Research Article

Identification of Genes Related to the Key Regulatory Circuit of Circadian Clock in Legume Plant  

Zongfei Li1,2,3,4 , Mengdie Cai1,2 , Zhenpeng Liu1 , Jie Zhang1,2 , Fang Wei1,2 , Xuanjun Fang1,2,3,4
1 Institute of Life Science, Jiyang College of Zhejiang A&F University, Zhuji, 311800, China
2 Cuixi Academy of Biotechnology, Zhuji, 311800, China
3 Hainan Institute of Tropical Agricultural Resources, Sanya, 572025, China
4 College of Life Sciences and Technology, Guangxi University, Nanning, 530005, China
Author    Correspondence author
Legume Genomics and Genetics, 2017, Vol. 8, No. 1   doi: 10.5376/lgg.2017.08.0001
Received: 28 Feb., 2017    Accepted: 28 Mar., 2017    Published: 15 Apr., 2017
© 2017 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Li Z.F., Cai M.D., Liu Z.P., Zhang J., Wei F., and Fang X.J., 2017, Identification of genes related to the key regulatory circuit of circadian clock in legume plant, Legume Genomics and Genetics, 8(1): 1-11 (doi: 10.5376/lgg.2017.08.0001)

Abstract

In order to reveal the evolution of the circadian clock regulation network in legume of three species (Medicago truncatula, Lotus japonicus and Glycine max). We find the regulation factor of the circadian clock of Arabidopsis thaliana through the Geneontology (GO), at the same time, according to the relevant literature, the regulation factor was supplemented and verified. Then regulation factor was obtained at the genome-wide level and Medicago truncatula, Lotus japonicus and Glycine max in the three species for comparison, identification of the corresponding direct homologous gene, analysis of the conserved functional domains, multiple sequence alignment, phylogenetic tree construction and evolution analysis and gene re-annotation. This study identified 108 Glycine max circadian clock related candidate genes, 51 Lotus japonicus circadian clock related candidate genes, 34 Medicago truncatula circadian clock related candidate genes. We selected LHY/CCA1, PRR and CHE genes from the candidate genes of the identified orthologous genes to construct 3 molecular phylogenetic trees, analysis showed that the circadian clock regulation pathway in Arabidopsis and legume of the three species occurred different degree of differentiation, especially in some key components such as direct homologous gene of the circadian clock regulates and the key genes of the florescence control. It has certain guidance and reference value for the researching of the circadian clock control network of the legume in the experimental stage.

Keywords
Legume; Circadian clock; Regulation; Gene; Identification

Introduction

The transcription network regulated by C-repeat-binding factors (CBFs) plays important role for increased freezing and drought tolerance in plants (Jaglo et al., 2001; Hsieh et al., 2002), the CBF pathway is transiently induced by cold and transitive downstream genes by binding to the CRT/DRE motif (CCGAC) in target gene promoters with the conserved AP2/EREBP DNA binding domain (Liu et al., 1998). Previous reports have indicated that overexpression of the Arabidopsis CBF1(AtCBF1) gene in transgenic Arabidopsis induced the expression of multiple CRT/DRE-containing genes and resulted in an increase in freezing and drought tolerance in both non-acclimated and cold-acclimated plants (Liu et al., 1998; Kasuga et al., 1999), similar results were observed with the constitutive overexpression of the AtCBF1 gene in transgenic brassica napus, sweet cherry, potato, tobacco, poplar, strawberry and eucalyptus plants (Jaglo et al., 2001; Kitashiba et al., 2004; Pino et al., 2008; Benedict et al., 2006; Navarro et al., 2011), the results indicate that transformation of AtCBF1 gene may represent a strategy in freezing tolerance breeding for freezing-sensitive crops.

