Environmental and Experimental Botany 180 (2020) 104245

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Environmental and Experimental Botany

journal homepage: www.elsevier.com/locate/envexpbot

Genome-wide identification and expression analysis of MYB gene family in

oil palm (Elaeis guineensis Jacq.) under abiotic stress conditions
Lixia Zhou, Rajesh Yarra, Longfei Jin, Hongxing Cao *
Coconut Research Institute, Chinese Academy of Tropical Agricultural Sciences/ Hainan Key Laboratory of Tropical Oil Crops Biology, Wenchang, Hainan, 571339, PR
China

A R T I C L E I N F O A B S T R A C T

Keywords: The MYB transcription factors are one of the largest gene families in plants and known to play critical roles in
EgMYB genes regulating various responses including abiotic stresses. Currently, a few of MYB family genes have been identified
Elaeis guineensis and characterized in various plants. In this study, we identified a set of 159 MYB genes in oil palm via genome-
Abiotic stress
wide screening. The 159 identified oil palm MYB genes belong to two subfamilies (R2R3-MYB and 3R-MYB type),
Transcription factors
and were divided into 25 subgroups based on phylogenetic analysis. These EgMYB genes were mapped on the 16
chromosomes of the oil palm genome with the co-linearity relationship among them. The intron/exon organi­
zation and motif compositions were conserved among the EgMYB genes. Gene duplication analysis also proved
that EgMYB genes experienced strong purifying selection and tandem duplications during evolution. Expression
profile analysis revealed the constitutive expression of EgMYB genes in different tissues of oil palm. Quantitative
PCR analysis of 21 EgMYB genes under different abiotic stress conditions (cold, salt, and drought) proved their
differential expression. A total of 20, 19, and 18 EgMYB genes were significantly up-regulated under cold, salt,
and drought stress conditions respectively. In addition, none of the analyzed EgMYB genes were down-regulated
under any of these stress conditions. Our study elucidated the role of EgMYB genes in abiotic stress conditions
and can be used as prominent candidate genes for improving abiotic stress tolerance in this important oil yielding
crop.

1. Introduction
The abiotic stresses such as salinity, drought, cold and high tem­
perature severely affect the growth, development, and yield of crops
(Zandalinas et al., 2020; Ali et al., 2019; Zhao et al., 2019; Zhang et al.,
2017). To cope up with the adverse environmental stress conditions, an
array of genes are expressed in a synchronized mode to regulate plant
growth and development (Lamers et al., 2020; Haak et al., 2017).
Finding the candidate genes and dissecting signaling mechanisms in
abiotic stress responses is a key determinant to develop abiotic
stress-tolerant crops (Anwar and Kim, 2020). Moreover, transcription
factors (TFs) play an important role in plant growth, development, and
stress response through self-regulation as well as by regulating the
expression of downstream target genes (Baillo et al., 2019; Wang et al.,
2016; Wang et al., 2015). A large number of TFs have known to mediate
abiotic stress responses in plants (Li et al., 2020; Baillo et al., 2019; Xiao
et al., 2018; Hoang et al., 2017; Tang et al., 2018; Xiong et al., 2014; Oh
et al., 2011).
MYB gene family is the largest and abundant transcription factor
(TF) families in plants and known to involve in vital roles including
development, abiotic stress response, hormone signal transduction and
secondary metabolism regulation (Li et al., 2020; Liu et al., 2015;
Ambawat et al., 2013; Dubos et al., 2010). In plants, MYB proteins are
characterized by a highly conserved DNA-binding domain (MYB) con­
sisting of 51~52 amino acid residues length at its N-terminal region with
one to four imperfect repeat (R)sequences (Li et al., 2020; Li et al.,
2019c; Li et al., 2016; Liu et al., 2012). Each repeat forms
helix-turn-helix (HTH) structure motif fold with three conserved tryp­
tophan residues. Based on the number and position of repeats, MYB
proteins are classified into four major types such as 1R-MYB, 2R-MYB,
3R-MYB, and 4R-MYB proteins and 2R-MYB proteins are predominantly
present in plants (Dubos et al., 2010).
To date, a few number of MYB genes (100-530) have been identified
and functionally analyzed in a wide range of plants with the help of
available plant genome sequeneces in various databases. A total of 198
(Arabidopsis thaliana), 183(Oryza sativa), 139(Solanum lycopersicum),166

