Introduction
The genus Brassica includes
different vegetables and oil crops that are grown in different countries.
Chinese kale (Brassica oleracea var. Alboglabra)
was originated in Southern China. This vegetable was cultivated on nearly 50000
ha in Guangdong Province of China during 2014 (Li et al. 2015).
Commonly, three to four crops of Chinese kale are produced in a single year.
Along with the domestic consumption, Chinese kale is also exported to Asia,
Europe and USA.
Bolting (BT) and flowering (FT) time are important
agronomic traits of crop quality, production (Zhang et
al. 2018). Understanding genetic mechanisms governing bolting
and flowering time is an essential factor in plant breeding (Oded et al. 2014). Plant
flowering is a series of developmental events. Budding and bolting mainly
controls flowering time (FT) of plants. Several genes control FT trait that is
an important determinant for the evolution and domestication. Genes controlling
FT trait have been explored in Arabidopsis
thaliana (Koornneef et al. 1998).
Nearly 80 genes have been shown to control the flowering process either by
direct or indirect mechanisms (Levy and Dean
1998). During the entire growth period of Chinese kale, BT and FT traits
directly influence the time of harvest, yield and quality.
Genetic map and QTL analysis are important
approaches for marker assisted breeding of plants. High-density genetic map is
an essential resource for mapping of the phenotypic traits of interest (Liu et
al. 2016a, b). Next-generation sequencing techniques have leveraged the
advantages of molecular markers. SLAF sequencing, when assisted by
next-generation sequencing technologies, is a useful strategy for discovering
single nucleotide polymorphisms (SNPs) (Li et al. 2019). SLAF-seq has
significantly improved the resolution of QTL mapping in numerous
crops by large-scale SNPs discovery (Sunet
al. 2013b). Previously, different QTLs controlling flowering time in
B. oleracea have been identified using genetic linkage maps developed by
crossing the members of different sub-species and old molecular markers such as
restriction fragment length polymorphisms (RFLP), amplified fragment length
polymorphisms (AFLP) and simple sequence repeats (SSR) (Li et al. 2015;
Honghao et al. 2016; Rahman et al. 2018). These maps cannot serve
effectively for molecular assisted selection of traits for breeding Chinese
kale as these were of low genetic density. Hence, there is a need to develop a
high-density genetic linkage map that can be used to find loci governing BT and
FT traits in Chines kale plants. The availability of a high-density genetic map
of Chinese kale along with the presence of reference genome of Arabidopsis can
further assist in the identification of novel genetic resources controlling the
flowering time trait of Chinese kale.
Keeping in view the importance of high-density
genetic resources, it deems necessary to build a genetic map of relatively high
density to perform QTL mapping of flowering traits of Chinese kale. Hence, this
study was carried out to identify the loci controlling BT and FT traits in
Chinese kale plants, construction of a high density genetic map and candidate
gene analysis.
Materials and Methods
Mapping population
An F2 population was raised by crossing ‘Dasun’ and ‘LB07M’
lines of Chinese kale. The line ‘Dasun’ has long bolting (BT) and flowering
(FT) times and was the male in the cross. ‘LB07M’ has BT and FT and acted as
female during cross. An F2 population consisting on 159 lines was
consisted derived from single seed.
Phenotypic evaluation of flowering
and bolting time
The two parents (30 plants of each), F1 (30 plants) and the F2
plants were sown on 26 September of 2018 year in the field at Research station
of Guangdong Academy of Agricultural Sciences, Guangzhou (25.1N, 115.0E),
China. The soil at the research station is a sandy loam with adequate
fertility. Field layout consisted of two-row plots, 20 (L) × 25 (W) cm, with
planting following a randomized block design. The flowering and bolting times were
evaluated using the values of each line and parent. Two rows were planted in
each plot for avoidance of errors caused by the border effects. BT was noted as
the day when the main flower stalk had grown to 1.0 cm. FT was noted when the first
flower was fully opened.