 

Banana (Musa sp.) is the fourth important global food crop after rice, wheat and maize in terms of gross value of production (Tripathi et al., 2004). It is widely cultivated in the tropical regions, and some south subtropical regions such as Yunnan, Guangxi and Guangdong province in China, are also engaged heavily in the production of banana. But banana is extraordinary sensitive to low-temperature, when the temperature decreases to 8°C, banana growth is arrested in the interior of the pseudostem and injury occurs (Zhang et al., 2011). Periodic cold stresses during winter or early spring are the main environmental constraints to the banana industry in south subtropical regions; enormous economic losses were incurred each year due to cold injuries (Kang et al., 2003). Therefore, genetic improvement on freezing tolerance is one of the major breeding goals of banana, especially for the banana cultivation in China. However, the most important commercial banana cultivars are triploid and sterile, and no true cold–resistant germplasm is available although plantain is relatively colder tolerant (Zhang et al., 2011), it is very difficult to obtain cold-resistant cultivars through conventional breeding methods. Genetic engineering is obviously the best choice for banana breeding, transgenic technology allows the target plants to obtain wanted gene (s) immediately, avoiding a long period of the selection process involved in conventional breeding practice.

 

The aim of this study was to introduce the AtCBF1 gene into banana, and determine whether introgression AtCBF1 enhanced chilling stress tolerance in transgenic banana. Our study led to further development of molecular responses in Musa to colds tress and establishes a foundation for cloning cold resistance relative genes in Musa.

 

1 Results

1.1 Sequence alignment to identify the homologous sequences of species

We get 52 genes by retrieving the model plant Arabidopsis thaliana's circadian clock, circadian clock regulation, circadian clock input and other related GO terms, some of which had a plurality of the GO annotation. Removed multiple annotated genes, we could get 42 genes related to the circadian regulation network. Added 8 genes which we got from other literatures, we received a total of 50 clock related genes in arabidopsis. The 50 genes basically cover the 3 parts of the circadian clock control network of Arabidopsis, including the circadian clock input of the optical signal input, the central oscillator, and some physiological activities of the circadian clock regulation.

 

We compared the sequence similarity between protein sequences of Arabidopsis thaliana and 3 species of legume species on the whole genome level (Table 1). The "Orthologs" term represents the number of circadian clock control network related genes in Arabidopsis thaliana in direct candidate genes of various species, the full-length ORF term represents the number of full-length ORF candidate genes, and the "F-PUT" term represents the number of genes that are covered by the PUT sequence in the full-length ORF. A total of 108 circadian clock regulatory network related candidate genes were identified in Glycine max, including 95 full-length ORF and 66 of full-length PUT sequence ratio. In Medicago truncatula, we identified circadian clock regulation network related candidate genes was 34 in all, including 33 full-length ORF. However, only 7 genes had PUT sequence ratio in all full-length ORF candidate genes. In Lotus japonicus, the number of circadian regulation network related candidate genes was 51, in which were 25 full-length ORF, and the proportion full-length PUT sequence was only 7.

 

 

Table 1 Comparison of 50 candidate genes from the three leguminous plants

 

From the general situation, the network related genes in Arabidopsis thaliana are the largest number of candidate genes in these 3 species of legumes, which may be related to the origin of the Glycine max. At the same time, the number of candidate genes with full-length PUT sequence coverage in Glycine max also far more than the number of the corresponding genes in Lotus japonicus and Medicago truncatula. This is probably due to the EST resources of Glycine max EST database more than Medicago truncatula and lotus EST database.

 

The 12 genes, PRR9,PHYC,PHYD,LKP2,FSD1 (fe superoxide dismutase 1),KAT2 (potassium channel in Arabidopsis thaliana 2),LCL,FLC (flowering locus c),ARR4 (response regulator 4),CHE,CO,COL1(CONSTANS-LIKE 1), related to circadian clock control network in Arabidopsis thaliana, which were not found a direct candidate gene in in these 3 species of legumes. For these 12 genes, their orthologous genes have been lost during the long-term evolution of legume. Therefore, these 12 genes may be an important event caused by legume and cruciferous differentiation.