* Corresponding author.
E-mail address: hongxing1976@163.com (H. Cao).

https://doi.org/10.1016/j.envexpbot.2020.104245
Received 25 July 2020; Received in revised form 23 August 2020; Accepted 25 August 2020
Available online 29 August 2020
0098-8472/© 2020 Elsevier B.V. All rights reserved.
L. Zhou et al.
(Medicago truncatula), 170(Rhododendron delavayi), 158(Solanum tuber­
osum),205(Gossypium raimondii), 524(Gossypium hirsutam), 252 (Glycine
max) and 245 (Helianthus annuus L.) MYB genes were identified and
analyzed (Chen et al., 2006; Liu et al., 2012; Saha et al., 2016; Zhang
et al., 2018a, 2018b; Sun et al., 2019; He et al., 2016; Salih et al., 2016;
Du et al., 2012b; Li et al., 2020). Furthermore, MYB proteins are also
played a vital role in regulating abiotic stress responses in plants (Baillo
et al., 2019; Dubos et al., 2010; Ambawat et al., 2013). MYB genes are
also known to regulate its downstream genes at the transcriptional and
post-transcriptional levels under abiotic stress conditions (Baillo et al.,
2019). Several studies have shown the role of MYB genes in various
abiotic stress responses. Over-expression of various MYB genes
enhanced the abiotic stress tolerance in a wide variety of species,
including AtMYB20 in rice (Cui et al., 2013); BpIMYB46 in Betula pla­
typhylla (Guo et al., 2017), OsMYB2, OsMYB3R-2, OsMYB48-1, OsMYB6
in rice (Yang et al., 2012; Ma et al., 2009; Xiong et al., 2014; Tang et al.,
2019), TaODORANT1 in wheat (Wei et al., 2017) and ZmMYB30 in
Arabidopsis (Chen et al., 2018a). Although numerous MYB genes have
been identified and functionally characterized in both model and
non-model plants under abiotic stress conditions, but identification and
characterization of MYB gene family members in oil palm is not done
yet. Therefore, genome-wide identification of MYB genes in oil palm is
vital for understanding their role in abiotic stress responses for devel­
oping stress-tolerant oil palm varieties.
Oil palm (Elaeis guineensis) is the most productive oil crop in the
world (Barcelos et al., 2015). However, abiotic stresses such as drought,
temperature (low and high) and nutritional stresses severely limit oil
palm productivity (Abdullah et al., 2017; Murugesan et al., 2017; Xiao
et al., 2017). Identifying and validating genes related to abiotic stress
responses in oil palm will provide the basis for molecular breeding of
stress-tolerant oil palm cultivars. The genome size of oil palm is 1.8 GB
with 26059 genes distributed over 16 chromosomes (http://palmxplore.
mpob.gov.my). Since completion of oil palm genome sequencing in
2013 (Singh et al., 2013), limited genome-wide identification studies
have been done in oil palm to elucidate the role of various genes and
transcription factors in abiotic stress responses (Xiao et al., 2017).
Recently (Xiao et al., 2017), the WRKY genes were identified in oil palm
through genome-wide screening and analyzed their expression analysis
under various abiotic stress conditions. To date, no genome-wide iden­
tification of MYB genes has been carried out in oil palm. Given this, it’s
an imperative need to conduct genome-wide characterization of the
MYB gene family in oil palm. In this study, we focused on genome-wide
identification and expression analysis of MYB genes in oil palm under
various abiotic stress conditions.
In the present study, we identified 159 MYB genes from the oil palm
genome using the known MYB gene sequences from Arabidopsis genome.
Further, the gene structure (intron/exon distribution), phylogenetic
relationships, motif composition, and duplication events were also
investigated. We also analyzed the expression levels of 21 EgMYB genes
to various abiotic stresses (cold, salt, and drought) using qRT-PCR. To
the best of our knowledge, this is the first report on genome-wide
identification of MYB genes and their expression analysis in oil palm
under abiotic stress conditions. Our study laid a foundation to dissect the
abiotic stress tolerance mechanisms in this important oil yielding crop
