Introduction
Grain production is the foundation of agricultural
development in a country. As one of the main grain crops, maize plays an
important role in agriculture (Zhao et al. 2016) and is rich in various nutrients, such as fat, vitamins,
protein, cellulose and trace elements (Zhao et al. 2018). However, there are many
disadvantages in the process of traditional breeding due to the variety of
maize and the complexity of heredity. Using molecular biology to identify gene
function and assist traditional breeding can speed up breeding.
As a small family in plants,
Trihelix transcription factor family was only limited to the study of light
response until the end of the 20th century. With the progress of
biotechnology and the rapid development of bioinformatics, more and more
members of Trihelix transcription factor family have been identified (Zhou et al. 2015). For
example, 30 Trihelix genes have been identified in Arabidopsis, 31 in rice and other species (Zhou et al. 2015). More
studies have found that Trihelix family genes play an important role in the
growth and development of different parts of plants, such as flowers, epidermal
hairs, stomata, seeds and embryos, as well as in the response of biological and
abiotic stresses such as diseases, salt stress, drought stress and cold stress
(Zhang et al. 2017). However, the study of identifying and analyzing the
gene family based on the whole genome level of maize has not been reported. In
this study, the Trihelix transcription factor family in maize was analyzed and
the basic information statistics, conservative domain analysis, gene structure
prediction, gene location on chromosome, amino acid physical and chemical
properties and expression analysis of Trihelix transcription factor gene family
in maize were carried out by using bioinformatics method. This study will
provide useful information for further analysis of the evolution and biological
function of trihelix transcription factor gene family in maize.
Materials and Methods
Plant material
From the plant transcription factor database
PlantTFDB (http://planttfdb.cbi.pku.edu.cn/), the nucleic acid and protein
sequences of maize Trihelix transcription factor family gene and Arabidopsis Trihelix transcription
factor family gene for correlation analysis of this study was downloaded (Liu et al. 2015).
Test method
Acquisition
of trihelix transcription factor sequence: The
Trihelix sequences of Arabidopsis and
maize were downloaded from the plant transcription factor database PlantTFDB
(http://planttfdb.cbi.pku.edu.cn/), 34 and 57 amino acid sequences of
transcription factor family proteins were obtained respectively. The Trihelix
protein sequences of maize and Arabidopsis
obtained in the above database include the proteins
translated by multiple transcriptions isoforms
with different Trihelix genes. In this study, the longest transcripts and their
encoded proteins selected by Trihelix gene with multiple transcripts were
analyzed subsequently, and 28 Trihelix gene coding
regions and their proteins of Arabidopsis
were obtained. Sequence and 44 Trihelix gene coding regions and their protein
sequences of maize.
Construction
of phylogenetic tree of transcription factor trihelix gene
Clustal X software was used to carry out multiple
matching analysis on the protein sequences of maize and Arabidopsis. Based on the comparison results, using MEGA5.05 to
build neighbor joining NJ, set Bootstrap as 1000 repetitions and other as
default parameters (Zhao et al. 2015).
Analysis
of conserved domains of amino acid sequences of trihelix transcription factor
family proteins
Using the Pfam Domain pattern redrawer function of
TBtools software, the conservative domain of amino acid sequence of Trihelix
protein in maize was predicted.
Location
of trihelix gene on chromosome
According to the published information of maize
genome B73 RefGen_v3, the distribution of 39 Trihelix transcription factor
family genes on 10 maize chromosomes was determined. The location of Trihelix
gene on chromosome was found by BLSAT comparison in Maize GDB database
(https://www.maizegdb.org/).
Analysis
of physico-chemical properties of amino acids
The number of amino acids, molecular weight,
theoretical isoelectric point, number of aliphatic amino acids and
hydrophobicity of proteins were analyzed by online Protparam tool provided by
ExPASY (https://web.expasy.org/protparam/) (Xie et al. 2014).
Sub-cellular
localization of trihelix
Using Plant-mPLoc (www.csbio. SJTU. Edu. CN), the
location of 44 Trihelix transcription factor family proteins in cells was
predicted (Zhu et al. 2012).
