Genome-Wide analysis of the AAAP gene family in moso bamboo (Phyllostachys edulis)
- Huanlong Liu†1, 3,
- Min Wu†1, 2,
- Dongyue Zhu1,
- Feng Pan1,
- Yujiao Wang1,
- Yue Wang1 and
- Yan Xiang1, 2, 3Email author
© The Author(s). 2017
Received: 28 June 2016
Accepted: 19 January 2017
Published: 31 January 2017
Members of the amino acid/auxin permease (AAAP) gene family play indispensable roles in various plant metabolism and biosynthesis processes. Comprehensive analysis of AAAP genes has been conducted in Arabidopsis, rice, maize and poplar, but has not been reported from moso bamboo. Phylogenetics, evolutionary patterns and further expression profiles analysis of the AAAP gene family in moso bamboo (Phyllostachys edulis) will increase our understanding of this important gene family.
In this current study, we conducted phylogenetic, gene structure, promoter region, divergence time, expression patterns and qRT-PCR analysis of the 55 predicted AAAP genes in moso bamboo based on the availability of the moso bamboo genome sequence. We identified 55 putative AAAP (PeAAAP1-55) genes, which were divided into eight distinct subfamilies based on comparative phylogenetic analysis using 184 full-length protein sequences, including 55 sequences from moso bamboo, 58 sequences from rice and 71 sequences from maize. Analysis of evolutionary patterns and divergence showed that the PeAAAP genes have undergone a extensive duplication event approximately 12 million years ago (MYA) and that the split between AAAP family genes in moso bamboo and rice occurred approximately 27 MYA. The microarray analysis suggested that some genes play considerable roles in moso bamboo growth and development. We investigated the expression levels of the 16 AAP subfamily genes under abiotic stress (drought, salt and cold) by qRT-PCR to explore the potential contributions to stress response of individual PeAAAP genes in moso bamboo.
The results of this study suggest that PeAAAP genes play crucial roles in moso bamboo growth and development, especially in response to abiotic stress conditions. Our comprehensive, systematic study of the AAAPs gene family in moso bamboo will facilitate further analysis of the functions and evolution of AAAP genes in plants.
KeywordsMoso bamboo Amino acid/auxin permease Phylogenetic analysis Conversed motif Expression patterns qRT-PCR
Amino acids are important organic substances that serve as an indispensable source of organic nitrogen for growth and development, playing vital roles in the metabolism, structure and biosynthesis of various compounds in eukaryotic organisms [1, 2]. In plants, amino acids are important components of nucleotides, chlorophyll, phytohormones and secondary metabolites . Amino acids are transported between different organs through both xylem and phloem, requiring the activity of amino acid transporters (AATs) in the plasma membrane . The first plant amino acid transporter was found in Arabidopsis 23 years ago, namely AtAAP1/NAT2 [4, 5]. Amino acid/auxin permease (AAAP) proteins are found in almost all eukaryotic organisms, belonging to the AAT family [1, 6, 7]. These proteins contribute to the responses to biotic and abiotic stresses and long distance amino acid transport, and they mediate the transport of amino acids across the cellular membrane [8–10]. In addition, previous reports showed that some members of amino acid transporters were located within the tonoplast, which were devoted to transport amino acids between vacuole and cytoplasm, and regulated the storage of amino acids in vacuole [11–14].
To date, the AAAP family is one of the largest families of AATs [1, 6, 7], comprising eight subfamilies, namely ProTs , GATs , LHTs , AAPs [1, 18], ANTs  and ATL subfamilies (ATLa and ATLb) . And all AAAP genes have a specific domain, PF01490 (Aa_trans).
To date, some functions of AAAP proteins have been studied in model plants such as Arabidopsis , poplar , maize  and rice . AtAAP3 appears to be involved in amino acid uptake from the phloem and soil . A recent study showed that AtAAP5 plays a role in amino acid uptake by the root . AtAAP6 is expressed in roots, sink leaves, cauline leaves and xylem parenchyma, suggesting that it functions in amino acid uptake from the xylem . In addition, AtAAP8 might play a crucial role in amino acid transport during fruit development [1, 26]. In rice, 18 genes in the AAP subfamily have been identified , three of which (OsAAP1, OsAAP7 and OsAAP16) encode general AAAP proteins, whereas OsAAP3 does not . OsAAP3 transports the basic amino acids lysine and arginine and has distinct substrate specificity compared with other rice or Arabidopsis AAPs . OsAAP6 is contribute to enhance root absorption and affect the distribution of various amino acids in early stages of seed development .