 

1.2 Identification of the direct candidate genes of LHY/CCA1 in legume

LHY and CCA1 are a class of Myb type R1 transcription factors whose expression is positively regulated by TOC1. Its highest peak expression is in the day and it is a negative regulator of the central oscillator of the circadian clock. In the night, LHY/CCA1 was inhibited by PIF3 (phytochrome interactingfactor3). PIF3 combines with G-box of CCA1, LHY and other gene promoter regions, and then to inhibit the expression of these genes. While after red light irradiation, PHYB is activated and go from the cytoplasm into the nucleus to combine with PIF3, then release the inhibition of PIF3 on CCA1, LHY and other genes. And further induced gene expression in the lower reaches of the gene and inhibited the expression of night time gene. LHY combines with the night element (AAATATCT) of TOC1 and other night genes to inhibit its transcriptional expression. During the day, the decrease of CCA1/LHY expression level can gradually release its inhibitory effect on TOC1, which makes the mRNA expression of TOC1 increased. When the expression of TOC1 reached a certain amount of time, it will positively regulate the expression of CCA1 and LHY, which makes the expression of CCA1 and LHY increased, thus forming a physiological cycle of oscillation. Therefore, in the regulatory pathway composed of CCA1/LHY and TOC1 constitute in Arabidopsis thaliana, TOC1 positively regulates the expression of LHY/CCA1 firstly. When the LHY/CCA1 reaches a certain amount of expression, it will be negatively inhibit the expression of TOC1. According to this model, MYB transcription factors CCA1 and LHY, as negative regulatory elements of transcriptional regulator, can be directly incorporated into the promoter region of TOC1. However, the positive regulation of TOC1 on the expression of CCA1 and LHY is not direct.

 

LHY are found in 2 direct homologous gene fragments located on the same chromosome in Lotus japonicus and Medicago truncatula, and 4 direct homologous genes are found in Glycine max (Table 2). In the lotus, 2 predicted gene segments were chr3.CM0208.430.nd and chr3.CM0208.410.nd respectively. In Medicago truncatula, these two forecast gene fragments were AC150443_50 and AC150443_49 respectively. Between the 2 genes of Lotus japonicus are 2 gene fragments of Medicago truncatula, but these 2 gene fragments cannot be spliced into a complete gene. It can be seen through comparing with the LHY gene, Chr3.CM0208.410.nd and AC150443_49 correspond to the HTH conserved domains of the LHY gene, while chr3.CM0208.430.nd and AC150443_50 correspond to the rest of the LHY gene. There may be 2 reasons in this case. One is the genomic information is not complete, which made the note divide 1 genes into 2 genes mistakenly. The other is that in alfalfa, between the HTH conserved domain and the rest part of the LHY gene to insert a fragment, which led to the loss of function of LHY gene in Medicago. We took the 4 gene fragments to compare with the EST library of Lotus japonicus and Medicago truncatula respectively. The results showed that the majority of AC150443_49 and AC150443_50 have correspondence EST, while chr3.CM0208.410.nd did not find the corresponding EST and only part of chr3.CM0208.430.nd region has the corresponding EST. We took chr3.CM0208.430.nd and AC150443_50 respectively as representatives of Lotus japonicus and Medicago truncatula LHY gene to build phylogenetic trees. But the location of chr3.CM0208.430.nd and AC150443_50 in the evolutionary tree can only serve as a reference.

 

 

Table 2 LHY in the direct candidate ortholog genes in three species of Legume

 

4 candidate genes of the LHY genes in Glycine max are all full-length, the similarity with LHY is 42% or more than 42% and the full-length of the 4 genes are covered by PUT sequence. However, GmLHY1 and GmLHY2 correspond to the same PUT sequence, GmLHY3 and GmLHY4 correspond to the same PUT sequence. And the similarity of GmLHY2 and PUT sequence is greater than the similarity of GmLHY1 and PUT sequence, the similarity of GmLHY3 is greater than the similarity of GmLHY4. Therefore, there were at least 2 GmLHY gene expressed in Glycine max.

 

LHY gene and CCA1 gene were both belong to R1 class MYB transcription factor, and were paralogous gene with each other. The HTH conserved domain of LHY protein is very obvious. It was worth noting that the CDD domain analysis in NCBI named the conserved region of the LHY protein as the SNAT domain. The comparison results of Pfam database showed that this domain was HTH conserved domain. In conclusion , this study named the domain as HTH. The HTH domain and the SNAT domain belong to the conserved domain of MYB transcription factor family. The difference is that the HTH domain is bound to a specific region of DNA, while the SNAT domain is the identification region of protein interaction. According to the comparison results of Pfam and the results of Figure 1, in addition to the highly conserved region of HTH, the corresponding 93 to 473 of the LHY protein from Arabidopsis thaliana was also relatively conserved, which corresponded to the 120568 structure in the B Pfam database. It can be seen from the amino acid sequence alignment, the HTH domain is very important to keep the function of LHY. It is also very conservative in this area even before the separation of leaf plants and dicotyledonous plants, the CCA1 gene of Arabidopsis have already been separated with LHY genes. The situation of Medicago truncatula is a special case. In its annotation information, the reason why the missing HTH domain in LHY gene is not clear for now. There may be an error in the annotation information,or the LHY itself has some form of mutation that led to the inactivation of the LHY gene.