and also to explore the functions of MYB genes in other crops.
2. Materials and methods
2.1. Identification of EgMYB genes
The oil palm genome sequences were downloaded from the National
Center for Biotechnology Information (NCBI) database. The amino acid
sequences of Arabidopsis MYB proteins (AtMYBs) were downloaded from
The Arabidopsis Information Resource (TAIR) (http://www.arabid
opsis.org) database. The Pfam protein family database (http://pfam.
sanger.ac.uk/) was employed to obtain the Hidden Markov model
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Environmental and Experimental Botany 180 (2020) 104245
(HMM) profile of the MYB domain (PF00249). The AtMYB gene se­
quences were used as query sequences to identify MYB genes from the
oil palm genome. The identified MYB genes that contain conserved
domains were further analyzed, and those without PF00249 conserved
domain were removed from the data. The BLASTp tool available at
National Center for Biotechnology Information (NCBI) was used to
analyze the oil palm MYB genes, whether they belong to the MYB gene
family or not. A total of 159 EgMYB genes were finally identified from
the oil palm genome. Further, we predicted the information about these
genes, including isoelectric point (pI) and molecular weight (Mw), by
using the ExPASy proteomic website (https://web.expasy.org/comp
ute_pi/). In addition, CELLO tool was used to predict the subcellular
localization of all EgMYB genes.
2.2. Analysis of phylogenetics, intron-exon structure, motif composition,
chromosomal distribution, and gene duplication events
A maximum likelihood (ML) phylogenetic tree of MYB gene family
from oil palm and Arabidopsis thaliana was constructed using MEGA 6.06
software based on amino acid sequences of conserved MYB domain and
with 1000 bootstrap replicates for reliability (Larkin et al., 2007).
Further, we downloaded the gene annotation summaries, CDS, and
mRNA sequences of oil palm MYB genes from the NCBI database (Sup­
plementary Table 1). mRNA sequences were aligned with the oil palm
whole-genome sequence for further confirmation of oil palm MYB gene
structures. The online tool i.e. Gene Structure Display Server program
was used to determine the oil palm MYB gene structures (intron-exon
organization). The Motif Elicitation (MEME) online program (htt
p://meme-suite.org/tools/meme) was employed to determine the
conserved motifs of MYB proteins by the Multiple Em (Supplementary
Table 2). The TB tools software (Chen et al., 2018a, 2018b) was
employed to map the chromosomal distribution of MYB genes in the oil
palm genome, according to the genome annotation documents available
at the oil palm genome database. The MCScanX tool (Multiple Collin­
earity Scan) was employed to analyze the gene duplication events of
identified oil palm MYBs with a set of parameters (Wang et al., 2012).
2.3. MYB gene expression analysis based on available transcriptome
datasets
The available transcriptome data of oil palm tissues, including
mesocarp (15 weeks (SRR190698), 17 weeks (SRR190699), 21 weeks
(SRR190701) & 23 weeks (SRR190702)), flower (SRR851108), fruit
(SRR851067), leaf (SRR851096), root (SRR851071) and shoot
(SRR851103) were downloaded from NCBI website in Sequence Read
Archive (SRA) database. Gene expression levels were calculated using
RPKM values with the help of the following formula as described by
Verma et al., 2013.
106 C
Reads per kb per million reads (RPKM) =
NL 103
/
Where C represents, aligned reads with one expressed sequence. N
represents, total aligned reads with all expressed sequences and L rep­
resents, number of bases in the coding sequence pertaining to the cor­
responding sequence.
2.4. Plant materials and abiotic stress treatments
To analyze the oil palm MYB genes expression under abiotic stresses
(cold, salt, and drought stress), a total of 36 oil palm (Elaeis guineensis)
seedlings were grown in nurseries of Coconut Research Institute, Chi­
nese Academy of Tropical Agricultural Sciences (Wenchang province,
China). The oil palm seedlings germinated in the same week were