Expression
analysis of trihelix family gene
Based on the published transcriptome data of maize
tissues at different developmental stages, the expression patterns of 39 genes
of Trihelix transcription factor family in different maize tissues and
developmental stages were analyzed. The heat map through the Amazing Heatmap function
in TBtools was drawn.
Results
Identification
of trihelix transcription factors
According to the Trihelix protein identified in
the plant transcription factor database plantTFDB, for the proteins translated
from different transcripts with the same Trihelix gene, the protein with the
longest amino acid sequence was selected for the following analysis. After
screening, 28 Trihelix proteins of Arabidopsis
and 44 Trihelix proteins of maize were obtained, which were AC209784.3, GRMZM2G002978, GRMZM2G016637, GRMZM2G016649,
GRMZM2G021831, GRMZM2G023119, GRMZM2G031493, GRMZM2G037128, GRMZM2G037493,
GRMZM2G037823, GRMZM2G047370, GRMZM2G063203, GRMZM2G080583, GRMZM2G081445,
GRMZM2G084684, GRMZM2G111760, GRMZM2G126148, GRMZM2G134439, GRMZM2G149590,
GRMZM2G153575, GRMZM2G156348, GRMZM2G157219, GRMZM2G162840, GRMZM2G163157,
GRMZM2G169580, GRMZM2G301122, GRMZM2G305362, GRMZM2G314660, GRMZM2G320827,
GRMZM2G326783, GRMZM2G334722, GRMZM2G339957, GRMZM2G375307, GRMZM2G379179,
GRMZM2G380094, GRMZM2G392168, GRMZM2G414159, GRMZM2G415229, GRMZM2G427087,
GRMZM2G428470, GRMZM2G469873, GRMZM2G481163, GRMZM5G818655 and GRMZM5G850092.
Phylogenetic
analysis of trihelix gene in maize and Arabidopsis
thaliana
The 28 Trihelix genes from Arabidopsis and 44 Trihelix genes from maize were sequenced by
ClustalW and the phylogenetic tree was established. Results showed that
Trihelix transcription factors of maize and Arabidopsis
can be divided into five subfamilies, named GT-1 subfamily, GT-2 subfamily,
SIP1 subfamily, GT γ subfamily and SH4 subfamily respectively (Fig. 1).
Among them, GT-1 subfamily has 6 members, GT-2 subfamily; 11 members, SIP1
subfamily; 9 members, GT γ subfamily; 9 members and SH4 subfamily also has
9 members. It was found that AT1g54060 and AT3g14180 in Arabidopsis regulated seed development (Zhou et al. 2015). These two genes are located in SIP1 subfamily,
hence, it is speculated that the genes in SIP1 subfamily may have the function
of regulating seed development. In GT-2 subfamily, Arabidopsis AT1g33240 (GTL1) is related to the development
of epidermal hair, and has the function of water conservation under drought
stress. Therefore, the gene of GT-2 subfamily may be related to the formation
of maize stem, leaf and organ. It can reduce transpiration and keep water under
drought condition, but the specific function needs to be further verified.
Fig. 1:
Phylogenetic analysis of Trihelix gene in maize and Arabidopsis
Fig. 2: Conserved domains of
Trihelix amino acid sequence in maize
Analysis
of conserved domain of trihelix transcription factor family protein sequence
Conservative domain is a kind of highly conserved
domain in the process of biological evolution. The analysis of the conserved
domain of the amino acid sequence of Trihelix protein in maize showed that all
44 Trihelix transcription factors in maize contained Myb_DNA-bind_4 domain
(Fig. 2). Some of them also contain the domains of Fasciclin, MADF_DNA_bdg,
AA_kinase, Myb_DNA-bind_6, Myb_DNA-binding and RMMBL. Myb_DNA-bind_4, Myb_DNA-bind_6
and Myb_DNA-binding are different forms of the same domain. MYB transcription
factors are involved in regulating the growth and development of various organs and tissues. Previous studies have found that MYB
transcription factor related genes are expressed in roots, stems, leaves,
flowers, fruits and other organs and tissues of plants (Niu et al. 2016). Therefore, it is
speculated that the functions of Trihelix transcription factor family are all
regulatory genes.
