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Title: Genome-wide transcriptomic analysis of a desert willow, Salix psammophila, reveals the function of hub genes SpMDP1 and SpWRKY33 in drought tolerance

Abstract

Background: Drought is a major environmental constraint to plant growth, development and productivity. Compared with most willows that are generally susceptible to drought, the desert willow Salix psammophila has extraordinary adaptation to drought stress. However, its molecular basis of drought tolerance is still largely unknown.Results: During polyethylene glycol 6000 (PEG 6000)-simulated drought stress, we found that the osmotic adjustment substances were accumulated and the antioxidant enzyme activities were enhanced in S. psammophila roots. A total of 8172 differentially expressed genes were identified in roots of S. psammophila through RNA-Sequencing. Based on K-means clustering, their expression patterns were classified into nine clusters, which were enriched in several stress-related processes including transcriptional regulation, response to various stresses, cell death, etc. Moreover, 672 transcription factors from 45 gene families were differentially expressed under drought stress. Furthermore, a weighted gene co-expression network was constructed, and eight genes were identified as hub genes. We demonstrated the function of two hub genes, magnesium-dependent phosphatase 1 (SpMDP1) and SpWRKY33, through overexpression in Arabidopsis thaliana. Overexpression of the two hub genes enhanced the drought tolerance in transgenic plants, suggesting that the identification of candidate drought tolerance genes in this study was highly efficient and credible.Conclusions: Our study analyzedmore » the physiological and molecular responses to drought stress in S. psammophila, and these results contribute to dissect the mechanism of drought tolerance of S. psammophila and facilitate identification of critical genes involved in drought tolerance for willow breeding.« less

Authors:
 [1]; ORCiD logo [2];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Chinese Academy of Forestry, Beijing (China)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Chinese Academy of Forestry, Beijing (China)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1557471
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
BMC Plant Biology
Additional Journal Information:
Journal Volume: 19; Journal Issue: 1; Journal ID: ISSN 1471-2229
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Jia, Huixia, Zhang, Jin, Li, Jianbo, Sun, Pei, Zhang, Yahong, Xin, Xuebing, Lu, Mengzhu, and Hu, Jianjun. Genome-wide transcriptomic analysis of a desert willow, Salix psammophila, reveals the function of hub genes SpMDP1 and SpWRKY33 in drought tolerance. United States: N. p., 2019. Web. https://doi.org/10.1186/s12870-019-1900-1.
Jia, Huixia, Zhang, Jin, Li, Jianbo, Sun, Pei, Zhang, Yahong, Xin, Xuebing, Lu, Mengzhu, & Hu, Jianjun. Genome-wide transcriptomic analysis of a desert willow, Salix psammophila, reveals the function of hub genes SpMDP1 and SpWRKY33 in drought tolerance. United States. https://doi.org/10.1186/s12870-019-1900-1
Jia, Huixia, Zhang, Jin, Li, Jianbo, Sun, Pei, Zhang, Yahong, Xin, Xuebing, Lu, Mengzhu, and Hu, Jianjun. Thu . "Genome-wide transcriptomic analysis of a desert willow, Salix psammophila, reveals the function of hub genes SpMDP1 and SpWRKY33 in drought tolerance". United States. https://doi.org/10.1186/s12870-019-1900-1. https://www.osti.gov/servlets/purl/1557471.
@article{osti_1557471,
title = {Genome-wide transcriptomic analysis of a desert willow, Salix psammophila, reveals the function of hub genes SpMDP1 and SpWRKY33 in drought tolerance},
author = {Jia, Huixia and Zhang, Jin and Li, Jianbo and Sun, Pei and Zhang, Yahong and Xin, Xuebing and Lu, Mengzhu and Hu, Jianjun},
abstractNote = {Background: Drought is a major environmental constraint to plant growth, development and productivity. Compared with most willows that are generally susceptible to drought, the desert willow Salix psammophila has extraordinary adaptation to drought stress. However, its molecular basis of drought tolerance is still largely unknown.Results: During polyethylene glycol 6000 (PEG 6000)-simulated drought stress, we found that the osmotic adjustment substances were accumulated and the antioxidant enzyme activities were enhanced in S. psammophila roots. A total of 8172 differentially expressed genes were identified in roots of S. psammophila through RNA-Sequencing. Based on K-means clustering, their expression patterns were classified into nine clusters, which were enriched in several stress-related processes including transcriptional regulation, response to various stresses, cell death, etc. Moreover, 672 transcription factors from 45 gene families were differentially expressed under drought stress. Furthermore, a weighted gene co-expression network was constructed, and eight genes were identified as hub genes. We demonstrated the function of two hub genes, magnesium-dependent phosphatase 1 (SpMDP1) and SpWRKY33, through overexpression in Arabidopsis thaliana. Overexpression of the two hub genes enhanced the drought tolerance in transgenic plants, suggesting that the identification of candidate drought tolerance genes in this study was highly efficient and credible.Conclusions: Our study analyzed the physiological and molecular responses to drought stress in S. psammophila, and these results contribute to dissect the mechanism of drought tolerance of S. psammophila and facilitate identification of critical genes involved in drought tolerance for willow breeding.},
doi = {10.1186/s12870-019-1900-1},
journal = {BMC Plant Biology},
number = 1,
volume = 19,
place = {United States},
year = {2019},
month = {8}
}