further selected for abiotic stress treatment experiments. For each
experiment, nine plants were used for abiotic stress treatments and three
L. Zhou et al.
plants were used as controls. For the cold treatment experiment, oil palm
seedlings were transferred to a growth chamber at 27 ℃ for one day and
then exposed to 8℃ at different time intervals (0 h (control), 4 h, 24 h,
and 48 h). The spear leaves were harvested from cold treated and control
plants and immediately frozen in liquid nitrogen for further experi­
ments. For the drought treatment experiment, drought parameters were
set as when soil water content reached 20 %. Subsequently, spear leaves
were collected after 0 h (control), 4 h, 24 h, and 48 h of drought stress
and immediately frozen in liquid nitrogen for further experiments. For
the salt treatment experiment, individual oil palm seedlings with roots
were immersed in a NaCl solution (300 mmol/L) and kept at 16 h of light
and 8 h of darkness photoperiod at 27 ℃, and spear leaves were har­
vested after 0, 4, 24, and 48 h after NaCl treatment and immediately
frozen in liquid nitrogen for further experiments. The control seedlings
for each treatment experiment were grown under 16 h of light and 8 h of
darkness photoperiod at 27℃ and with three biological replicates and
repeated three times for each stress treatment.
2.5. RNA isolation and qRT-PCR analysis
Total RNA was extracted from the leaves of cold, drought, salt-
treated and control plants using QRREM method as described by Iqbal
et al., 2019. Extracted RNA samples were further assessed by agarose gel
electrophoresis and Nanodrop spectrophotometer for quantity and
quality check. cDNA was synthesized using 1 μg RNA with MightyScript
first-strand cDNA synthesis kit with gDNA digester, by following man­
ufacturer’s instructions. Quantitative real-time PCR reactions were
performed in a Mastercycler ep realplex4 machine using 2 × SYBR Green
qPCR ProMix (low ROX) protocol in 384-well optical plates. MYB
gene-specific primers were designed using the QuantPrime qPCR primer
designing tool. The reactions were performed with a final reaction vol­
ume of 10 μl and amplification reaction conditions were 95 ◦ C/5 s, 55
◦
C/15 s, and 68 ◦ C/20 s. The melting curve stage was rising from 60 ◦ C
to 95 ◦ C/20 min. All reactions were performed with three biological as
well as three technical repeats. The 2-ΔΔCt method was adopted for
analyzing the expression levels and the ELF gene was used as an internal
control (Xia et al., 2014). One way ANOVA was used to determine the
statistical significance at p < 0.05 and p < 0.01 with the help of SPSS
software.
3. Results
3.1. Genome-wide identification of MYB genes in Elaeis guineensis
A total of 159 MYB genes were successfully identified from the oil
palm genome and designated them as EgMYB01 to EgMYB159. Detailed
information of all identified MYB genes was provided in Supplementary
Table 1 and Supplementary Table 2. The length of amino acids in EgMYB
proteins ranged from 147 to 1150 (Supplementary Table 1). The mo­
lecular weight and isoelectric points of the predicted proteins ranged
from 127 to 17 and 10.12 to 4.75 respectively (Supplementary Table 1).
Further, the subcellular localization of EgMYB proteins were predicted
and the majority of them were localized in the nucleus. But EgMYB53
was localized in the nucleus, chloroplast, and mitochondria (Supple­
mentary Table 1).
3.2. Chromosomal location of EgMYB genes
To know the genomic distribution of EgMYB genes, we searched the
chromosomal locations of the MYB gene family in the oil palm genome
based on the annotation of DNA sequences. Our results demonstrated
that all the identified 159 oil palm MYB genes were distributed to 16
chromosomes in the genome. Among the 159 MYB genes, 135 MYB
genes were found to be unevenly distributed among 16 chromosomes. In
total, 11 EgMYB genes are located on chromosome 1; 13 EgMYB genes on
chromosome 2; 14 EgMYB gene on chromosome 3; 9 EgMYB genes on
