Genome-wide identification and evolutionary analysis of leucine-rich repeat receptor-like protein kinase genes in soybean
© Zhou et al. 2016
- Received: 6 December 2015
- Accepted: 24 February 2016
- Published: 2 March 2016
Leucine-rich repeat receptor-like kinases (LRR-RLKs) constitute the largest subfamily of receptor-like kinases in plant. A number of reports have demonstrated that plant LRR-RLKs play important roles in growth, development, differentiation, and stress responses. However, no comprehensive analysis of this gene family has been carried out in legume species.
Based on the principles of sequence similarity and domain conservation, a total of 467 LRR-RLK genes were identified in soybean genome. The GmLRR-RLKs are non-randomly distributed across all 20 chromosomes of soybean and about 73.3 % of them are located in segmental duplicated regions. The analysis of synonymous substitutions for putative paralogous gene pairs indicated that most of these gene pairs resulted from segmental duplications in soybean genome. Furthermore, the exon/intron organization, motif composition and arrangements were considerably conserved among members of the same groups or subgroups in the constructed phylogenetic tree. The close phylogenetic relationship between soybean LRR-RLK genes with identified Arabidopsis genes in the same group also provided insight into their putative functions. Expression profiling analysis of GmLRR-RLKs suggested that they appeared to be differentially expressed among different tissues and some of duplicated genes exhibited divergent expression patterns. In addition, artificial selected GmLRR-RLKs were also identified by comparing the SNPs between wild and cultivated soybeans and 17 genes were detected in regions previously reported to contain domestication-related QTLs.
Comprehensive and evolutionary analysis of soybean LRR-RLK gene family was performed at whole genome level. The data provides valuable tools in future efforts to identify functional divergence of this gene family and gene diversity among different genotypes in legume species.
- Leucine-rich repeat receptor-like kinase (LRR-RLK)
- Phylogenetic analysis
- Expression profiling
- Evolutionary analysis
Receptor-like kinases (RLKs) are a diverse group of transmembrane proteins characterized with a ligand-binding domain to receive signal molecules, a membrane-spanning domain to anchor the protein, and a cytoplasmic protein kinase domain to transduce signals downstream . In both plants and animals, RLKs mediate plenty of signaling messages at the cell surface and act as key regulators during developmental processes [2–4]. The first RLK of higher plant was isolated from maize and subsequently numerous RLKs have been identified from more than 20 plant species . In plant, the superfamily of RLKs is divided into three major groups based on the presence or absence of the receptor and kinase domain [1, 6, 7]. According to the divergence of extracellular domains, RLKs can be further classified into 17 subgroups, including leucine-rich repeat (LRR) RLKs, S-domain RLKs, and so on [8, 9]. Among all these subgroups, LRR-RLK is the largest one in plants by far, the members of which contain several tandem repeats of about 24 amino acids with conserved leucine residues in the extracellular regions [7, 10].
Genetic and biochemical studies have demonstrated that plant LRR-RLKs play important roles in diverse processes during growth and development [11, 12]. In Arabidopsis, LRR-RLKs including SERK1/2, EMS1, BAM1/2, RPK2 and FER have been proved to modulate the processes of anther development and fertilization [13–18]. Enough evidences supported that CLV and RPK2 were essential receptor-like kinases in formation and maintenance of shoot apical meristem [19, 20]. Some other reports also revealed that LRR-RLK genes such as BRI and BAK1 were involved in brassinosteroid signaling transduction while a few other LRR-RLK genes were associated with the stress responses of abscisic acid [21–23]. Moreover, some LRR-RLK genes were also reported to possess dual functions due to the cross talks between plant development and defense processes or the recognition of multiple ligands by one receptor . For example, Arabidopsis ERECTA gene has been characterized not only to regulate ovule development  but also to be involved in resistance to bacterial wilt .