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    Works referencing / citing this record:

    Colorimetric Method for Determination of Sugars and Related Substances
    journal, March 1956

    • DuBois, Michel.; Gilles, K. A.; Hamilton, J. K.
    • Analytical Chemistry, Vol. 28, Issue 3, p. 350-356
    • DOI: 10.1021/ac60111a017

    Transcriptome dynamics of Arabidopsis during sequential biotic and abiotic stresses
    journal, May 2016

    • Coolen, Silvia; Proietti, Silvia; Hickman, Richard
    • The Plant Journal, Vol. 86, Issue 3
    • DOI: 10.1111/tpj.13167

    Genome-scale transcriptome analysis of the desert poplar, Populus euphratica
    journal, March 2011


    Gene networks involved in drought stress response and tolerance
    journal, November 2006

    • Shinozaki, K.; Yamaguchi-Shinozaki, K.
    • Journal of Experimental Botany, Vol. 58, Issue 2
    • DOI: 10.1093/jxb/erl164

    Physiological and transcriptome analysis of heteromorphic leaves and hydrophilic roots in response to soil drying in desert Populus euphratica
    journal, September 2017


    Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
    journal, August 2005


    Time-Series Transcriptomics Reveals That AGAMOUS-LIKE22 Affects Primary Metabolism and Developmental Processes in Drought-Stressed Arabidopsis
    journal, February 2016

    • Bechtold, Ulrike; Penfold, Christopher A.; Jenkins, Dafyd J.
    • The Plant Cell, Vol. 28, Issue 2
    • DOI: 10.1105/tpc.15.00910

    Designing Microarray and RNA-Seq Experiments for Greater Systems Biology Discovery in Modern Plant Genomics
    journal, February 2015


    Towards a better understanding of protein changes in common bean under drought: A case study of N-glycoproteins
    journal, September 2017


    A Cotton MYB Transcription Factor, GbMYB5, is Positively Involved in Plant Adaptive Response to Drought Stress
    journal, February 2015

    • Chen, Tianzi; Li, Wenjuan; Hu, Xuehong
    • Plant and Cell Physiology, Vol. 56, Issue 5
    • DOI: 10.1093/pcp/pcv019

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    • Plant Physiology, Vol. 57, Issue 2
    • DOI: 10.1104/pp.57.2.315

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    • Li, Fei; Zhang, Huanru; Zhao, Husheng
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    • Lu, Xiang; Li, Qing-Tian; Xiong, Qing
    • The Plant Journal, Vol. 86, Issue 6
    • DOI: 10.1111/tpj.13181

    Genome-wide transcriptional response of Populus euphratica to long-term drought stress
    journal, October 2012


    Transcriptome analysis revealed the drought-responsive genes in Tibetan hulless barley
    journal, May 2016


    Arabidopsis RGLG2, Functioning as a RING E3 Ligase, Interacts with AtERF53 and Negatively Regulates the Plant Drought Stress Response
    journal, November 2011

    • Cheng, Mei-Chun; Hsieh, En-Jung; Chen, Jui-Hung
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    • DOI: 10.1104/pp.111.189738

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    journal, August 2010


    Climatic controls on sap flow dynamics and used water sources of Salix psammophila in a semi-arid environment in northwest China
    journal, July 2014


    Proline and reactive oxygen/nitrogen species metabolism is involved in the tolerant response of the invasive plant species Ailanthus altissima to drought and salinity
    journal, January 2014


    Drought stress and reactive oxygen species: production, scavenging and signaling
    journal, March 2008

    • Cruz de Carvalho, Maria Helena
    • Plant Signaling & Behavior, Vol. 3, Issue 3
    • DOI: 10.4161/psb.3.3.5536

    Protein damage, repair and proteolysis
    journal, February 2014

    • Chondrogianni, Niki; Petropoulos, Isabelle; Grimm, Stefanie
    • Molecular Aspects of Medicine, Vol. 35
    • DOI: 10.1016/j.mam.2012.09.001

    OsCML4 improves drought tolerance through scavenging of reactive oxygen species in rice
    journal, January 2015