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Environmental and Experimental Botany 180 (2020) 104245
chromosome 4; 15 EgMYB genes on chromosome 5; 6 EgMYB genes on
chromosome 6; 10 EgMYB genes on chromosome 7; 3 EgMYB genes on
chromosome 8; 2 EgMYB genes on chromosome 9; 12 EgMYB genes on
chromosome 10; 7 EgMYB genes on chromosome 11; 7 EgMYB genes on
chromosome 12; 9 EgMYB genes on chromosome 13; 5 EgMYB genes on
chromosome 14; 7 EgMYB genes on chromosome 15; and 5 EgMYB genes
on chromosome 16 (Fig. 1), whereas 24 EgMYB genes were attributed to
the chromosomes that were undetermined. Most of the EgMYB genes
(15) were present on the chromosome 5, followed by chromosome 3
(14MYBs) and chromosome 2(13MYBs), whereas chromosome 9 had the
lowest number of MYB genes (2) (Fig. 1).
3.3. EgMYB gene structure and motif composition analysis
The intron-exon structure of 159 EgMYB genes was analyzed by the
Gene Structure Display Server program (Fig. 2). The results demon­
strated that most of the MYB genes possessed introns ranging from 0 to
11 (Fig. 2). Among the 159 EgMYB genes, the highest number (11) of
introns were possessed by three MYBs including EgMYB151, EgMYB153
and EgMYB 156 followed by EgMYB136 and EgMYB140 (10 introns),
EgMYB124 (8 introns), EgMYB133 (7 introns), EgMYB125, EgMYB129
and EgMYB134 (6 introns). A total of eight genes (EgMYB122, EgMYB
123, EgMYB127, EgMYB132, EgMYB135, EgMYB148, EgMY154, and
EgMYB155) completely lacked the introns. Three genes including
EgMYB151, EgMYB153, and EgMYB156 had the highest number of exons
(12). The majority of the MYB genes had a very limited number of in­
trons (0-3), indicating the conserved number of introns among the
MYBs. The variation in the EgMYB gene structure indicated the signifi­
cant divergence of the oil palm genome.
Further, we analyzed the protein motif analysis to know the diver­
sification of the EgMYB gene family in oil palm. Our results predicted the
existence of 10 conserved motifs among all identified 159 MYB genes
(Supplementary Table 3; Fig. 3). However, no motif was repeated in any
of the EgMYB protein (Fig. 3).
3.4. Duplication events of oil palm MYB genes
To analyze the duplication events of the EgMYB gene family, we used
MCScanx and Circos software to detect the duplicated blocks in the oil
palm genome. The non-synonymous and synonymous substitution ratios
(ka/ks = 1, neutral selection; ka/ks>1, positive selection; ka/ks<1,
negative selection) were calculated for MYB gene duplication events
analysis. The Ka/Ks ratio values were found to be greater than one (>1)
for 5 duplicated gene pairs, where as Ka/Ks ratio values were between
0.5 and 1.0 for another 52 pairs (Supplementary Table 4). The majority
of EgMYB gene pairs exhibited less than 1 of Ka/Ks values, indicating
that EgMYB genes undergone a strong purifying selection during evo­
lution with a little variation after duplication. Moreover, the duplication
events predictable to happen between 0.058 to 34.009mya (Supple­
mentary Table 4). Results indicated that EgMYB genes undergone tan­
dem duplications on 16 chromosomes (Fig. 4). The majority of the
EgMYB genes have existed in duplicated genomic regions. All of the 16
chromosomes contained duplicated MYB genes, whereas chromosomes
8 and 9 contained the lowest number of duplications. The chromosomes
3, 7, and 15 were associated with the highest number of gene duplica­
tions (Fig. 4). Altogether, suggesting that tandem duplication played an
essential role in the expansion of the MYB gene family of oil palm.
3.5. Phylogenetic analysis of EgMYB genes
A maximum likelihood (ML) phylogenetic method was employed to
generate a phylogenetic tree for MYB proteins among oil palm (159 MYB
proteins) and Arabidopsis thaliana (130 MYB proteins) (Fig. 5). The
phylogenetic tree divided the MYB genes in oil palm and Arabidopsis into
25 subgroups (S1-S25) (Fig. 5). These 25 subgroups belong to two major
types of MYB protein families such as 3R-MYB and R2R3-MYB family
L. Zhou et al. Environmental and Experimental Botany 180 (2020) 104245