Bamboo, one of the most important non-timber forest products worldwide, comprises over 70 genera and 1,200 species . A majority of these species are distributed in the subtropical regions of China, especially regions south of the Yangtze River. Moso bamboo is an important species in China with the highest value in several areas among all bamboos, being used to produce timber, paper, artwork and food (young shoots) . However, moso bamboo faces many types of environmental conditions during growth and development, such as high or low temperatures, salt concentrations and soil moisture levels, which limit its distribution and quality. A previous study showed that functional and regulatory proteins contribute to abiotic stress resistance in plant , and AAAP proteins are the fundamental functional proteins. Therefore, in the current study, we investigated AAAP proteins in moso bamboo to identify proteins that function in stress resistance. To date, bioinformatic analysis in model plants has greatly increased our understanding of AAAP genes. In addition, the draft genome sequence of moso bamboo was completed in 2013 , providing a great bioinformatics foundation to perform a comprehensive genome survey of the AAAP family in moso bamboo.
Identification of moso bamboo AAAP genes
The conserved AAAP domains (PF01490) of rice AAAP protein sequences were originally applied as seed sequences to search the NCGR database (www.ncgr.ac.cn/bamboo) . Redundant sequences were removed manually based on the results of Cluster W 2.11 alignment , and each candidate sequence was confirmed using the Pfam (http://pfam.xfam.org/) [33, 34] and SMART (http://smart.embl-heidelberg.de/) databases . The number of amino acids, CDS lengths and physicochemical parameters of AAAP genes were obtained from Bamboo GDB (http://www.bamboogdb.org). Comparing coding sequence and the corresponding genomic DNA sequences of AAAP genes, we obtained their exon/intron structures from GSDS. The TMHMM Server version 2.0 (http://www.cbs.dtu.dk/services/TMHMM/) was used to predict the putative TM (transmembrane) regions of each PeAAAP protein with default settings.
Phylogenetic and conserved motif analyses
Multiple sequence alignment was performed using ClustalX 2.11 software , and a phylogenetic tree was constructed based on the alignment with the N-J method using MEGA 6.0 software and bootstrap analysis of 1,000 replicates. The combined phylogenetic tree of OsAAAP, ZmAAAP and PeAAAP proteins was generated using the same method. The motifs of PeAAAP proteins were identified using the MEME tool (http://meme-suite.org/tools/meme) (parameter setting: maximum number of motifs, 20; maximum width, 50.).
Calculation of Ka/Ks values
Pairwise alignment of AAAP genes encoding sequences of the orthologous and paralogous pairs was first performed using ClustalX 2.11 software and the results of alignment were subsequently further analyzed using the MEGA 6.0, and then the synonymous substitution rate (Ks) and nonsynonymous substitution rate (Ka) were computed using DnaSP 5 software [37, 38]. The divergence time (T) was calculated using the formula T = Ks/2λ (λ = 6.5 × 10−9) [29, 39]. The following parameters were used to perform sliding window analysis of the Ka/Ks ratios of all homologous gene pairs: window size, 150 bp; step size, 9 bp.
Putative promoter region analysis
The 2,000-bp upstream sequences of the genetic sequences were identified as putative promoter regions, which contains various cis-regulatory elements identified using the PLACE website (http://www.dna.affrc.go.jp/PLACE/) .
Plant material and growth conditions
Eight-week-old seedlings were grown in artificial growth chamber with a constant photoperiod (14 h light/8 h darkness) and temperatures average around 22 °C. Moso bamboo seeds for breeding seedlings were collected in the Tianmu Mountain National Nature Reserve in Zhejiang Province, China. In addition, the permission of seeds collection for the experiments was obtained from Prof. Dingqing Tang of School of Forestry and Bio-technology, Zhejiang A & F University. And the identification of these seeds was also performed by Prof. Dingqing Tang. The seedlings were treated with 20% PEG-6000, 200 mM NaCl and 4 °C to induce drought stress, salt stress and cold stress, respectively. In order to obtain reliable experimental data and reduce experimental error, for each sample, we executed three repeated trials for the same stimulation and carried out three biological replicates for expression analysis. For each induction treatment, we collected samples at six time points (0, 1, 3, 6, 12 and 24 h) and immediately stored at – 80 °C freezer for RNA extraction. In addition, untreated plant materials (0 h) were used as the control group.