The rapidly increasing sequenced genomes have facilitated identification of whole gene family by bioinformatics tools at genomic level in plant. To date, the structure features and expression profiles of LRR-RLK genes have been described in plants including Arabidopsis , rice , and poplar . In most of these species, LRR-RLKs appeared to be large families with hundreds of members and evolved to perform diverse functions [28–30]. Some reports also revealed that LRR-RLK genes had redundant functions due to extensive gene duplication in genome. For example, although single mutant of serk1 or serk2 displays normal anther morphology, serk1 serk2 double mutant could rescue the phenotype of exs or ems mutants which failed to form pollen due to the absence of tapetal cell layer and production of extra sporogenous cells in Arabidopsis [13, 14]. Translational fusion study of SERK1/SERK2 to variants of green fluorescent protein also suggested that SERK1/SERK2 may function as part of a protein complex .
Soybean (Glycine max) is the most important legume source of protein for animal feed and economic source of vegetable oil for human nutrition . During the evolutionary history, soybean genome underwent two rounds of whole genome duplication (WGD) approximately 59 and 13 million years ago (MYA) . Unlike most of other diploids, nearly 75 % of genes exhibit multiple copies in soybean genome due to the lack of immediate diploidization during the relatively recent WGD . Therefore, the structure features of most gene families in soybean are more complex than in Arabidopsis, rice or poplar. Although only a few members of LRR-RLK genes have been functionally characterized in soybean, enough evidences supported that soybean LRR-RLK genes also played important roles in various plant development and defense processes including leaf senescence, cell elongation, and cold stress tolerance [34–36].
In the present study, a genome-wide search for LRR-RLK genes was performed in soybean and a total of 467 GmLRR-RLKs had been identified. Detailed analysis of genome organization, sequence phylogeny, gene structure, conserved domains, duplication status, and expression profiling were carried out. In addition, the evolutionary patterns of the LRR-RLK gene family were examined in soybean by analysis of genes in tandem and segmental duplication regions. Moreover, the effect of artificial selection in soybean LRR-RLK gene family was also detected during soybean domestication. Our results provide a framework for further evolutionary and functional characterization of the LRR-RLK gene family in soybean.
Identification and genome distribution of LRR-RLK gene family in soybean
In order to identify all members of LRR-RLKs in soybean genome, a batch BLAST search was performed against soybean protein database using the amino acid sequences of all Arabidopsis LRR-RLKs as queries. All of the retrieved soybean proteins were then submitted to SMART and PFAM databases for annotation of the domain structure. Only candidate containing at least one LRR domain and a kinase domain was regarded as a “true” LRR-RLK. After removing of the unsupported sequences and redundant genes manually, a total of 467 putative LRR-RLK genes were identified from the whole genome of soybean. The identified soybean LRR-RLK genes encode peptides ranging from 423 to 1563 a.a. in length. Detailed information for each gene, including the accession number and the characteristics of the encoded protein, was listed in Additional file 1. Among all these putative GmLRR-RLKs, only three proteins (Glyma.03G026800, Glyma.07G047200 and Glyma.13G228300) were predicted to have two kinase domains. Comparing with LRR-RLK genes identified in Arabidopsis, rice and populus genome (213, 309 and 379 members respectively) [26–28], soybean LRR-RLK gene family identified in this study is the largest one in plant so far. The number of GmLRR-RLKs is about 2.2 fold of that of AtLRR-RLKs, which is consistent with the ratio of putative soybean homologs to each Arabidopsis gene [32, 37].
Phylogenetic analysis of soybean LRR-RLKs
The classification of groups and subgroups for soybean LRR-RLK proteins
No. of Genes
Length of amino-acid (a.a.)
Percentage with signal peptide
Since most of the AtLRR-RLKs with similar functions have a tendency to cluster together, the soybean LRR-RLK genes in the same group or subgroup may have similar functions with their Arabidopsis homologs. Except for groups IV and VIII having no Arabidopsis ortholog with identified function, all the other groups have at least one AtLRR-RLK functional characterized. For example, GmLRR-RLKs in groups I, II, III, VII, and XII were clustered with AtLRR-RLKs involved in organ/tissue development and defense signaling [13, 14, 40–43]. Group V included the Arabidopsis SCM gene related to root hair specification and the SRF gene in cell wall biology [44, 45]. In addition, the Arabidopsis LRR-RLK genes involved in brassinosteroid and peptide signaling fell into the group X  and genes related to cell fate specification, organ morphogenesis , vascular development [48, 49], abscisic acid signaling, and defense response  were grouped in group XI. Moreover, subgroup XIII-a contained two FEI genes which were involved in signaling pathway of cell wall development , while subgroup XIII-b included ERECTA and ERECTA-LIKE genes regulating the stomata development and organ size .