Location analysis
of trihelix gene on chromosome
Based on the B73_ref_v4 information of maize
genome, the length of 39 genes of Trihelix transcription factor family was
determined (Table 1), and analyzed their distribution on 10 maize chromosomes
(Fig. 3). The distribution of these 39 Trihelix transcription factor family
members on 10 chromosomes of maize is not uniform, including 4 genes on
chromosome 1; 5 genes on chromosome 2, 3, 4 and 10; 6 genes on chromosome 5; 2
genes on chromosome 6 and 9; 1 gene on chromosome 7; 3 genes on chromosome 8
Stripe gene (Fig. 3).
Analysis
of physical and chemical properties of trihelix transcription factor family
proteins
The amino acid composition and physico-chemical
properties of different Trihelix transcription factor family proteins are
different, and the amino acid number, molecular weight, theoretical isoelectric
point, fat coefficient, and hydrophilic average coefficient are quite different
in different Trihelix transcription factors. As shown in Table 2, the maximum
number of amino acids is Trihelix 21, up to 1021; the minimum is Trihelix 40,
up to 206; the maximum number of fatty amino acids is Trihelix 1, up to 83.65;
the minimum number of fatty amino acids is Trihelix 4, only 50.58. The proteins
of Trihelix transcription factor family in maize contain
both acid amino acids and basic amino acids. The molecular weight of amino
acids is between 24343.26 and 110243.1, most of which are neutral and basic.
The average coefficient of hydrophilicity is only negative but not positive,
which indicates that all the transcription factor family proteins are
hydrophilic rather than hydrophobic. Fat coefficient can be used as an index of
protein stability. Generally, the higher fat coefficient is, the higher protein
stability. It was found that the fat coefficient of Trihelix transcription
factor family was between 48-83, hence was
speculated that the stability of Trihelix transcription factor family was poor.
This specific situation needs further study.
Table
1:
Length of Trihelix gene
Gene |
Locus |
Gene location |
Trihelix1 |
AC209784.3 |
chr3
181108342..181111529 |
Trihelix2 |
GRMZM2G002978 |
chr2
59356652..59361967 |
Trihelix3 |
GRMZM2G016637 |
chr6
25704007..25705812 |
Trihelix4 |
GRMZM2G016649 |
chr2
21790379..21794847 |
Trihelix5 |
GRMZM2G021831 |
chr2
45778700..45780304 |
Trihelix6 |
GRMZM2G023119 |
chr1
122580368..122582737 |
Trihelix7 |
GRMZM2G031493 |
chr3
156798288..156800105 |
Trihelix8 |
GRMZM2G037128 |
chr4
240522538..240525859 |
Trihelix9 |
GRMZM2G037493 |
chr1
186468875..186472999 |
Trihelix10 |
GRMZM2G037823 |
chr5
170970565..170973058 |
Trihelix11 |
GRMZM2G047370 |
chr10
126489799..126493558 |
Trihelix12 |
GRMZM2G063203 |
chr4
149896373..149900088 |
Trihelix13 |
GRMZM2G080583 |
chr3
209734160..209736175 |
Trihelix14 |