Expression profile analysis
To study gene expression levels of PeAAAP genes in different tissues or development stages. The expression profile for each gene was obtained from Short Read Archive (SRA) database of NCBI. And then the raw RNA-seq reads of BioProject ERP001341 were trimmed to remove low quality base-calls (Q < 20) and adaptor sequences with pipeline Fastq clean . The paired clean reads were mapped to the Phyllostachys heterocycla reference genome using pipeline tophat2 with defaults parameters, and different expressed genes were detected by Cufflinks . The heatmap of PeAAAP genes in seven different tissues and/or developmental stages (leaf, early panicle, advanced panicle, root, rhizome, 20-cm shoot and 50-cm shoot) was exhibited using the Heatmapper Plus tool .
To research the expression levels of PeAAAP genes, qRT-PCR analysis based on SYBR-green fluorescence was performed for each members of the AAP subfamily. Total RNA was extracted from the plant samples using RNA prep Pure Plant Kit (Tiangen) according to the manufacturer’s instructions, which was reverse transcribed into cDNA subsequently using a PrimeScript™ RT Reagent Kit (TaKaRa). Primer Express 3.0 was used to design the gene-specific primers of each PeAAP genes, and the tonoplast intrinsic protein 41 (TIP41) was used as an internal control . The following program was used for qRT-PCR: 95 °C for 30 s; 40 cycles of 95 °C for 10 s, 55 °C for 15 s, 72 °C for 10 s.
Identification of AAAP genes in moso bamboo
Detailed information about 55 predicted AAAP proteins in moso bamboo
Phylogenetic and conserved domain analysis of AAAP proteins in moso bamboo
Evolutionary patterns and divergence of the AAAP gene family in moso bamboo, rice and maize
Paralogous (Pe-Pe) and orthologous (Pe-Os and Pe-Zm) gene pairs
Putative promoter region analysis
Cis-elements play critical roles in plant growth and development, including determining the tissue-specific or stress-responsive expression patterns of genes, and multi-stimulus-responsive genes are closely correlated with cis-regulatory elements in their promoter regions [48, 49]. Cis-elements have decisive effects on binding to target genes. In this study, we identified three type cis-elements, including cold-responsive, drought-responsive and salt-responsive elements in the promoter regions to help elucidate the potential functions of AAAP genes in moso bamboo [50, 51]. Numerous cis-elements were widespread in the promoter regions, such as S000176 and S000415 for drought stress, S000453 for salt stress and S000407 for cold stress (Additional file 6: Table S2). Moreover, contrasting with the cis-regulatory elements of salt stress, there was the higher amount of cis-elements for drought and cold stress. These results suggest that transcription factors that regulate AAP genes may respond to abiotic stress and have the potential for improving abiotic stress responses, especially drought and cold. These findings may be helpful for further investigating stress tolerance mechanisms in moso bamboo.
Comparative analysis of AAAP genes in moso bamboo, rice and maize
Differential expression profiling of moso bamboo AAAP genes
In general, the overall analysis of gene expression profiles in different tissues will contribute to study the dynamic gene expression of AAAP genes in moso bamboo. The high-throughput RNA sequencing (RNA-Seq), as one of essential next generation sequencing technology, will allow to reveal a snapshot of RNA presence and quantity from a genome at a given moment in time [52, 53]. In addition, the draft genome sequence of moso bamboo has been released . By now, many studies of expression profiles in several gene families were reported and mainly focused on different tissues [54–56]. While, the genome-wide expression profile of PeAAAP genes still remains unclear.
Six gene pairs (PeAAAP12/PeAAAP41, PeAAAP14/PeAAAP36, PeAAAP21/PeAAAP38, PeAAAP26/PeAAAP49, PeAAAP43/PeAAAP55 and PeAAAP44/PeAAAP52) of these above identified exhibit distinct expression patterns in different tissues or developmental stages, suggesting that duplicated genes may have different evolutionary fates. For instance, PeAAAP43 is expressed at a high level in rhizome and shoots, however, its counterpart PeAAAP55 shows slight relative expression level. By contrast, remaining gene pairs have the same or similar patterns of expression accumulation.
qRT-PCR analysis of moso bamboo AAAP genes
The phylogenetic analysis indicated that the AAP subfamily contains 16 PeAAAP genes and that these genes are closely related to stress-responsive genes in rice. This observation prompted us to investigate possible stress-responsive genes among the 16 PeAAAP genes by qRT-PCR. We investigated the expression levels of 16 selected AAP subfamily members (PeAAAP1, PeAAAP5, PeAAAP9, PeAAAP11, PeAAAP14, PeAAAP17, PeAAAP18, PeAAAP21, PeAAAP25, PeAAAP26, PeAAAP33, PeAAAP34, PeAAAP36, PeAAAP38, PeAAAP40 and PeAAAP49) in the leaves of young seedlings in response to PEG, salt and cold treatment using qRT-PCR. The specific primers used in qRT-PCR analysis of these genes are shown in Additional file 9: Table S5.