 

 

Figure 1 The LHY conservation domain, sequences alignment figures, molecular phylogenetic tree and evolutionary distance

Note: A: LHY conservation domain analysis; B: LHY sequences alignment; C: Molecular evolution tree of LHY proteins; D: The distance of LHY protein bewteen four species

 

1.3 Identification of candidate genes of PRR family

The PRR (pseudo-response regulator)family of Arabidopsis thaliana is closely linked with the circadian clock. PRR1 (aka TOC1), 3, 5, 7, 9 is known as the circadian clock five quartets, which played important roles in controlling the rhythm of the circadian clock. In addition, PRR2 also played a role in the circadian clock of Arabidopsis thaliana. The direct homologous gene of PRR9 was not found and there werer more homologous genes of PRR5 in legume. On the basis of molecular evolutionary tree, part of the PRR5 candidate gene of Medicago truncatula and Glycine max did not correspond to Arabidopsis thaliana genes (Figure 2). it need further research for the mutation of the number of PRR genes whether five quartets of the Arabidopsis changed into a trio and seven quartets needed furth research. In the Arabidopsis thaliana PRR family, the genetic relationship among PRR1, PRR2, PRR3, PRR5, PRR7, and PRR9 is far away. The results showed that PRR gene have an effect on the circadian clock, a phase and amplitude, flowering time and sensitivity to extend the control of hypocotyl red. PRR transcript accumulates regularly and the order is PRR9-PRR7-PRR5-PRR3-TOC1. Its highest peak appeared in 2 hours to 10 hours after dusk, from PRR9 to TOC1. Studies have indicated that PRR is involved in the optical signal input pathway in the physiological pathway of circadian clock, but it is not necessary for producing a rhythmic oscillation of the circadian clock. PRR7 and PRR9 genes of Arabidopsis thaliana also played roles in temperature mediated circadian clock system, and the functions of the two had overlap.

 

 

Figure 2 Conserved domain analysis of CHE protein

 

We can see from the conserved domain analysis and the homology sequences alignment diagram, plant class PRR genes have two conserved regions, namely the REC region and the CCT region (Figure 3). The REC region is composed of 2 parts, one is the histidine protein kinase, which contains the phosphorylation site, the other is a response regulator protein, including the recognition sites of molecular interactions and might be in homologous gene or being dimerization site by itself. CCT region exists in the C- side of PRR and is responsible for the transfer of light signal. CCT region and B-BOX type zinc finger structure, GATA type zinc finger structure, as well as the REC structure to regulate the plant light signal transduction pathway. So, the conserved regions of the CCT are also present in other proteins of the light signaling pathway, such as CO, COL protein.

 

 

Figure 3 Conserved functional domain analysis, amino acid alignment, molecular evolution tree and evlutional distance of PRR proteins

Note: A: Conserved functional domain analysis of PRR protein; B: PRR amino acid sequences alignment; C: Molecular evolution tree of PRR proteins; D: The distance of PRR protein between four species

 

PRR1 and PRR5 did not find direct candidate ortholog genes in Medicago truncatula.. PRR7 and PRR2 each had a direct homologous gene and PRR2 had two direct candidate ortholog genes in medicago truncatula. These 4 direct candidate ortholog genes partial expressed in Medicago truncatula.

 

PRR1 had 1 direct candidate ortholog gene, while PRR2, PRR5 and PRR7 each had 2 direct candidate ortholog genes in Lotus japonicus, in which only part of PRR1 expressed in Lotus japonicus.

 

PRR1 and PRR2 each had 4 direct candidate ortholog genes in Glycine max, PRR5 had 5 orthologous candidate gene in Glycine maxs, PRR7 had 3 orthologous candidate genes in Glycine max. PRR3’s orthologous candidate gene is distantly related in Glycine max.