Fig. 1. EgMYB genes distribution across 16 chromosomes of oil palm genome. The scale represents the length of oil palm chromosomes.

Fig. 2. Gene structure of 159 MYB genes from Elaeis guineensis.

(Fig. 5). A total of seven EgMYB genes (EgMYB124, EgMYB125,
EgMYB129, EgMYB133, EgMYB134, EgMYB135 & EgMYB140) and five
of AtMYB genes attributed to the 3R-MYB subfamily, whereas other 152
EgMYB and 125 AtMYB genes belonged to the R2R3-MYB family. The
MYB genes that belong to the R2R3-MYB family were further sub-
divided into S1-S7, S9-S16, and S18-S25 subgroups. Each S1, S2 and
S7 subgroup consisting of 8 EgMYB genes, S4 consisting of 9 EgMYB
genes, S5 and S13 consisting of 10 EgMYB genes, S6, S9 and S19
consisting of 3 EgMYB genes, S10 and S20 consisting of 11 EgMYB genes,
S11 consisting of 1 EgMYB gene, S14 consisting of 18 EgMYB genes, S16
and S22 consisting of 5 EgMYB genes, S18 consisting of 15 EgMYB genes,
S21 consisting of 14 EgMYB genes, S23 consisting of 2 EgMYB genes, S24
and S25 consisting of 4 EgMYB genes. Moreover, no EgMYB genes were
attributed to S3, S8, S12, S15 or S17 subgroups, suggesting few of MYB
genes have been lost in oil palm genome evolution and attained during
evolution in Arabidopsis. Some of the subgroups contain more EgMYB

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L. Zhou et al. Environmental and Experimental Botany 180 (2020) 104245

Fig. 4. Gene duplication of EgMYB genes on 16 chromosomes of oil palm

genome. Red color lines inside the circle represent duplicated gene pairs. Each
chromosome number is represented with a different colored box.

Fig. 3. A total of ten conserved motifs distribution in EgMYB genes. Each motif
is represented by a number (1-10) in the colored box. Sequence logos of amino
acid residues of 10 conserved motifs of EgMYB proteins are also shown.

genes than AtMYB genes suggesting functional divergence of MYB genes

in different plant species. Phylogenetic analysis revealed that clustering
of various MYB genes into the same group may have conserved functions
and its need to be clarified via experimental approaches

3.6. Expression profile analysis of EgMYB gene family in six tissues of

Elaeis guineensis

We used the raw transcriptome data of oil palm tissues (mesocarp,

root, flower, fruit, leaf, and shoot) from the SRA database of the NCBI to
analyze the expression level of oil palm MYB genes. A heatmap of
EgMYBs was generated with corresponding FPKM values of tissues using
a pheatmap tool to analyze the abundance of MYB transcripts (Fig. 6).
We only evaluated the transcript abundance of 119 EgMYB genes due to
the unavailability corresponding probe sets in the data set. Interestingly,
a total of ~78 (65 %) EgMYB genes displayed the highest transcript
abundance levels in roots (20 MYBs), flower (19MYBs), leaf (16 MYBs)
and shoot (13MYBs) and mesocarp tissues (10 MYBs). However, most of
the EgMYBs that showed the highest expression in specific tissues were
not up-regulated in any other tissues (Fig. 6). But only 4 EgMYBs have
shown similar expression in two different tissues including EgMYB05 in
mesocarp (23 weeks old) and shoot, EgMYB28 in fruit and root,
EgMYB114 in mesocarp (15 weeks old) and flower, EgMYB 123 in fruit
and root. Moreover, a total of five MYB genes (EgMYB29, EgMYB 121,
Fig. 5. Phylogenetic analysis of 159 EgMYB (oil palm) and 130 AtMYB (Ara­
bidopsis) genes. A maximum likelihood (ML) phylogenetic tree of 289 MYB
genes of two plants was constructed using MEGA 6.06 software with pro­
tein sequences.
EgMYB124 EgMYB156, and EgMYB140) were down-regulated in most of
the tissues. Our results revealed the tissue-specific expression of EgMYB
genes (Fig. 6).
3.7. Expression patterns of EgMYB genes under abiotic stresses
A total of 21 EgMYB genes have chosen to examine expression
analysis in different abiotic stress (cold, salinity, and drought) condi­
tions in oil palm using quantitative real-time PCR. Interestingly various

5
L. Zhou et al. Environmental and Experimental Botany 180 (2020) 104245

Fig. 6. The heat map depicting the expression profile analysis of 119 EgMYB genes in various organs or tissues (mesocarp, flower, fruit, leaf, root, and shoot) of oil
palm. Expression levels of MYB genes are indicated by different colors as shown on the scale. Heat map was generated by using pheatmap software.