DNA extraction
Young leaves from F2 individuals and two parental lines were
collected. For SLAF library construction, DNA was extracted using a Sangon Dzup
plant DNA extraction kit following the provided instructions. DNA quality was assessed
by standard electrophoresis method.
SLAF library construction and data
analysis
SLAF sequencing was performed in accordance to the methodology proposed by
Sun et al. (2013a). Briefly,
preliminary studies were performed to select suitable restriction enzymes for
the production of restriction fragments and high-quality SLAFs. Different
restriction enzymes were screened in a pilot study and finally the genomic DNA
of Chinese kale was digested with “HaeIII” and “Hpy166II” enzymes. Afterwards,
a single nucleotide overhung was joined with the obtained fragments and duplex
tag-labeled sequencing adaptors were ligated with “A-tailed” fragments. SLAFs
(DNA fragments) of 400 to 500 bp were separated and sequenced on an Illumina
HiSeq 2500 system.
The identification and genotyping of SLAF markers
were performed according to the procedure of Sun et al. (2013a). Raw
reads with < Q30 scores were removed. The left-over reads were allotted to
the plant samples according to the duplex barcode sequences and clustered on
the basis of sequence homologies perceived by BLAST analysis.
Genetic linkage map construction
The genetic map was constructed in accordance to the Wu et al. (2018). The incomplete significant segregation
distortion markers were removed, leaving 4,337 Marker loci showing MLOD values larger
than 5.0 were used for linkage group (LG) creation (Zhang et al. 2015). By calculating the MLOD value between
two tags, the labels with MLOD value less than 3 of other SLAF tags were
filtered out; a total of 4,296 loci was generated in the 9 linkage groups. Efficient maximum likehood
estimation method was used for each chromosome to construct a genetic map using
HighMap software.
QTL analysis
QTL analysis was performed by rQTL using an interval mapping method (Broman et al. 2003). The walking
speed of 1 cM was set during composite interval mapping (CIM) (Zhiwen et al. 2012). The
statistical likelihood ratio (LOD score) was calculated to denote the
significance of each QTL interval. Afterwards, the threshold of the LOD score
for significance (P=0.05) was sorted
using 10,000 permutations as suggested by Liu et al. (2016a, b).
Annotation of candidate genes
The candidate genes found in major QTL regions were annotated by
performing sequence alignments with a reference genome of Brassica oleracea in the Ensembl plant genome database and the
Bolbase database (Yu et al. 2013)
using the Blastn function with default parameters. Information regarding the
gene functional annotations and protein features were acquired from different
public databases as described by (Liu et
al. 2016a, b).
Results
Genetic analysis of the BT and FT
traits
Table 1: Results summary of the SLAF sequencing
Parameter |
Value |
Enzyme
digestion protocol |
HaeIII + Hpy166II |
Digestion
normally |
91.37% |
Digestion
partly |
8.63% |
Fragment
length |
264-314bp |
Clean
reads |
423.21M |
Average
Q30 |
94.78% |
Average
GC content |
40.53% |
Develop
the total number of SLAF |
191,209 |
Paired-end
mapped reads |
74.01% |
Singled-end
mapped reads |
5.46 % |
Polymorphic
SLAF |
27,875 |
Number of
linkage groups |
9 |
Number of
markers above |
4,296 |
Genetic
map total map distance |
1,075.66cM |
Genetic
map average distance |
0.25cM |
The F2 population of B.
oleracea was created by crossing ‘Dasun’ and
‘LB07M’ lines. This population was used to investigate the inheritance of FT
and BT. The values for FT and BT ranged 42 to 80 and
37 to 61 days respectively (Fig. 1). The phenotypic distribution patterns of
both traits in the F2 population (Fig. 1) showed that both the
traits are inherited quantitatively.
