627T 0.1 5.61
20 Mi_0450 19.2 4.62
20 Mi_0145 30.8 5.83
20 mango_rep_c4542 33.9 6.17
Blush intensity 20 Mi_0341 45.6 6.65
20 SSKP003C1_C682T 57.6 5.99
20 Mi_0343 67.5 5.75
20 Mi_0277 68.6 5.69
20 mango_rep_c15051 69.6 5.62
20 mango_rep_c8905 70.4 5.60
20 Mi_0357 71.1 5.57
20 Mi_0330 72.4 5.49
20 Mi_0046 73.1 5.43
20 Contig2601 74.0 5.33
Bloom 13 Contig1142 0.4 5.80
9 Mi_0417 109.2 4.86
9 Mi_0402 122.4 8.05
9 mango_rep_c9549 124.5 7.91
9 Mi_0142 128.8 7.14
9 Mi_0497 129.6 7.03
Beak shape 11 mango_c48384 17.7 6.16
11 mango_rep_c52196 17.8 6.16
Pulp color 16 Mi_0217 125.8 5.18
13 Mi_0029 5.6 4.36
Branch habit 8 Mi_0192 29.6 4.90
16 Contig3904 97.5 4.48
16 Contig1327 100.4 4.42
LG, linkage group; TA ×KP, Tommy Atkins ×Kensington Pride; Cr ×KP, Creeper ×Kensington Pride; I ×KP, Irwin ×Kensington Pride; LOD, likelihood of the odds.
markers with an SCL value over a set threshold had been included
in the group. At that point, the larger JoinMap group was used
to force group formation in the next mapping population until
all possible markers were included in the group. We started
this process in OneMap with the TA ×KP population as the
data for this population showed the least segregation distortion,
likely due to the accuracy of the parental genotypes. Using either
hand-pollination or open-pollination to create a population
of F1 hybrid individuals, the assumption is that all clones of
a cultivar that are potential parents have identical genotypes.
Thus, there should be no problem with using multiple trees
of a cultivar as a parent, rather than a single tree. However,
in both hand-pollinated and open-pollinated populations, there
may be genotypic differences in the multiple trees used as parents.
These slight genotypic differences may not be easily detectable
when using a few diagnostic markers, but may be detected
when more markers are applied or when segregation distortion
in that population for some markers is observed. The TA ×
KP population had the least amount of this type of distortion,
perhaps due to the genetic identity of all the TA and KP clones
used as parents. In contrast, the I ×KP population, although
almost twice as large as the TA ×KP population (180:100), had
off types identified when all 1,054 markers were used as well
as significant distortion that may have been due to the use of
several Irwin maternal parents that were not completely identical
in genotype. The I ×KP map had many fewer mapped markers
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Kuhn et al. Mango Genetic Map
FIGURE 2 | Graphs of the plot of the likelihood of the odds that a SNP marker is associated with the trait of polyembryony. (A) Linkage group 8 of the Cr
×KP map. (B) Linkage group 8 of the TA ×KP map.
FIGURE 3 | Graphs of the plot of the likelihood of the odds that a SNP marker is associated with the trait of bloom. (A) Linkage group 9 of the I ×KP map.
(B) Linkage group 13 of the TA ×KP map.
than the TA ×KP map and did not contribute new markers to
the consensus map that were unique to I ×KP.
Qualitative Trait Association to the Genetic
Map
To be useful for MAS, important agronomic traits must be
associated with markers. A map is not necessary to identify
markers associated with a trait, but confidence in this association
increases as multiple markers near the trait locus on the genetic
map also show significant association with the trait. This was the
case for seven of 14 of our qualitative traits used for the initial
trait association studies.
Polyembryony
Mango has its origins in Southeast Asia, primarily in the
area from north-western Myanmar, Bangladesh, and north-
eastern India. From these origins, two centers of diversity
developed. A subtropical group in the Indian sub-continent
that is characterized by monoembryonic seed and a tropical
group in the south-east-Asia region that is characterized by
polyembryonic seed (Mukherjee and Litz, 2009).