GRMZM2G081445 |
chr2 2477288..2480012 |
Trihelix15 |
GRMZM2G084684 |
chr5
165851118..165855227 |
Trihelix16 |
GRMZM2G111760 |
chr5
67179847..67182803 |
Trihelix17 |
GRMZM2G126148 |
chr4
214285333..214292130 |
Trihelix18 |
GRMZM2G134439 |
chr5
98271643..98275405 |
Trihelix19 |
GRMZM2G149590 |
chr10
111290454..111310709 |
Trihelix20 |
GRMZM2G153575 |
chr2
198399758..198404962 |
Trihelix21 |
GRMZM2G156348 |
chr2
12096511..12099684 |
Trihelix22 |
GRMZM2G157219 |
chr6
164197746..164205689 |
Trihelix23 |
GRMZM2G162840 |
chr4
95679251..95683955 |
Trihelix24 |
GRMZM2G163157 |
chr8
150144895..150146384 |
Trihelix25 |
GRMZM2G169580 |
chr5
190240849..190244560 |
Trihelix26 |
GRMZM2G301122 |
chr10
8797221..8799613 |
Trihelix27 |
GRMZM2G305362 |
chr8
39016488..39018390 |
Trihelix28 |
GRMZM2G314660 |
chr1 3077768..3082278 |
Trihelix29 |
GRMZM2G320827 |
chr2
21267618..21268758 |
Trihelix30 |
GRMZM2G326783 |
chr9
134037126..134043118 |
Trihelix31 |
GRMZM2G334722 |
chr5
86823953..86848300 |
Trihelix32 |
GRMZM2G339957 |
chr8
155242721..155246236 |
Trihelix33 |
GRMZM2G375307 |
chr7
145738119..145742498 |
Trihelix34 |
GRMZM2G379179 |
chr1
182354881..182356502 |
Trihelix35 |
GRMZM2G380094 |
chr5
175054039..175055248 |
Trihelix36 |
GRMZM2G392168 |
chr10
119916058..119917843 |
Trihelix37 |
GRMZM2G414159 |
chr5
22100008..22104260 |
Trihelix38 |
GRMZM2G415229 |
chr10
141020598..141023637 |
Trihelix39 |
GRMZM2G427087 |
chr10 134039236..134040599 |
Trihelix40 |
GRMZM2G428470 |
chr9
114551277..114553268 |
Trihelix41 |
GRMZM2G469873 |
chr4
113063854..113066335 |
Trihelix42 |
GRMZM2G481163 |
chr1
94880052..94881644 |
Trihelix43 |
GRMZM5G818655 |
chr3
57990230..57991817 |
Trihelix44 |
GRMZM5G850092 |
chr4 196983547..196984915 |
Table 2:
Analysis of physical and chemical properties and subcellular localization of
Trihelix transcription factor family proteins
Gene |
Locus |
Amino acid number |
Molecular weight |
Theoretical isoelectric point |
Fat coefficient |
Average coefficient of hydrophobicity |
Predicted location |
Trihelix1 |
AC209784.3 |
682 |
72410.16 |
9.61 |
83.65 |
-0.152 |
Cell membrane. Nucleus. |
Trihelix2 |
GRMZM2G002978 |
519 |
55331.10 |
7.19 |
69.79 |
-0.438 |
Chloroplast. |
Trihelix3 |
GRMZM2G016637 |
335 |
36762.77 |
5.95 |
61.58 |
-0.805 |
Nucleus. |
Trihelix4 |
GRMZM2G016649 |
774 |
83274.20 |
5.90 |
50.58 |
-0.882 |
Nucleus. |
Trihelix5 |
GRMZM2G021831 |
439 |
46481.48 |
8.87 |
53.08 |
-0.803 |
Nucleus. |
Trihelix6 |
GRMZM2G023119 |
210 |
23061.93 |
10.02 |
56.24 |
-0.796 |
Nucleus. |
Trihelix7 |
GRMZM2G031493 |
277 |
30181.88 |
8.94 |
67.15 |
-0.570 |
Nucleus. |
Trihelix8 |
GRMZM2G037128 |
669 |
72502.03 |
5.91 |
81.08 |
-0.311 |
Nucleus. |
Trihelix9 |
GRMZM2G037493 |
714 |
76269.47 |
5.93 |
52.59 |
-0.862 |
Nucleus. |
Trihelix10 |
GRMZM2G037823 |
214 |
24343.26 |
8.74 |
61.67 |
-0.742 |