 

In 4 PRR1 genes of Glycine max, GmPRR1a and GmPRR1b were clustered into one class, GmPRR1c and GmPRR1d were clustered into one class. One of the prominent features of GmPRR1c was the loss of some active sites and phosphorylation sites in the conserved domain of REC. This evolutionary event occured in the separation of GmPRR1c and GmPRR1d. The structure mutations might cause the GmPRR1c lost the biological activity function and mutate into a false gene. And it may also be a result of another evolution. The ancestral genes of GmPRR1c and GmPRR1d occurred subfunctional after the replication, it made the loss of part of the GmPRR1c activity. However, there are also retain recognition sites and dimerization sites interacted with other molecules. It may be associated with other GmPRR1 to form a two dimers, which played a supporting role. It can be seen that the evolutionary distance of GmPRR1c and GmPRR1d (0.096) was far greater than the evolutionary distance of GmPRR1a and GmPRR1b (0.052) from Table 3, which indicated that the time of separation of GmPRR1c and GmPRR1a was much longer than that of GmPRR1d and GmPRR1b and meaned that the selective pressure GmPRR1a and GmPRR1b facing was greater than that of GmPRR1c and GmPRR1d facing. This can also be seen from homologous sequences associated with pictures (Figure 3). Several domain missing occurred in the  GmPRR1d and GmPRR1c, suggesting that they faced the less selected pressure.

 

 

Table 3 The direct candidate ortholog genes of PRR gene family in three species of Legume

 

1.4 Identification of candidate genes of CHE family

CHE is a member of the TCP family of transcription factors. Previous studies have found that when CCA1 and LHY are accumulated to a certain degree, they can inhibit the expression of TOC1 by directly binding to the promoter region of TOC1. However, it did not found that the relevant functional domain to regulate the expression of LHY and CCA1 in the TOC1 protein (Figure 2). In order to solve this problem, Pruneda-Paz et al. (2009) using yeast one hybrid technology to screen transcription factors associated with LHY and CCA1 gene regulation. The results showed that the TCP transcription factor I family specific binding to the region, which is a length of about 171bp, named CHE and in the front of CCA1 gene start codon. But the CHE protein did not bind to the LHY gene related region. The sequence of CHE protein binding CCA1 gene region was GGNCCCAC, which was named as TBS. Further studies showed that during the day, CCA1 and LHY were highly expressed to promote CHE expression, while in the night, the amount of CHE expression increased, and the amount of LHY and CCA1 expression was inhibited to a minimum. At the end of the day, TOC1 would be combined with the CHE to restart the next cycle.

 

CHE gene did not find the CHE direct candidate ortholog gene in 3 species in the legume. The relationship between Glycine max, Medicago truncatula, Lotus japonicus and CHE closest homologous genes were respectively AC151824_21, chr5.CM1439.250.Nd and Glyma10g43190. Their direct homology in Arabidopsis thaliana was all AT5G23280. This suggested that AT5G23280 may be replaced by CHE in the legume to regulate the expression of CCA1, or AT5G23280 regulates the expression of LHY in the pea family.

 

2 Discussion

In this study, we analyze the circadian clock control network of the Legume through the biological information method. 50 key genes of the circadian clock regulatory network were obtained by using Geneontology (GO) annotation in Arabidopsis thaliana and the latest literature. It involed the input part of the circadian clock, such as the light and the temperature, the central oscillator and the output of the circadian clock, etc.. We have identified candidate genes related to the circadian clock of 108 Glycine max, 51 candidate genes related to the circadian clock of Lotus japonicus and the circadian clock of candidate genes related to 34 Medicago truncatula.

 

We selected LHY/CCA1, PRR and CHE genes from the identified direct homologous genes to construct three molecular phylogenetic trees. The function and evolution trend of these genes were analyzed in combination with the results of functional domain and multiple sequence alignment. Our analysis showed that the circadian clock regulation pathway had differentiation in these 3 species of the Arabidopsis thaliana and legume, especially in some key components such as the core components of the circadian clock control and the key genes of controlling the flowering period. Take the Arabidopsis thaliana as a reference, the differentiation degree of the related gene of circadian clock control network of Lotus japonicus and Medicago truncatula was greater than that of Glycine max, which may be due to Lotus japonicus and Medicago truncatula genome is far less than that of Glycine max.