In our case, embryony type, which is dimorphic
(monoembryonic or polyembryonic) showed significant
association to a single locus on LG 8 in two of the three mapping
populations (Table 7). In crosses between a monoembryonic
maternal parent (I, TA, or Cr) and a polyembryonic paternal
parent (KP), polyembryony segregated 1:1. One possible
explanation for this segregation pattern proposed by Aron et al.
(1998) is that the gene regulating polyembryony is heterozygous
with a dominant polyembryony allele. Monoembryonic
individuals are homozygous recessive. The marker Mi_0173
(LG 8) shows a significant association with the polyembryony
trait in both TA ×KP and Cr ×KP. This is expected as the
dominant allele is coming from the same polyembryonic parent
(KP). No marker association with polyembryony was seen in I
×KP. This may have been due to the inability to map Mi_0173
in the I ×KP mapping population as discussed above. In
preliminary use of Mi_0173 to screen a germplasm collection,
significant association of this marker to the polyembryony trait
was also observed (data not shown), suggesting that the position
of the trait on LG 8 is not specific to the polyembryonic KP
parent common to four of the mapping populations. Our trait
association data supports Aron’s model of the genetic regulation
of polyembryony. The parents of the mapping populations in
this study do not adequately represent the genetic diversity of
either mono- or polyembryonic cultivars available in germplasm
collections. Further dissection of the polyembryony trait in
crosses between more genetically diverse cultivars of different
origins will increase our understanding of the genetics of this
important trait.
Other Horticultural Traits
We saw significant associations of six other traits to specific loci
on the genetic map: bloom, pulp color, branch habit, ground
skin color, blush intensity, and beak shape. Bloom, pulp color,
and branch habit showed association to markers in two different
mapping populations (TA ×KP, I ×KP), but on different linkage
groups in each. These traits may be regulated differently in the
Frontiers in Plant Science | www.frontiersin.org 9April 2017 | Volume 8 | Article 577
Kuhn et al. Mango Genetic Map
different accessions. For example, the bloom trait is the amount
of wax efflorescence covering the fruit and it was scored as light
(I and KP) and heavy (TA). A potential explanation would be
that the heavy phenotype for bloom in TA requires activation
of wax biosynthetic genes to increase wax production, while the
light phenotype in I and KP activates other pathways that use the
same long chain fatty acid precursors and reduce wax production.
A similar argument can be made for the pulp color and branch
habit traits, which also show association to different loci and LGs
in different mapping populations.
Significant association of SNP markers with blush intensity,
beak shape, and ground skin color was only observed in TA ×
KP. For blush intensity, the TA and I parents are scored as a 5,
KP is an intermediate 3, and Cr is 1. For beak shape, TA, KP, and
I are scored as 4 and Cr as 2. One might expect that the blush
trait should map in both TA ×KP and I ×KP and beak shape
should map only in Cr ×KP. Our results suggest that these traits
are regulated in a more complex manner. For ground skin color,
the two markers strongly associated with this trait in TA ×KP are
found at 0 cM and 0.1 cM on LG 17. The next mapped marker is
more than 26 cM distant. These two markers only mapped in TA
×KP and thus this region of the linkage group cannot be seen in
the other populations.
Allopolyploidy?
We observed segregation patterns of markers that fit more
closely to tetrasomic inheritance. For example, in the NMBP1243
×KP population, Mi_0055 showed a segregation pattern of
0:25:75:0 (Homozygous Allele1: Heterozygous: Homozygous
Allele2: Missing data or null allele). No parental combination of
genotypes for diploid parents could produce such a segregation
pattern, but as tetraploid parents, XYYY ×YYYY, where X is
Allele 1 and Y is Allele 2, the expected segregation would be
0:1:3:0, which fits closely with the observed ratio.