In summary, the qRT-PCR results revel that 13 genes (PeAAAP9, PeAAAP11, PeAAAP14, PeAAAP17, PeAAAP18, PeAAAP21, PeAAAP25, PeAAAP26, PeAAAP34, PeAAAP36, PeAAAP38, PeAAAP40, and PeAAAP49) exhibited significant changes in response to all three stress treatments, showing that these genes may exhibit different responses to abiotic stress. It was not difficult to found that these results accord with the putative promoter analysis results of AAP subfamily members (Additional file 6: Table S2). There were several cis-elements showing a widely distribution in these members, such as elements S000415 (ACGT), S000407 (CANNTG) and S000453 (GAAAAA) in drought, cold and salt stress response, respectively. These results suggested that a number of PeAAAP genes might play crucial roles in regulating abiotic stress responses.
As an indispensable gene family, the eukaryotic-specific AAAP family plays a pivotal role in the process of plant growth and development, which is one of the largest families of AATs identified to date [21, 22]. According to previous studies, several AAAP genes have been characterized both physiologically and genetically, such as Arabidopsis AAP and AUX subfamily [18, 25, 57, 58], and rice AAP subfamily [27, 28]. By contrast, AAAP family members have not previously been characterized in moso bamboo. Therefore, in the current study, we identified and characterized 55 predicted AAAP genes in moso bamboo using genome wide analysis, and compared these with 58 OsAAAPs and 71 ZmAAAPs, showing that the number of AAAP genes in moso bamboo (55) is the fewest among these three species [22, 23]. The 184 AAAP proteins were found to be divided into eight distinct subfamilies, with every subfamily containing different members from these three species, meaning that AAAP genes had diversified before moso bamboo, rice and maize split. A count of these subfamilies in different species shows that AAP subfamily is the largest one. And AAAP genes with the similar structure showed a tendency to be grouped into the same subfamily, we sought some more valuable evidence to support the reliability of the subfamily classification, including gene structure, motif compositions and TM regions. Furthermore, all members in AUX subfamily have the same numbers and types of TM regions, exon/intron structures and motif compositions, suggesting that these members share a closer evolutionary relationship in the process of AAAP evolution. These results are in accordance with the results of a previous study of the AAAP family in poplar . Furthermore, these results may show that the functions diversified among different members of AAAP genes in mso bamboo. In addition, a previous study showed that AAP1 had 11 TMs in Arabidopsis, which was different from AAP subfamily in moso bamboo, signifying the divergence between different species.
Recent gene duplication events, which help organisms adapt to different environments during growth and development [59, 60] as well as are an important evolutionary mechanism for the rapid expansion and evolution of gene families . To better explain the patterns of macroevolution in moso bamboo, we calculated the value of Ks and Ka in moso bamboo, maize and rice. Specifically, we estimated the Ks and Ka models of paralogous genes (Pe-Pe) and orthologous genes (Pe-Os and Pe-Zm) and calculated the Ks value for each gene pair. We estimated that a large-scale duplication event was occurred approximately 12 MYA in moso bamboo and that the divergence times for orthologous genes (Pe-Os and Pe-Zm) was approximately 27 MYA. Peng et al. estimated that the divergence time between moso bamboo and rice was 48.6 MYA, and maize was 64.6 MYA . Ratio of nonsynonymous to synonymous substitutions (Ka/Ks) can be used to measure the history of selection acting on coding sequences . In general, Ka/Ks ratio less than 1, equal to 1 and greater than 1 means negative or stabilizing selection, neutral selection and positive selection, respectively [46, 47]. Interestingly, in this study, the Ka/Ks ratios were less than 1, evidencing that the homologous gene pairs of AAAP family in moso bamboo have undergone a markedly purifying selection in the course of evolution.
The overall analysis of gene expression profiles in different tissues will contribute to study the dynamic gene expression of AAAP genes in moso bamboo. Therefore, we displayed the gene expression profiles of 55 identified PeAAAP genes using published transcriptome data in NCBI database. Among them, twenty-one genes (PeAAAP7, PeAAAP10, PeAAAP13, PeAAAP14, PeAAAP15, PeAAAP16, PeAAAP17, PeAAAP27, PeAAAP28, PeAAAP29, PeAAAP36, PeAAAP41, PeAAAP43, PeAAAP45, PeAAAP50, PeAAAP51 and PeAAAP53) exhibited relatively high expression level in all seven different tissues or developmental stages, suggesting their importance in the processes of moso bamboo growth and development. While a few numbers of AAAP genes show tissue-specific in this analysis.