Analysis of SLAF sequencing data
and genotyping
DNA sequencing provided nearly 4.8 Gb raw data
containing 423.21 M clean reads with fragments length ranging from 264 to 314
bp (Table 1). The Q30 score was 94.78%, and the guanine-cytosine proportion was
36.10%. The details of SLAF sequencing are provided in Table 1. A total of 11.5
M and 15.4 M high quality reads were obtained (Table 2). The aa
× bb segregation patterns with 13,329 SLAFs were used for further analysis
(Fig. 2).
High-density linkage map
construction
A total of 4,296 markers were mapped onto nine chromosomes, designated Chr 1-Chr 9 (Table 3). The average mapped markers integrity
was 99.77%, as indicative of the high quality of the genetic map. Ultimately, a
genetic linkage map of 1,075.66 cM was obtained (Fig. 3). On an average basis,
chromosomes contained 477.3 spanning at an average distance of 119.52 cM. The
map lengths of the 9 chromosomes ranged from 83.86 cM (Chr 2) to 164.24 cM (Chr 6). Chromosome 9 and 2 contained
maximum (592) and minimum (295) numbers of markers, respectively (Table 3).
QTL mapping of FT and BT traits
Phenotypic data of FT and BT traits is provided in Fig. 1. Three QTL were
detected for both traits (Table 3). The primary QTL for BT (LOD=17.77) was
identified as the map position of the chromosome 2 (Table 3 and Fig. 5). This
accounted for 41.14% of the total phenotypic variance for the trait. Whereas,
one minor QTL controlling the same trait was located at the chromosome 7
(LOD=6.56) and accounted for 15.00% of the total phenotypic variance for the BT
trait (Table 4).
The primary QTL for the FT was also located at the
chromosome 2, and accounted for 45.08% of the total phenotypic variance for the
FT trait (Table 4; Fig. 4, 5). It is worth mentioning that both major QTLs
controlling the FT and BT traits were located on chromosome 2 and have a total
spanned distance of 83.86 cM. This indicated that pleiotropic or neighbor
gene(s) are governing the FT and/or BT traits.
Association of SNP markers and
functional genes
Based on the evidences from previously published literature (Table 5)
three candidate genes (Bo2g089890, Bo2g009900 and Bo2g048220) were selected
mainly governing BT and FT traits. The gene Bo2g089890 (SAM1) is homologous of Arabidopsis gene
AT3G15170 which encodes the cup-shaped cotyledon protein-2 that regulates shoot apical
meristem (Arús and Orton 1983; Takada et al. 2001; Vroemen et al. 2003). The second
selected gene Bo2g009900 (WNK8) is homologous to Arabidopsis gene AT5G41990
which regulates the floral meristem and phyllotactic patterning (Chandler 2014; Zhang et al. 2016).
Discussion
In this study, SLAF sequencing was used to construct a high-density
genetic map of B. oleracea using an F2
segregating population of 159 individuals obtained by crossing plants of
Chinese kale lines ‘Dasun’ and ‘LB07M’. Parents of the mapping population had
different bolting time and flowering time profiles. Particularly, ‘Dasun’ has
longer bolting and flowering times than ‘LB07M’. Our map spanned 1,075.66 cM in
9 linkage groups, designated Chr1–Chr9. There were a few maps available for
Chinese kale despite of many linkage maps have been reported for B. oleracea. Compared with previously
reported genetic map of B. oleracea (Babula et al. 2003; Huang et
al. 2017), this newly constructed map had fewer gaps and high
linearity between genetic and physical distance.
Flowering time correlates with production and
quality of Chinese kale. In a previous study, loci controlling flowering time
were mapped in F2 populations using SSR and SRAP markers (Li et al. 2015). The two QTLs
were found on LG5 at a distance of 1.0 cM, governing bolting and flowering
times in Chinese kale (Li et al. 2015).
In this study both major QTL of BT and FT (1.1 and 2.1) were located at
chromosome 2 at the distance less than 1.0 cM, showing their presence at an
identical locus (Table 4 and Fig. 5). The correlation coefficient between BT
and FT time in F2 was 0.872, showing a very significant positive correlation.