Nucleus. |
Trihelix11 |
GRMZM2G047370 |
405 |
46187.92 |
5.91 |
68.91 |
-0.896 |
Nucleus. |
Trihelix12 |
GRMZM2G063203 |
379 |
41935.71 |
6.28 |
63.11 |
-0.727 |
Nucleus. |
Trihelix13 |
GRMZM2G080583 |
668 |
71709.60 |
5.78 |
53.8 |
-0.758 |
Nucleus. |
Trihelix14 |
GRMZM2G081445 |
318 |
34724.07 |
9.59 |
63.08 |
-0.750 |
Nucleus. |
Trihelix15 |
GRMZM2G084684 |
381 |
40870.93 |
9.38 |
69.87 |
-0.640 |
Nucleus. |
Trihelix16 |
GRMZM2G111760 |
366 |
38952.08 |
5.01 |
71.53 |
-0.589 |
Nucleus. |
Trihelix17 |
GRMZM2G126148 |
664 |
70652.29 |
5.61 |
54.04 |
-0.796 |
Chloroplast. |
Trihelix18 |
GRMZM2G134439 |
436 |
49782.63 |
6.47 |
59.79 |
-1.059 |
Nucleus. |
Trihelix19 |
GRMZM2G149590 |
510 |
56488.55 |
8.81 |
78.22 |
-0.454 |
Nucleus. |
Trihelix20 |
GRMZM2G153575 |
334 |
36440.24 |
5.89 |
66.95 |
-0.794 |
Nucleus. |
Trihelix28 |
GRMZM2G314660 |
533 |
57191.20 |
6.09 |
58.91 |
-0.727 |
Nucleus. |
Trihelix29 |
GRMZM2G320827 |
725 |
76401.90 |
6.73 |
51.71 |
-0.732 |
Chloroplast. |
Trihelix30 |
GRMZM2G326783 |
208 |
22949.16 |
11.09 |
66.35 |
-0.682 |
Nucleus. |
Trihelix31 |
GRMZM2G334722 |
673 |
76473.17 |
9.57 |
75.23 |
-0.447 |
Nucleus. |
Trihelix32 |
GRMZM2G339957 |
387 |
40507.55 |
4.55 |
70.26 |
-0.522 |
Nucleus. |
Trihelix33 |
GRMZM2G375307 |
350 |
38799.78 |
9.7 |
61.71 |
-0.847 |
Nucleus. |
Trihelix34 |
GRMZM2G379179 |
337 |
36717.50 |
6.94 |
69.08 |
-0.631 |
Nucleus. |
Trihelix35 |
GRMZM2G380094 |
319 |
35873.99 |
5.6 |
60.75 |
-0.966 |
Nucleus. |
Trihelix36 |
GRMZM2G392168 |
402 |
42967.31 |
7.15 |
58.41 |
-0.805 |
Nucleus. |
Trihelix37 |
GRMZM2G414159 |
392 |
42106.22 |
6.61 |
54.16 |
-0.846 |
Nucleus. |
Trihelix38 |
GRMZM2G415229 |
776 |
82452.12 |
6.11 |
48.45 |
-0.830 |
Nucleus. |
Trihelix39 |
GRMZM2G427087 |
271 |
31896.87 |
8.94 |
58.38 |
-1.204 |
Chloroplast. |
Trihelix40 |
GRMZM2G428470 |
206 |
22628.80 |
11.19 |
68.88 |
-0.657 |
Nucleus. |
Trihelix41 |
GRMZM2G469873 |
317 |
33468.76 |
9.17 |
69.15 |
-0.466 |
Nucleus. |
Trihelix42 |
GRMZM2G481163 |
398 |
45440.35 |
5.97 |
73.54 |
-0.814 |
Nucleus. |
Trihelix43 |
GRMZM5G818655 |
321 |
34106.44 |
9.41 |
65.26 |
-0.567 |
Nucleus. |
Trihelix44 |
GRMZM5G850092 |
528 |
56690.91 |
7.38 |
61.31 |
-0.722 |
Nucleus. |
Subcellular
localization of trihelix transcription factor
We use the online tool Plant-mPLoc (http://www.csbio.sjtu.edu.cn/bioinfo/plant-multi/) to
predict subcellular localization (Zhu et al. 2012). Results showed that the Trihelix family of
transcription factors are basically located in the nucleus, in which Trihelix 1
is present in both the nucleus and the cell membrane; Trihelix 2, Trihelix 17,
Trihelix 29 and Trihelix 39 are present in the chloroplast (Table 2). In
conclusion, the Trihelix family of transcription factors plays a major role in
the nucleus, which may have transcriptional regulation function.