In plant, many stress-related genes generated a series of stress responses to meet the adverse environmental condition during growth and development. AAAPs are highly regulated by environmental signals and play positive roles in abiotic stress responses in many plants [62, 63]. AAP genes were previously studied in several species, leading to the identification of 18 and 8 genes in the AAP subfamily in rice and Arabidopsis, respectively. The expression pattern of a gene can provide significant clues about its function, as demonstrated by Zhao et al. . Thus, we performed qRT-PCR to investigate the expression patterns of PeAAAP genes under PEG, cold and NaCl treatment. The PeAAP subfamily members showed significantly differential expression patterns under the three abiotic stresses examined. Most PeAAP genes were upregulated by all three abiotic stress treatments, suggesting that PeAAP genes may play crucial roles in abiotic stress responses in moso bamboo. For instance, PeAAAP9 was highly expressed (over 100-fold that of control levels) under PEG (drought), cold and salt stress treatment. However, this gene shows a relatively lower expression frequency in leaf, meaning that PeAAAP9 responds to environmental stress. And conversely, some genes are unresponsive, especially PeAAAP1 has low expression level in both microarray and qRT-PCR analysis. Furthermore, there were six paralogous pairs in AAP subfamily. Of these gene pairs, five of them (PeAAAP14/PeAAAP36, PeAAAP18/PeAAAP33, PeAAAP21/PeAAAP38, PeAAAP25/PeAAAP40 and PeAAAP26/PeAAAP49) under cold treatment and two gene pairs (PeAAAP14/PeAAAP36 and PeAAAP18/PeAAAP33) under salt treatment (NaCl) had similar expression levels and tendency in the same paralogous pair. These results might suggest that homologous genes had similar putative functions in processes of organism growth and development.
In this study, we investigated phylogenetic, gene structure, promoter region, divergence time, microarray analysis and qRT-PCR analysis of the 55 predicted AAAP genes in moso bamboo. The qRT-PCR was used to explore the expression patterns of 16 selected AAAP genes under three abiotic stresses: drought (20% PEG-6000), salt (200 mM NaCl) and cold (cultured at 4 °C). These results of this study increase our understanding of AAAP family members, including their possible contributions to abiotic stress responses and other putative functions in process of moso bamboo growth and development.
Amino acid/auxin permease
Amino acid permease
Amino acid transporter
Aromatic and neutral amino acid transporter
Amino acid transporter-like
Gamma amino acid butyric acid
Gene structures display server
Lysine histidine transporter
Million years ago
National center of biotechnology information
National center for gene research
Quantitative real-time PCR
Simple modular architecture research tool
Short read archive
Tonoplast intrinsic protein
Transmembrane hidden markov model.
We thank the professors and colleagues of the Laboratory of Modern Biotechnology, Key Laboratory of Crop Biology of Anhui Province and National Engineering Laboratory of Crop Stress Resistance Breeding for their advising and help in this research. And thank Prof. Dingqing Tang, School of Forestry and Bio-technology, Zhejiang A & F University, for giving us the great help in seeds collection for this study.
This study was supported by the National Natural Science Foundation of China (No. 31670672) and Special Fund for Forest Scientific Research in the Public Welfare (No. 201404601).
Availability of data and materials
RNA-seq data for expression profiles from this article were downloaded from NCBI database (accession numbers: ERP001341) (http://trace.ncbi.nlm.nih.gov/Traces/sra/?study=ERP001341). The genome sequences of moso bamboo, rice and maize were obtained from moso bamboo GDB server (http://www.bamboogdb.org), Rice Genome Annotation Project database (http://rice.plantbiology.msu.edu) and Phytozome database (https://phytozome.jgi.doe.gov), respectively. Moso bamboo AAAP gene IDs were listed in Table 1. The IDs of rice and maize AAAP gene were exhibited in Additional file 7: Table S3.
The authors listed in this article have done the necessary work in the process of writing the article, as shown below: HLL constructed the main frame of this article and wrote the manuscript, MW participated in the plot of this article and collected plant materials, DYZ had a hand in designing and actualizing experiments in this article and assisted to complete the writing of this paper, FP collated and analyzed the experimental data and revised the manuscript, YJW helped to write the manuscript and implemented the soft ware, YW helped to handle figures and tables. YX, as the correspondence author, provided financial support for the article and designed the way and frame of this study. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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