Using the Map for Breeding
We have produced a mango consensus genetic map based
on individual maps from seven F1 hybrid populations. The
individual maps showed strong agreement which makes the
consensus map a powerful tool for comparative mapping and
the association of markers and alleles to important horticultural
traits. Desirable parents can be selected from germplasm
collections based on the presence of favorable alleles for the
desired trait and used in either hand-pollination crosses or open-
pollination of the maternal parent to increase the efficiency of
selection of improved material. The trait-associated SNP markers
described here can be used to select progeny containing these
favorable alleles by genotyping, which is now reliable, rapid, and
inexpensive. Genotyping for these traits at the seedling stage will
significantly reduce the expense in field use, maintenance and
evaluation of material over years. The map opens the way for
MAS in mango breeding.
MAS is an excellent tool for preselection of seedlings
more likely to show improved traits, but in many fruit tree
crops the required genetic resources are not available. The
set of markers and genetic map we developed are valuable
resources for mango breeders, helping them identify accessions
as potential parents and validate progeny as hybrids. The
markers and map are a significant step toward improving the
efficiency of both traditional breeding and selection through
early identification of progeny with trait- and allele-associated
genotypes.
The consensus map and qualitative trait-associated markers
presented here are the first for mango and demonstrate the utility
of such genomics tools for breeding and selection of improved
mango cultivars. However, markers associated with important
quantitative traits are also needed to further improve mango
breeding efficiency. Recently, we have begun a project to produce
a map of the TA ×KP population by genotyping by sequencing
(GBS). The GBS map should be based on more than 100,000
SNP markers and provide the appropriate resolution for the
association of quantitative traits to SNP markers for the TA
×KP population and, by extension, to other mango hybrid
populations with sufficient amounts of accurate phenotypic
data.
AUTHOR CONTRIBUTIONS
DK, IB, ND—mango mapping populations; DK, DI, AS,
RO, YC—SNP markers; DK, AG, JR—data reformatting and
mapping; DK, IB, ND, DI, AG, JR, RO, YC, AS—conception and
design of the work, drafting, and revising the manuscript.
FUNDING
DK, AG, JR were funded by USDA-ARS CRIS #6631-21000-022-
00D and the National Mango Board NACA#58-6038-5-001. AS,
RO were funded by MOAG Chief scientist grant 203-859. YC
was funded by MOAG Chief scientist grant 203-088. ND, IB
were funded by QDAF, Australia, #HF10189 and Horticulture
Innovation Australia (HIA) #MG12015.
ACKNOWLEDGMENTS
Thanks to Elaini Oliveira dos Santos Alves (UESC, Bahia, Brazil),
Carlos Antonio Fernandes Santos, and Francisco Pinheiro Lima
Neto (Embrapa Semiarido, Petrolina, Pernambuco, Brazil) for
sharing the H ×TA mapping population. Thanks to Ashley
Johnson, Paola Sanchez, and Barbie Freeman (USDA-ARS-
SHRS, USA) for outstanding effort in genotyping all the mapping
populations. Special thanks to Leo Ortega and the National
Mango Board (USA) for their exceptional support in funding
and encouraging this research. We acknowledge the assistance of
Cheryldene Maddox (QDAF, Australia) with the maintenance of
the mango genepool collection and phenotypic data collection,
and Louise Hucks (QDAF, Australia) for laboratory technical
assistance.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: http://journal.frontiersin.org/article/10.3389/fpls.2017.
00577/full#supplementary-material
Frontiers in Plant Science | www.frontiersin.org 10 April 2017 | Volume 8 | Article 577
Kuhn et al. Mango Genetic Map
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
Copyright © 2017 Kuhn, Bally, Dillon, Innes, Groh, Rahaman, Ophir, Cohen and
Sherman. This is an open-access article distributed under the terms of the Creative
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and that the original publication in this journal is cited, in accordance with accepted
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