abiotic stresses induced the expression of all EgMYB genes (Fig. 7;
Supplementary Table 5). Except for EgMYB79 and EgMYB124, remain­
ing all have shown increased expression under cold stress conditions.
Salt stress-induced the expression levels of 19 MYB genes, except
EgMYB03, EgMYB90, and EgMYB157 (Fig. 7). Drought stress also
significantly enhanced the expression levels of 18 MYB genes, except
EgMYB07, EgMYB22, EgMYB90, and EgMYB126 genes. In addition, a
total of 14 MYB genes (EgMYB38, EgMYB43, EgMYB57, EgMYB76,
EgMYB82, EgMYB91, EgMYB104, EgMYB106, EgMYB111, EgMYB127,
EgMYB133, EgMYB146, EgMYB 151 and EgMYB155) were significantly
up-regulated under all abiotic stress conditions (cold, salt and drought)
(Fig. 7; Supplementary Table 5), indicating the regulatory role of EgMYB
genes in a wide array of abiotic stress responses. Moreover, none of the
analyzed EgMYB genes were down-regulated in any of the abiotic stress
conditions. Our results strongly supporting the role of EgMYB genes in
abiotic stress tolerance. The primers used for quantitative PCR analysis
were provided in Supplementary Table 6.
4. Discussion
MYB gene family members are widely found in plants, and are known
to play vital roles in plant development (Zheng et al., 2016), metabolism

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L. Zhou et al. Environmental and Experimental Botany 180 (2020) 104245

Fig. 7. Relative expression of 21 EgMYB genes under abiotic stress conditions (cold, salt, and drought stress). Asterisks represent significant difference at P ≤ 0.05(*)
and P ≤ 0.01(**).

