Characterization of the Transcriptome of the Xerophyte Ammopiptanthus mongolicus Leaves under Drought Stress by 454 Pyrosequencing

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Abstract

Background

Ammopiptanthus mongolicus (Maxim. Ex Kom.) Cheng f., an endangered ancient legume species, endemic to the Gobi desert in north-western China. As the only evergreen broadleaf shrub in this area, A. mongolicus plays an important role in the region’s ecological-environmental stability. Despite the strong potential of A. mongolicus in providing new insights on drought tolerance, sequence information on the species in public databases remains 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 stress-treated A. mongolicus plants was performed.

Results

Using 454 pyrosequencing technology, 8,480 and 7,474 contigs were generated after de 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 reads produced a total of 11,357 putative unique transcripts (PUTs). Functional annotation and classification of the transcripts were conducted by aligning the 11,357 PUTs against the public protein databases and nucleotide database (Nt). Between control and drought-treated plants, 1,620 differentially expressed genes (DEGs) were identified, of which 1,106 were up-regulated and 514 were down-regulated. The differential expression of twenty candidate genes in metabolic pathways and transcription factors families related to stress-response were confirmed by quantitative real-time PCR. Representatives of several large gene families, such as WRKY and P5CS, were identified and verified in A. mongolicus for the first time.

Conclusions

The additional transcriptome resources, gene expression profiles, functional annotations, and candidate genes provide a more comprehensive understanding of the stress response pathways in xeric-adapted plant species such as A. mongolicus.

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Most cited references 50

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Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance.

Wangxia Wang, Basia Vinocur, Arie Altman (2003)

Abiotic stresses, such as drought, salinity, extreme temperatures, chemical toxicity and oxidative stress are serious threats to agriculture and the natural status of the environment. Increased salinization of arable land is expected to have devastating global effects, resulting in 30% land loss within the next 25 years, and up to 50% by the year 2050. Therefore, breeding for drought and salinity stress tolerance in crop plants (for food supply) and in forest trees (a central component of the global ecosystem) should be given high research priority in plant biotechnology programs. Molecular control mechanisms for abiotic stress tolerance are based on the activation and regulation of specific stress-related genes. These genes are involved in the whole sequence of stress responses, such as signaling, transcriptional control, protection of membranes and proteins, and free-radical and toxic-compound scavenging. Recently, research into the molecular mechanisms of stress responses has started to bear fruit and, in parallel, genetic modification of stress tolerance has also shown promising results that may ultimately apply to agriculturally and ecologically important plants. The present review summarizes the recent advances in elucidating stress-response mechanisms and their biotechnological applications. Emphasis is placed on transgenic plants that have been engineered based on different stress-response mechanisms. The review examines the following aspects: regulatory controls, metabolite engineering, ion transport, antioxidants and detoxification, late embryogenesis abundant (LEA) and heat-shock proteins.

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Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.

Qiang Liu, Mie Kasuga, Yoh Sakuma … (1998)

Plant growth is greatly affected by drought and low temperature. Expression of a number of genes is induced by both drought and low temperature, although these stresses are quite different. Previous experiments have established that a cis-acting element named DRE (for dehydration-responsive element) plays an important role in both dehydration- and low-temperature-induced gene expression in Arabidopsis. Two cDNA clones that encode DRE binding proteins, DREB1A and DREB2A, were isolated by using the yeast one-hybrid screening technique. The two cDNA libraries were prepared from dehydrated and cold-treated rosette plants, respectively. The deduced amino acid sequences of DREB1A and DREB2A showed no significant sequence similarity, except in the conserved DNA binding domains found in the EREBP and APETALA2 proteins that function in ethylene-responsive expression and floral morphogenesis, respectively. Both the DREB1A and DREB2A proteins specifically bound to the DRE sequence in vitro and activated the transcription of the b-glucuronidase reporter gene driven by the DRE sequence in Arabidopsis leaf protoplasts. Expression of the DREB1A gene and its two homologs was induced by low-temperature stress, whereas expression of the DREB2A gene and its single homolog was induced by dehydration. Overexpression of the DREB1A cDNA in transgenic Arabidopsis plants not only induced strong expression of the target genes under unstressed conditions but also caused dwarfed phenotypes in the transgenic plants. These transgenic plants also revealed freezing and dehydration tolerance. In contrast, overexpression of the DREB2A cDNA induced weak expression of the target genes under unstressed conditions and caused growth retardation of the transgenic plants. These results indicate that two independent families of DREB proteins, DREB1 and DREB2, function as trans-acting factors in two separate signal transduction pathways under low-temperature and dehydration conditions, respectively.

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Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.

K Shinozaki, K Yamaguchi-Shinozaki (2000)

Recently, a major transcription system that controls abscisic-acid-independent gene expression in response to dehydration and low temperature has been identified. The system includes the DRE/CRT (dehydration-responsive element/C-repeat) cis-acting element and its DNA-binding protein, DREB/CBF (DRE-binding protein/C-repeat binding factor), which has an AP2 domain. DREB/CBF contains two subclasses, DREB1/CBF and DREB2, which are induced by cold and dehydration, respectively, and control the expression of various genes involved in stress tolerance. Recent studies are providing evidence of differences between dehydration-signaling and cold-stress-signaling cascades, and of cross-talk between them.

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Author and article information

Contributors

Mukesh Jain: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 27 August 2015

Publication date Collection: 2015

Volume: 10

Issue: 8

Electronic Location Identifier: e0136495

Affiliations

[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

National Institute of Plant Genome Research, INDIA

Author notes

Competing Interests: The authors have declared that no competing interests exist.

Conceived and designed the experiments: TP LG XX WY JEC. Performed the experiments: TP LG DS JEC. Analyzed the data: TP LG DS NC. Contributed reagents/materials/analysis tools: NC ST JC. Wrote the paper: TP NC XX JEC.

* E-mail: xiaxl@ 123456bjfu.edu.cn (XX); yinwl@ 123456bjfu.edu.cn (WY); jec16@ 123456psu.edu (JEC)

Article

Publisher ID: PONE-D-14-58483

DOI: 10.1371/journal.pone.0136495

PMC ID: 4552034

PubMed ID: 26313687

SO-VID: c11abb40-dfbc-4a8a-8f2c-7301c75d6278

License:

This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication

History

Date received : 17 February 2015

Date accepted : 4 August 2015

Page count

Figures: 8, Tables: 2, Pages: 25

Funding

The work was supported by the following: The National Natural Science Foundation of China (31070597, 31270656), http://www.nsfc.gov.cn/; and Scientific Research and Graduate Training Joint Programs from BMEC (Stress Resistance Mechanism of Poplar). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Custom metadata

Data Availability Transcriptome data of this study are available at the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA, http://www.ncbi.nlm.nih.gov/Traces/Sra) under accession number SRP026002. Other transcriptome data used in this study are also available under accession number of SRX216074 and SRX142053. The high quality assembled PUTs were deposited in the NCBI Transcriptome Shotgun Assembly Sequence Database http://www.ncbi.nlm.nih.gov/genbank/tsa) under accession number SUB932387.

Characterization of the Transcriptome of the Xerophyte Ammopiptanthus mongolicus Leaves under Drought Stress by 454 Pyrosequencing

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Abstract

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Most cited references 50

Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance.

Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis.

Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways.

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