Gene structure and conserved motif analysis
To further understand the potential functions of the LRR-RLK genes in soybean, all putative motifs of these proteins were predicted by using the program MEME (Multiple Em for Motif Elicitation). The results suggested that the motif compositions among groups or subgroups were consistent with the phylogenetic classification. Differences among groups or subgroups were observed in not only types of motifs but also number of specific motif in one protein (Additional file 4). In addition, searching for the possible signal peptides in all soybean LRR-RLKs using SignalP showed that 359 members have signal peptides. Meanwhile, the transmembrane (TM) domain was also predicted with TMHMM and a total of 442 GmLRR-RLKs had at least one while 25 members had no TM domain, among which 205 proteins had at least two TM domains. These results also indicated that most of the closely related members in the phylogenetic tree exhibited similar motif, which further suggested that a great deal of functional redundancy existed among soybean LRR-RLK proteins in the same subgroup (Fig. 3 and Additional file 5).
Gene duplication and orthologous relationships of soybean LRR-RLK genes
Gene duplication is always considered to be one of primary driving forces during the evolution of genomes . Segmental duplication, tandem duplication and transposition events are regarded as three main causes for the expansion of gene family in plant . In our analysis, the tandem duplication cluster was defined as a region containing two or more soybean LRR-RLK genes within 200 kb. The results showed that about 20.3 % (94 out of 464) genes in this gene family were located in regions with tandem duplications and composed 33 clusters in total (Additional file 6). The largest tandem duplication cluster contained as many as ten genes while the smallest one contained only two. Further analysis also revealed that the tandem duplication clusters were distributed unevenly among 14 phylogenetic groups. Group XII contained the most clusters with eight clusters including 35 genes while Groups III, IV, V, VI, VII, IX, XIV had no cluster.
Expression profiles of LRR-RLK genes in soybean
To gain a broader understanding of the putative functions of soybean LRR-RLKs, the expression profiles of these genes were examined by using the RNA-Seq dataset from different soybean tissues. The distinct transcript abundance patterns of all 467 LRR-RLK genes were identified from RNA-Seq atlas data of tissues including roots, root hairs, nodules, leaves, stems, flowers, SAM, pods, and seeds. Although some genes exhibited low transcript abundance like genes encoding transcription factors, most of them demonstrated distinct tissue specific expression pattern (Additional file 8). Detailed analysis showed that 53 (11.3 %), 68 (14.6 %), 65 (13.9 %), 53 (11.3 %), 95 (20.3 %), 87 (18.6 %), 75(16.1 %), 67 (14.3 %), and 51 (10.9 %) GmLRR-RLKs had specific transcript accumulation in roots, root hairs, nodules, leaves, stems, SAM, pods, seeds, and flowers respectively, suggesting that these LRR-RLK genes might function as tissue-specific regulators in different cells or organs.