7
L. Zhou et al.
Fig. 7. (continued).
(Pu et al., 2020; Chen et al., 2017b), cell differentiation (Kasahara et al.,
2005), cell cycle regulation (Huang et al., 2013), hormone (Sun et al.,
2019) and environmental factor responses (Li et al., 2020; Baldoni et al.,
2015; Katiyar et al., 2012). In recent days, many researchers systemat­
ically identified MYB gene family members in various plants by utilizing
the available whole genome sequences (Li et al., 2020; Tan et al., 2020;
Qing et al., 2019; Yang et al., 2019). However, to date, none of the re­
ports are published for the identification and functional role of the MYB
gene family in oil palm. In present investigation, we identified 159 MYB
genes in the oil palm genome and this is the first systematic study on
EgMYB genes through bioinformatics tools and expression profiling
analysis. We also determined the EgMYB gene structure, chromosomal
distribution, phylogenetic analysis, gene duplication events, and
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Environmental and Experimental Botany 180 (2020) 104245
expression profile analysis in various tissues and under abiotic stress
conditions. The identified number of MYB genes in oil palm (159)
(Supplementary Table.1) are neither high nor less than those MYB genes
in various plants (Sesamum indicum L., 287 MYBs; Sunflower, 245 MYBs;
rice, 183 MYBs; Arabidopsis, 198 MYBs; Solanum tuberosum, 158 MYBs;
Jatropha curcas, 125 MYBs; Tamarix hispida, 14 MYBs) (Mmadi et al.,
2017; Li et al., 2020; Chen et al., 2006; Sun et al., 2019; Zhou et al.,
2015; Zhang et al., 2018a)
The varied nucleotide sequence length among 159 EgMYB genes
demonstrated their complexity in the oil palm genome. The evolution of
numerous gene families mainly depends on the organization of gene
structure (Xiao et al., 2017; Xu et al., 2012). A varied number of introns
(0-11) was possessed by EgMYB genes. Moreover, the majority of the
L. Zhou et al.
Fig. 7. (continued).
EgMYB genes were possessed typical splicing of 3 exons and 2 introns.
Further, 71.70 % of EgMYBs contained two introns. Our results are also
consistent with the recent findings of MYB genes (HaMYB and StMYBs)
in sunflower and potato (Li et al. 2020; Sun et al., 2019). The molecular
weight and isoelectric point values of EgMYB proteins were significantly
different among them, indicating the functional divergence of MYB
proteins similar to other plant proteins behaviour in various
micro-environment conditions (Li et al., 2020; Feng et al., 2017). EgMYB
proteins contained 10 conserved motifs with different compositions.
Phylogenetic tree analysis of 159 EgMYB protein sequences divided
them into 25 subgroups (S1-S25) based on two kinds of MYB-families
(3R-MYB and R2R3-MYB), suggesting the MYB gene family conservation
and diversification among the land plants. Moreover, EgMYB genes had
undergone a strong purifying selection and tandem duplication events
during expansion of MYB genes. These findings coincide with the pre­
vious studies on genome-wide identification of MYB genes in various
plants (Li et al., 2020; Du et al., 2012a; Du et al., 2012b)
The MYB transcription factors exhibit varied expression profiling in
various tissues or organs to control various biological and physiological
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Environmental and Experimental Botany 180 (2020) 104245
processes in plants (Ambawat et al., 2013). The gene expression
profiling data is indispensable to dissect the functional roles of various
genes. As shown in Fig. 6, EgMYB gene transcripts abundance was
associated with different tissues/organs (root, shoot, leaf, flower, and
mesocarp of fruit). However, the expression pattern of each EgMYB gene
was altered in each tissue/organ (Fig. 6). Approximately, 65 % (78 of
119) of the EgMYB genes were expressed in all tissues, suggesting the
vital roles of MYB genes in controlling plant growth and developmental
processes. (Li et al., 2020; Li et al., 2019a; Mmadi et al., 2017; Ambawat
et al., 2013)
Recent studies demonstrated the regulatory role of MYB genes in
abiotic stress response of plants (Li et al., 2020; Tang et al., 2019; Zhou
et al., 2019; Zhang et al., 2018a). In this study, we analyzed the
expression levels of 21 EgMYB genes under three abiotic stress condi­
tions including salinity, cold, and drought. Most of the EgMYB genes(20)
were significantly up-regulated under cold stress conditions. Our find­
ings were also correlated with the previous findings on cold-induced
MYB genes in rice (OsMYB3R-2), Arabidopsis (AtMYB14), apple
(MdMYB 23) (Dai et al., 2007; Chen et al., 2013; An et al., 2018). A total
L. Zhou et al.
of 19 EgMYB genes were also induced by salt stress and these findings
were also consistent with the previous reports on salt stress-induced
MYB genes in sunflower (HaMYB15.14), wheat (TaSIM), rice (RTBP1)
and Arabidopsis (AtTBP1, HPPBF-1)(Li et al., 2020; Yu et al., 2017;
Nagaoka and Takano, 2003; Hwang et al., 2001). Drought stress-induced
MYB genes were also reported in various plants including sunflower (Li
et al., 2020), wheat (Li et al., 2019b; Zhao et al. 2018), and rice (Tang
et al., 2019). In our study also, a total of 18 EgMYB genes were induced
by drought stress. Moreover, EgMYB38, EgMYB43, EgMYB57, EgMYB76,
EgMYB82, EgMYB91, EgMYB104, EgMYB106, EgMYB111, EgMYB127,
EgMYB133, EgMYB146, EgMYB 151 and EgMYB155 were up-regulated
in all three abiotic stress conditions, indicated the significant contribu­
tion of EgMYB genes in varied abiotic stress conditions.
5. Conclusions
In conclusion, we identified 159 MYB genes in the oil palm genome
via genome-wide screening. A comprehensive analysis of an intron-exon
organization, phylogenetic relationships, distribution on chromosomes,
gene duplication, conserved motifs, and expression levels under abiotic
stress conditions was also performed. Expression profiling analysis of
EgMYBs in different tissues of oil palm revealed the constitutive
expression of MYB genes with significant functional divergence. Further,
a quantitative PCR analysis of 21 EgMYB genes in leaves of the oil palm
under three different abiotic stress conditions (cold, salinity, and
drought) revealed their differential expression. Our findings will explore
the research on EgMYB gene family functional characterization under
abiotic stress conditions and to develop the stress-tolerant oil palm
plants for better oil yield in adverse environmental conditions.
Author Contributions
LZ and HC conceived and designed the experiments. LZ and RY
performed the experiments; LZ, RY and LJ validated the data, LZ, RY and
LJ performed the formal analysis; LZ, and RY participated in original
draft preparation; HC supervised the research
Declaration of Competing Interest
The authors reported no declarations of interest.
Acknowledgements
This research work was financially supported by Hainan Provincial
Natural Science Foundation of China (319QN324), Central public-
interest scientific institution basal research fund for the Chinese Acad­
emy of Tropical Agricultural Sciences (No.1630152019001); and the
fund for species and varieties conservation of sector project of the
Ministry of Agriculture and Rural Affairs (18200039), China.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.envexpbot.2020.10
4245.
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