 

3 Materials and Methods

3.1 Source and acquisition of gene data

Acquisition and analysis of the original data of the Medicago truncatula, the Lotus japonicus and the Glycine max mainly based on online. Table 4 listed genomic databases and corresponding websites of 4 species for online bioinformatics analysis.

 

 

Table 4 Bioinformatics analyse the four species’ corresponding database and website name and website

 

3.2 Using GO (Geneontology) to obtain the circadian clock regulated network related gene information of Arabidopsis thaliana

We search for biological clock, circadian clock, circadian rhythm etc. keywords on the Ontology Gene, get the Go term in Table 5, then enter the TAIR database, get the circadian clock related genes sequence and other related information.

 

 

Table 5 GO item and GO number of plant circadian clock regulated network

 

3.3 Identification of a direct homologous gene

The amino acid sequences of the related genes in Arabidopsis thaliana were used to carry out Blastp or tBlastn on the respective genomic databases of these 3 species in Leguminous. Took the E value of sequence below -30 as candidate sequence, selected the highest similarity sequence in the NCBI reverse Blastp Arabidopsis protein library to determine whether is a direct gene. If not, it is indicated that the gene didn’t have direct homologous genes to the species. Conversely, took the sequence as the standard, then identified other direct homologous genes.

 

3.4 Analysis of conserved structure functional domain

Comprehensive utilized CDD (Conserved Domain Search) on the NCBI (Marchler-Bauer, 2007) to analyze the conserved structure domain on the target sequence.

 

3.5 Multiple sequence alignment, phylogenetic tree’s construction and evolutionary analysis

Amino acid sequence alignment of the 4 species in the direct candidate ortholog genes by using ClustalX program and the default parameters (Devlin and Kay, 2001). The phylogenetic tree was constructed with the NJ method of MEGA4 software, and the evolutionary distance was calculated above 1000 times (Johnson, 2001; Paloma, 2005). At the same time, according to the phylogenetic tree, we can roughly calculate the evolutionary history of a gene between legume and cruciferae.

 

3.6 Expression data acquisition and analysis

The PUT sequence in Plant GDB is a high quality EST sequence and full length cDNA, which through the clustering to remove redundance and partially splice. Take the nucleotide sequence BLASTN of direct candidate ortholog genes compare with the nucleotide sequence PUT. If the similarity of PUT sequence matching the base is greater than 95%, length longer than 200 bp and the E value is less than 1E-30, we think that part of the PUT can prove the matching of orthologous candidate gene expression is true. We divide the EST evidence into 3 classes: F, E, N. F on behalf of the entire candidate genes have PUT sequence coverage, or both ends of the PUT sequence coverage and the entire gene 80% sequence is covered by PUT sequence. N indicates the gene can not find a matching ratio of PUT sequence and E represents that the gene owns a part or a few parts are in line with the requirements of the PUT sequence coverage, but has not yet reached the F standard.

 

3.7 Gene re-annotation

Because of incomplete genome information or annotation errors, there were no full-length ORF genes when identificated the 3 candidate genes in the legume specie. We re-annotated the corresponding genomic region of the ORF gene in the GenScan and obtained the full-length ORF gene. The obtained ORF sequence re-Blast compared to the corresponding PlantGDB genome sequence of the species to confirm whether it corresponded to the original genomic region. At the same time, the amino acid sequence of ORF sequence was translated into reverse Blastp Arabidopsis protein database to confirm whether it was related to the direct homologous gene.

 

Authors' contributions

Li Zongfei was the executor of this experiment, and was responsible for the experimental design, implementation, data analysis and draft writing; Cai Mengdie and Liu Zhenpeng were participated in the data analysis, the formation and amendment of the draft; Wei Fang and Zhang Jie were responsible for manuscript proofreading; Fang Xuanjun determined the research project conception, guided writing and revising paper. All authors have read and approved the final manuscript.

 

Acknowledgements

This research was supported by the Zhuji Cuixi Academy of Biotechnology (Foundation of Life science and Biotechnology Innovation, No: 201601201). Xuan Jia is the English review for the this manuscript.

 

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