Some previous studies e.g., Chaim et
al. (2001); Fazio et al. (2003) and Rao et
al. (2003) have also reported that QTLs for closely related
traits are likely to be located on identical or same regions of chromosomes.
Fig. 1: The phenotypic distribution of the bolting (A) and flowering time (B)
traits in the F2 population of B.
oleoracea. P1 shows the average
bolting or flowering time of parent one (LB07M). P2 shows the
average bolting or flowering time of parent two Dasun.
F1 shows the average bolting or flowering time of F1
generation
Fig. 2: Numbers of each marker segregation type on the linkage maps of Chinese
kale. X-axis represents segregation patterns whereas y-axis shows number of
SLAFs
Fig. 4: The collinearity of chromosomes with the B. oleoracea
reference genome. The x-axis indicates the genetic distance of B. oleoracea
chromosomes accordingly, and the y-axis represents the linearity order of the
physical position in the soybean genome
Fig. 5: Distribution of QTLs and selected candidate genes of BT and FT traits on
Chromosome-2 of Chinese Kale. (A) Candidate genomic region putatively
controlling BT trait on chromosome-2. (B) Candidate genomic region putatively controlling FT trait on
chromosome-2
Fig. 6: Possible involvement of selected candidate genes in floral pathway of
Chinese kale plant. Selected genes ID are shown in red color
Fig. 3: Distribution of SLAF markers on nine chromosomes of Chinese kale. A black bar indicates a SLAF marker. The x-axis represents chromosome number and the y-axis indicates genetic distance in centi-morgan (cM)
Three candidate genes were selected
based on the reference genome, previously published literature (Table 5) and
their homologous genes related to same traits in other plants. The putative
role of these candidate genes in floral pathway is shown in Fig. 6. Two
candidate genes, Bo2g089890 and Bo2g009900 that were selected on the Table 2: SLAF-seq data summary
for Chinese kale F2 population
Samples |
Clean reads |
Q30 % |
GC % |
SLAF number |
Total depth |
Average depth |
Dasun |
11,506,750 |
95.05 |
40.12 |
146,077 |
5,487,967 |
37.57 |
LB07M |
15,469,125 |
94.63 |
40.50 |
155,551 |
7,134,346 |
45.86 |
Offspring |
2,492,061 |
94.77 |
40.53 |
122,703 |
1,174,674 |
9.57 |
Table 3: Basic characteristics of Chinese kale linkage groups
Chromosome |
Marker no. |
Map length |
Maximum distance |
Marker interval |
Integrity (%) |
Double crossover (%) |
Missing (%) |
Chr 1 |
286 |
84.71 |
3.27 |
0.30 |
99.82 |
0.01 |
0.18 |
Chr 2 |
295 |
83.86 |
3.59 |
0.29 |
99.80 |
0.00 |
0.20 |
Chr 3 |
760 |
154.81 |
3.34 |
0.20 |
99.75 |
0.01 |
0.25 |
Chr 4 |
390 |
87.12 |
2.58 |
0.22 |
100.0 |
0.01 |
0.00 |
Chr 5 |
460 |
130.89 |
3.91 |
0.29 |
99.79 |
0.02 |
0.21 |
Chr 6 |
368 |
164.24 |
2.64 |
0.45 |
99.51 |
0.07 |
0.49 |
Chr 7 |
527 |
101.59 |
3.21 |
0.19 |
99.73 |
0.01 |
0.27 |
Chr 8 |
618 |
129.33 |
3.65 |
0.21 |
99.79 |
0.02 |
0.21 |
Chr 9 |
592 |
139.11 |
4.22 |
0.24 |
99.74 |
0.02 |
0.26 |
Total |
4296 |
1075.66 |
4.22 |
0.25 |
99.77 |
|
|
Table 4: An overview of QTLs related with FT and BT traits
QTL ID |
Chromosome |
Start (cM) |
End (cM) |
max LOD |
PVE |
1.1 |
2 |
6.983 |
7.298 |
17.77 |
41.14 |
1.2 |
7 |
48.81 |
49.12 |
6.56 |
15.00 |
2.1 |
2 |
6.04 |
6.35 |
18.80 |
48.08 |
PVE= Phenotypic contribution rate
Table 5: Selected candidate genes associated with BT and FT traits in B. oleracea
found on major QTLs
Gene name |
Gene ID |
Function |
Reference |