Artificial selection analysis for LRR-RLKs during soybean domestication
In order to identify the selective GmLRR-RLKs during soybean domestication, F st value of each locus was calculated between two populations (Fig. 6b and Additional file 10). The results showed that 71.6 % loci (5182 out of 7239 loci) underwent non-selection with F st <0.15 during soybean evolution. However, a total of 302 SNPs in 98 soybean LRR-RLK genes were identified as selected loci with F st value cutoff 0.45 (Additional file 11). Although a number of these SNPs (134 out of 302) were located in the introns of GmLRR-RLKs, nearly one third (89 SNPs) of them resulted in non-synonymous alteration. Further analysis showed that all subgroups of GmLRR-RLKs had selected genes except for group XIV. Group XI has the most selected soybean LRR-RLK genes (21 genes) while group IV has only one gene. Especially, although Glyma.11G214400 and Glyma.18G050700 have the largest number of selected SNPs (36 and 32 SNPs respectively), majority SNPs in the first gene resulted in non-synonymous alteration while most of SNPs appeared in the introns of the second one. Furthermore, a number of selected LRR-RLK genes between the wild and cultivated populations were detected in regions previously reported to contain domestication-related QTLs (Additional file 11). These included six GmLRR-RLKs located at QTLs related to pod traits including pod dehiscence/number/maturity [61, 62], five genes located at QTLs conditioning twinning habit [63–65], four genes at QTL regions of seed weight/hard-seededness and two genes at regions related to lodging [63, 65]. These selected genes reflected the important roles of GmLRR-RLKs on soybean domestication and contribute to the cultivation of soybeans in order to meet the demands of human beings.
Here we performed comprehensive and evolutionary analyses of LRR-RLK gene family in soybean, and provided detailed information on its members. A total of 467 putative LRR-RLK genes were identified in the soybean genome, which represented the largest LRR-RLK gene family identified in plant so far and a relatively large gene family in soybean. The distribution of all these genes was non-random across all soybean chromosomes and majority of them were located in segmental duplicated regions rather than tandem duplicated clusters. The exon/intron compositions and motif arrangements were considerably conserved among members in the same groups or subgroups. The transcriptional profiles of many duplicated genes were also similar in different soybean tissues even though some of them exhibited divergent expression patterns. The close phylogenetic relationship of GmLRR-RLKs and identified AtLRR-RLK genes in the same subgroup provided insight into their putative functions. Moreover, some artificial selected GmLRR-RLKs have also been identified by comparing the gene diversities of these loci during the evolution from wild to cultivated soybeans. Taken together, all these results provided valuable tools in future efforts to identify specific gene functions of this family and gene diversity among different genotypes of soybean.
Arabidopsis LRR-RLKs and soybean genome resources
The amino acid sequences of all Arabidopsis LRR-RLKs were acquired from the TAIR database v10.0 (http://www.arabidopsis.org/). The classification of AtLRR-RLKs and nomenclature of groups were based on PlantsP server v.2011 of Arabidopsis 2010 project (http://plantsp.genomics.purdue.edu/projects/lrr/Clouse2010.htm) . The genomic, coding and amino-acid sequences of all annotated soybean genes were according to genome sequence of Glycine max Wm82.a2.v1 from Phytozome v10 (http://phytozome.jgi.doe.gov/pz/portal.html) .
Identification of LRR-RLK genes in soybean genome
The amino-acid sequences of all Arabidopsis LRR-RLK members were used to run a local blast search against the protein database of all annotated soybean genes by using Bioedit v7  and all proteins with an E-value less than 10−6 were selected as putative soybean LRR-LRKs. These putative GmLRR-RLKs were further filtered by removing redundant sequences and functional annotation, following by analysis with SMART (http://smart.embl-heidelberg.de)  and PFAM (http://pfam.xfam.org/)  to ensure the presence of LRR and kinase domains.
Multiple sequence alignments and phylogenetic tree construction
The amino-acid sequence of kinase domain for each GmLRR-RLK and AtLRR-RLK protein was extracted after prediction of kinase domains from these proteins. Multiple sequence alignments were performed by using ClustalX (version 1.83) with default parameters . Unrooted phylogenetic trees were constructed for soybean LRR-RLKs alone or soybean/Arabidopsis together with MEGA 6.0  using the neighbor-joining (NJ) method. The nodes were tested by bootstrap analysis with 1000 replicates and the tree with the highest likelihood was selected for further analysis.