Tissue-specific
expression of trihelix in maize
We analyzed the expression of 39 Trihelix genes in
different stages of maize development by using the transcriptome sequencing
data released by Stelpflug et al. (2016) and drew a heatmap based on the
FPKM value of each gene in each stage of maize development. The tissues
analyzed include germinated seeds, different
Fig. 3:
Location of Trihelix transcription factor family genes on different chromosomes
of maize
Fig. 4:
Expression map of Trihelix gene in different tissues of maize
regions of roots, seedlings, stems at different
positions, apical meristem of stems, leaves, internodes, spikes, anthers, and
filaments (maize whiskers) at different stages of development. The expression
pattern of Trihelix transcription factor family gene is different in different
maize tissues and development stages (Fig. 4). Most of the genes were highly
expressed in different tissues and periods, except GRMZM2G037493,
GRMZM2G031493, GRMZM2G326783 and GRMZM5G818655. At the stage of Anthers R1,
GRMZM2G021881 expression level was increased. The overall expression of
GRMZM2G149590, GRMZM2G149590.2, AC207984.3_FG011 and GRMZM2G016637 was also
relatively low. Compared with the overall expression level, expression of
GRMZM2G375307, GRMZM2G481163 and GRMZM2G320827 were highest. Compared with the
overall expression level, the five genes, GRMZM2G157219, GRMZM2G427087, GRMZM2G002978,
GRMZM2G428470 and GRMZM2G334722, were also expressed higher. The overall
expression of GRMZM2G469873, GRMZM2G339957, GRMZM2G379179,
GRMZM2G037823, GRMZM2G850092, GRMZM2G162840, GRMZM2G080583, GRMZM2G380094,
GRMZM2G392168, GRMZM2G301122 and GRMZM2G414229
were also high. The expression levels of GRMZM2G01649, GRMZM2G414159,
GRMZM2G037128 and GRMZM2G314660 were significantly increased in meiosis and
root formation.
Discussion
Transcription factors play an important role in
plant growth, development and response to changes in the external environment,
and are the key to regulate various physiological activities (Zhu et al. 2019). In recent years, many
transcription factors related to drought, high salt, low temperature, hormone,
pathogen response and development have been isolated from plants. It has been
found that the over-expression of some transcription factors can enhance the
resistance and adaptability of plants to stress by transgenic means (Zhuang et al. 2009; Liu et al. 2010).
Trihelix transcription factor
family plays an important role in plant growth and development and response to
stress (Zhou et al. 2017). It is involved in plant growth and development,
including light response gene regulation, flower organ morphogenesis and
response to stress, including abiotic stress such as cold damage, drought, high
salt and biological stress such as pathogen stress (Liang et al. 2017). In this
study, 44 Trihelix sequences were screened from the Trihelix transcription
factor family of maize by bioinformatics analysis, which is more than 28
Trihelix sequences of Arabidopsis. It
is suggested that the expansion of Trihelix gene may be to make maize better
adapt to some environments and then to develop evolutionary characteristics. By
comparing the physical and chemical properties of Trihelix transcription factor
protein, it was found that the number of acid amino acids in 44 Trihelix
transcription factor proteins was more than basic amino acids. There are only
hydrophilic proteins in this gene family, and the molecular weight difference
between each gene is large, indicating that Trihelix transcription factor
family protein is relatively rich.
In this study, the distribution
relationship of Trihelix transcription factors in maize was discovered by
evolutionary tree. It was found that the members of Trihelix gene family
involved in seed development were located in SIP1 subfamily, and the members
involved in abiotic stress were mostly located in GT-2 subfamily, indicating
that the function and classification of Trihelix transcription factors in maize
were not significantly related (Li et al. 2015). In the conservative domain analysis, it was found that
each member of the Trihelix transcription factor family has the same domain,
but some members also have different conservative domains, suggesting the
diversity of gene function. According to the expression analysis, GRMZM2G016649, GRMZM2G414159, GRMZM2G037128 and GRMZM2G314660 were expressed in a large number in
meiosis and root formation, suggesting that they play an important role in the
seed development of plants.
Conclusion
The Trihelix transcription factor family in maize
was identified by bioinformatics and will provide some basic data for further
utilization of Trihelix transcription factors in maize breeding.
Acknowledgements
The authors acknowledge the Scientific Research
Project fund of Jilin Provincial Education Department (JJKH20190979KJ), Science
and Technology Innovation Development Project of Jilin City (#201831781 to
X.Y.), Natural Science Foundation of Jilin Province of China (#20180101233JC to
Z.-Y.X.) and Doctor Talent Research Foundation of Jilin Agricultural Science
and Technology University (#20185002 to L. J.).
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