SAM1 |
Bo2g089890 |
Regulation of shoot apical meristem. |
(Takada et al. 2001;
Vroemen et al. 2003) |
WNK8 |
Bo2g009900 |
Regulating floral meristem, phyllotactic
patterning |
(Chandler 2014; Zhang et
al. 2016) |
GA20OX3 |
Bo2g048220 |
Initiation of flowering. |
(Mutasa-Göttgens and Hedden
2009; Plackett et al. 2011; Rebers et al. 1999; Tenreira et
al. 2017) |
major QTL 1.2, which controls the traits
for bolting time or first flowering bud. These genes encode the cup-shaped
cotyledon protein-2 (Bo2g089890) and serine/threonine-protein kinase
(Bo2g009900), which have been shown to regulate shoot apical and flower
meristems, respectively, according to the GO annotations and previously
published literature (Table 5). The gene Bo2g009900, is homologous to
Arabidopsis gene AT5G41990, and encodes a WNK8 like serine/threonine-protein
kinase. The same gene in Arabidopsis plants has been shown to regulate the
flowering time by modulating the photoperiod pathway (Wang et al. 2010).
The WNK8 protein also interacts with the EDM2 protein that in turn, modulates
floral meristem and developmental processes (Tsuchiya and Eulgem 2010). The
flower organ specification processes are centered within the flower meristem
(FM) to generate floral organs (Chandler 2014), with the FM differentiation
determined by the stem cells within the shoot apical meristem (Zhang et al.
2016). This coordinated role of SAM and FM highlights the importance of both of
these meristems in bolting time or appearance of the first flower node. When
considering the importance of the shoot apical and flower meristems in the
development of first flower node (Zhang et al. 2018), the genes
Bo2g024555 and Bo2g009900 are important candidates for bolting time or
appearance of the first flower node trait in B. oleoracea. Chromosome 02 appears to be a strong candidate having
major QTLs with the genes controlling bolting time.
The candidate gene for flowering time, Bo2g048220,
is homologous to Arabidopsis
AT5G07200, and encodes the gibberellic acid (GA) 3-oxidase (GA3ox) protein. The
GA oxidases proteins primarily dictate early floral initiation (Rebers et al. 1999; Mutasa-Göttgens and
Hedden 2009; Tenreira et al. 2017) and fruit
development (Rebers et al. 1999)
by regulating different floral networks (Mutasa-Göttgens
and Hedden 2009). The GA3ox catalyzes the last step in bioactive GA
biosynthesis. GA is a regulator of flowering initiation (Plackett et al.
2011). The exogenous application of GA3 and GA4 has shown
early bud development in apple plants (Bertelsen et al. 2002).
As both major QTLs are residing on chromosome 02,
this genomic region can be helpful for developing early maturing Chinese kale
varieties using marker assisted breeding technology.
Conclusion
This is the first report highlighting the involvement GA3ox, WNK8 and SAM1
genes in the quantitative inheritance of early BT and FT traits in Chinese kale
plants. Secondly, the high-density genetic map of Chinese kale constructed in
this study will offer a suitable basis for further study of Chinese kale, such
as gene mapping, map-based cloning of specific genes, quantitative trait locus
mapping and marker-assisted selection.
Acknowledgements
This study was supported by the projects of Guangdong Agriculture
Department Foundation (2019KJ122) and Guangdong Academy of Agricultural
Sciences Foundation of the Dean Project (Grant No. 201816B).
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