The chromosome location, gene structure, and motif analysis of the soybean LRR-RLK genes
All members of GmLRR-RLKs were mapped onto soybean chromosomes based on the physical positions of them. The image of chromosomal location was produced with MapInspect software (http://mapinspect.software.informer.com). The number and positions of exons and introns for soybean LRR-RLK genes were determined by comparison of the coding sequences with their corresponding genomic DNA sequences using GSDS v2.0 . The presence of signal peptides and transmembrane domains was predicted with Signalp v4.1 (http://www.cbs.dtu.dk/services/SignalP/) , TMHMM v2.0 (http://www.cbs.dtu.dk/services/TMHMM/)  and Phobius (http://phobius.sbc.su.se/)  respectively. The combination of phylogenetic tree, gene and protein structures was generated using iTOL tool (http://itol.embl.de) .
Duplication analysis and calculating the date of duplication events
Tandem duplications were characterized as multiple members of this gene family occurring within neighboring intergenic regions. In this study, soybean LRR-RLK genes clustered together within 200 kb were regard as tandem duplicated genes based on the criteria of other plants in previous reports [28, 78]. The segmental duplicated GmLRR-RLKs were characterized according to the PGDD database (http://chibba.agtec.uga.edu/duplication/). The Ks and Ka values for duplicated gene pairs were also calculated by using PGDD database. The Ks values were used to calculate the approximately dates of duplication events and the clock-like rate (λ) of synonymous substitution was set 6.1x10−9 substitutions/synonymous site/year for soybean [32, 79, 80].
Transcriptional profile analysis
RNA-seq data of soybean tissues for roots, root hairs, nodules, leaves, stems, flowers, SAM, pods, and seeds was obtained from Phytozome v10 (http://phytozome.jgi.doe.gov/pz/portal.html) and the expression profiles of all GmLRR-RLKs were selected for further analysis. Soybean LRR-RLK genes were clustered based on the expression profiles and hierarchical clustering of transcriptional data was performed with MultiExperiment Viewer (Mev) v.4.9.0 using Pearson correlation and Average Linkage Clustering algorithm .
Quantitative real time RT-PCR analysis
Soybean plants (ecotype Williams 82) were grown on soil in the chamber under long day conditions (16 h light/8 h dark cycle) at 25 ± 1 °C. Roots, stems, simple leaves, trifoliolate leaves, shoot apical meristem (SAM) from 2-week-old seedlings, flowers, pods and 1-week-old seedlings were collected for total RNA isolation. Total RNA was extracted using TRIzol Reagent (Invitrogen, USA) and was treated with RNase-free DNase (TaKaRa, Japan). Five micrograms of total RNA were reverse-transcribed using the ReverTra Ace qPCR RT Kit (TOYOBO, Japan) in a reaction of 20 μL. The cDNA was diluted 50 times as the template for quantitative RT-PCR. The PCR amplification was carried out on an Applied Biosystems 7300 Real-Time PCR System, using SYBR Premix Ex Taq kit (TaKaRa, Japan). The procedure of the reaction was set according to the manufacturer’s protocol and sequences of primers used were shown in Additional file 12. The relative expression level of each gene, corresponding to the expression level of Actin, was calculated using 2−ΔΔt method .
Selective analysis of GmLRR-RLKs among soja genus
SNP data of 25 wild soybeans and 31 cultivated soybeans were downloaded from NCBI web site (http://www.ncbi.nlm.nih.gov/SNP/snp_viewTable.cgi?handle=NFCRI_MOA_CAAS). SNP loci of the GmLRR-RLKs were identified based on the physical position of each gene. The v1.1 version of soybean gene annotation was used since the physical positions of all SNPs were based on this version of soybean genome. The gene diversity of each SNP loci in G.max and G.soja, and F st value were calculated by Genepop V4.0 . The SNP locus with F st >0.45 was defined as a putative selective site during domestication.
Availability of data and materials
The data supporting the results of this article is included within the article and its additional files.
This work was supported by the National Natural Science Foundation of China (31271753), the State High-tech Research and Development Program (Grant No. 2013AA102602), the Fundamental Research Funds for Excellent Young Scientists of ICS-CAAS (Grant to Y. G.), and the Agricultural Science and Technology Innovation Program (ASTIP) of Chinese Academy of Agricultural Sciences.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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