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Characterization of the Transcriptome of the Xerophyte Ammopiptanthus Mongolicus Leaves Under Drought Stress by 454 Pyrosequencing

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Characterization of the Transcriptome of the Xerophyte Ammopiptanthus Mongolicus Leaves Under Drought Stress by 454 Pyrosequencing RESEARCH ARTICLE Characterization of the Transcriptome of the Xerophyte Ammopiptanthus mongolicus Leaves under Drought Stress by 454 Pyrosequencing Tao Pang1☯, Lili Guo1,2☯, Donghwan Shim3,4☯, Nathaniel Cannon3, Sha Tang1, Jinhuan Chen1, Xinli Xia1*, Weilun Yin1*, John E. Carlson3* 1 National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Key Laboratory for Silviculture and Conservation, Beijing Forestry University, Beijing, People’s Republic of China, 2 College of Agricultural, Henan University of Science and Technology, Luoyang, People’s Republic of China, 3 The Schatz Center for Tree Molecular Genetics, Department Ecosystem Science and Management, Pennsylvania State University, University Park, Pennsylvania, United States of America, 4 Department of Forest Genetic Resources, Korea Forest Research Institute, Suwon 441–350, Korea ☯ These authors contributed equally to this work. * [email protected] (XX); [email protected] (WY); [email protected] (JEC) OPEN ACCESS Abstract Citation: Pang T, Guo L, Shim D, Cannon N, Tang S, Chen J, et al. (2015) Characterization of the Transcriptome of the Xerophyte Ammopiptanthus Background mongolicus Leaves under Drought Stress by 454 Pyrosequencing. PLoS ONE 10(8): e0136495. Ammopiptanthus mongolicus (Maxim. Ex Kom.) Cheng f., an endangered ancient legume doi:10.1371/journal.pone.0136495 species, endemic to the Gobi desert in north-western China. As the only evergreen broad- Editor: Mukesh Jain, National Institute of Plant leaf shrub in this area, A. mongolicus plays an important role in the region’s ecological-envi- Genome Research, INDIA ronmental stability. Despite the strong potential of A. mongolicus in providing new insights Received: February 17, 2015 on drought tolerance, sequence information on the species in public databases remains Accepted: August 4, 2015 scarce. To both learn about the role of gene expression in drought stress tolerance in A. mongolicus and to expand genomic resources for the species, transcriptome sequencing of Published: August 27, 2015 stress-treated A. mongolicus plants was performed. Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used Results by anyone for any lawful purpose. The work is made Using 454 pyrosequencing technology, 8,480 and 7,474 contigs were generated after de available under the Creative Commons CC0 public domain dedication. novo assembly of RNA sequences from leaves of untreated and drought-treated plants, respectively. After clustering using TGICL and CAP3 programs, a combined assembly of all Data Availability Statement: Transcriptome data of this study are available at the National Center for reads produced a total of 11,357 putative unique transcripts (PUTs). Functional annotation Biotechnology Information (NCBI) Sequence Read and classification of the transcripts were conducted by aligning the 11,357 PUTs against Archive (SRA, http://www.ncbi.nlm.nih.gov/Traces/ the public protein databases and nucleotide database (Nt). Between control and drought- Sra) under accession number SRP026002. Other transcriptome data used in this study are also treated plants, 1,620 differentially expressed genes (DEGs) were identified, of which 1,106 available under accession number of SRX216074 were up-regulated and 514 were down-regulated. The differential expression of twenty can- and SRX142053. The high quality assembled PUTs didate genes in metabolic pathways and transcription factors families related to stress- were deposited in the NCBI Transcriptome Shotgun response were confirmed by quantitative real-time PCR. Representatives of several large Assembly Sequence Database http://www.ncbi.nlm. nih.gov/genbank/tsa) under accession number gene families, such as WRKY and P5CS, were identified and verified in A. mongolicus for SUB932387. the first time. PLOS ONE | DOI:10.1371/journal.pone.0136495 August 27, 2015 1/25 Ammopiptanthus mongolicus Transcriptome Analysis under Drought Stress Funding: The work was supported by the following: Conclusions The National Natural Science Foundation of China (31070597, 31270656), http://www.nsfc.gov.cn/; and The additional transcriptome resources, gene expression profiles, functional annotations, Scientific Research and Graduate Training Joint and candidate genes provide a more comprehensive understanding of the stress response Programs from BMEC (Stress Resistance pathways in xeric-adapted plant species such as A. mongolicus. Mechanism of Poplar). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Introduction Drought stress prevents plants from realizing their full genetic potential, and greatly inhibits plant growth and productivity in agriculture in arid and semiarid areas [1]. By disrupting water balance, drought stress reduces plant development, reproduction, seed, and fruit yields [2]. Plants respond to drought stress with complex cascades of gene expression and signal trans- duction [3]. The identification and application of genes associated with stress tolerance are of interest in the development of drought tolerance in crop plants [4]. Approximately 2000 drought-responsive genes have been identified in Arabidopsis thaliana [5]. For some xero- phytes, like Populus euphratica, gene discovery and transcriptome analyses have led to the identification of numerous potential stress-related genes [6–8]. These studies are contributing new gene resources, revealing drought responsive mechanisms in xerophytes and enabling pro- duction of more stress tolerant plants. Ammopiptanthus mongolicus (Maxim. Ex Kom.) Cheng f., is a relatively primitive species found in the semi-arid region of north-western China [9]. The genus Ammopiptanthus (in the Leguminosae) contains only two species (A. mongolicus and A. nanus) which are considered endangered. This is of great concern ecologically given that the two species are the only ever- green broadleaf shrubs in this largely desert area [10]. Strong osmotic stress resistance makes it possible for A. mongolicus to survive in very inhospitable areas, where the annual precipitation can be as low as 150 mm and the lowest temperature is below -30°C. Our previous studies have elucidated cold resistance mechanisms in A. mongolicus. It is of even greater importance to dis- cover the genes and metabolic pathways associated with drought stress tolerance in A. mongoli- cus [11]. Individual drought-related genes have been cloned and identified, such as AmCBL1 [12], AmNHX2 [13], AmVP1 [14], AmEBP1 [15] and AmLEA [16]. However, the few gene resources for A. mongolicus in GenBank (5,801 ESTs and 164 nucleotide sequences as of Dec 1st, 2014) are inadequate to fully characterize stress response pathways. Originally, Sanger sequencing of cDNA libraries, which is relatively low throughput, costly and nonquantitative, was used for gene discovery and transcriptome analysis [17]. In recent years, rapid developments in next-generation sequencing (NGS), such as massively parallel 454 pyrosequencing and Illumina-based RNASeq, have spurred rapid developments in genomics and transcriptomics research [18]. Because of its advantages of longer read lengths, speed and accuracy, 454 pyrosequencing has been widely applied in de novo sequencing, especially in gene discovery and functional identification with non-model organisms, such as Aegilops var- iabilis [19], Metasequoia glyptostroboides [20], Cicer arietinum [21], Eucalyptus grandis [22], Phalaenopsis orchids [23], Populus euphratica [24], and Liriodendron tulipifera [25, 26]. A few studies have reported gene expression profiles from A. mongolicus under drought stress. Guo et al. analysed differential gene expression under cold and drought stress using complementary DNA-amplified fragment length polymorphism (cDNA-AFLP) technology [27]. They identified several drought-responsive genes associated with transcription, metabolic processes and protein modification. Zhou et al. reported the identification of candidate genes related to drought stress from the A. mongolicus root transcriptome using 454 pyrosequencing PLOS ONE | DOI:10.1371/journal.pone.0136495 August 27, 2015 2/25 Ammopiptanthus mongolicus Transcriptome Analysis under Drought Stress technology [28]. Also, Liu et al.[29] reported 5,282 ESTs from a cDNA library prepared from A. mongolicus plants under cold and drought stresses. Of the 1,594 putatively unique tran- scripts assembled from the 5,282 ESTs, 528 were specific to stress-response. Recently, Wu et al. [30] reported the transcriptome analysis of A. mongolicus using dehydration treatment on filter paper, identifying 2,028 DEGs in common across three time points (2, 8, 24 h). Here, we describe the analysis of gene expression patterns in seedlings of the xerophyte A. mongolicus subjected to drought stress by extended water deprivation simulating natural drought conditions. Two cDNA libraries constructed from RNA of leaves from drought- treated seedlings and untreated seedlings were sequenced on a 454 pyrosequencing platform. Insights into the functions of expressed genes were obtained from COG annotations, GO clas- sifications and KEGG metabolic pathway analysis. The putative functions of transcripts from leaves observed in this study represent a different set of genes from the previous reports from transcriptomes of root tissues and seedlings
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