    Genome-wide transcriptional and physiological responses to drought stress in leaves and roots of two willow genotypes
    journal, October 2015


    Water Stress, Growth, and Osmotic Adjustment
    journal, February 1976

    • Hsiao, T. C.; Acevedo, E.; Fereres, E.
    • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 273, Issue 927
    • DOI: 10.1098/rstb.1976.0026

    Growth responses of 15 Salix genotypes to temporary water stress are different from the responses to permanent water shortage
    journal, June 2010


    Poplar trees reconfigure the transcriptome and metabolome in response to drought in a genotype- and time-of-day-dependent manner
    journal, April 2015


    Reactive oxygen species homeostasis and signalling during drought and salinity stresses
    journal, April 2010


    Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels
    journal, November 1971


    Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle
    journal, January 2007


    Arabidopsis RZFP34/CHYR1, a Ubiquitin E3 Ligase, Regulates Stomatal Movement and Drought Tolerance via SnRK2.6-Mediated Phosphorylation
    journal, October 2015

    • Ding, Shuangcheng; Zhang, Bin; Qin, Feng
    • The Plant Cell, Vol. 27, Issue 11
    • DOI: 10.1105/tpc.15.00321

    Proline accumulation in plants: a review
    journal, April 2008


    Arabidopsis Sigma Factor Binding Proteins Are Activators of the WRKY33 Transcription Factor in Plant Defense
    journal, October 2011


    Arabidopsis WRKY33 Is a Key Transcriptional Regulator of Hormonal and Metabolic Responses toward Botrytis cinerea Infection
    journal, March 2012

    • Birkenbihl, Rainer P.; Diezel, Celia; Somssich, Imre E.
    • Plant Physiology, Vol. 159, Issue 1
    • DOI: 10.1104/pp.111.192641

    QTL analyses of drought tolerance and growth for a Salix dasyclados × Salix viminalis hybrid in contrasting water regimes
    journal, December 2004

    • Rönnberg-Wästljung, A. C.; Glynn, C.; Weih, M.
    • Theoretical and Applied Genetics, Vol. 110, Issue 3
    • DOI: 10.1007/s00122-004-1866-7

    Differential expression analysis for sequence count data
    journal, October 2010


    Genetic strategies for dissecting complex traits in biomass willows (Salix spp.)
    journal, November 2013


    Overexpression of OsERF48 causes regulation of OsCML16 , a calmodulin-like protein gene that enhances root growth and drought tolerance
    journal, March 2017

    • Jung, Harin; Chung, Pil Joong; Park, Su-Hyun
    • Plant Biotechnology Journal, Vol. 15, Issue 10
    • DOI: 10.1111/pbi.12716

    WGCNA: an R package for weighted correlation network analysis
    journal, December 2008


    Genome-wide transcriptome analysis of two maize inbred lines under drought stress
    journal, December 2009


    KEGG: Kyoto Encyclopedia of Genes and Genomes
    journal, January 2000

    • Kanehisa, Minoru; Goto, Susumu
    • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
    • DOI: 10.1093/nar/28.1.27

    The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase
    journal, October 1999

    • Jeong, Sangho; Trotochaud, Amy E.; Clark, Steven E.
    • The Plant Cell, Vol. 11, Issue 10
    • DOI: 10.1105/tpc.11.10.1925

    Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation
    journal, May 2010

    • Trapnell, Cole; Williams, Brian A.; Pertea, Geo
    • Nature Biotechnology, Vol. 28, Issue 5
    • DOI: 10.1038/nbt.1621

    Effect of drought on pigments, osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China
    journal, June 2011


    Arabidopsis Transcriptome Analysis under Drought, Cold, High-Salinity and ABA Treatment Conditions using a Tiling Array
    journal, June 2008

    • Matsui, A.; Ishida, J.; Morosawa, T.
    • Plant and Cell Physiology, Vol. 49, Issue 8
    • DOI: 10.1093/pcp/pcn101

    Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
    journal, November 2003


    Overexpression of a Calcium-Dependent Protein Kinase Confers Salt and Drought Tolerance in Rice by Preventing Membrane Lipid Peroxidation
    journal, May 2014

    • Campo, Sonia; Baldrich, Patricia; Messeguer, Joaquima
    • Plant Physiology, Vol. 165, Issue 2
    • DOI: 10.1104/pp.113.230268

    Rapid Estimates of Relative Water Content
    journal, February 1974

    • Smart, Richard E.; Bingham, Gail E.
    • Plant Physiology, Vol. 53, Issue 2
    • DOI: 10.1104/pp.53.2.258

    Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
    journal, December 1998


    Genome-wide survey and expression analysis of the stress-associated protein gene family in desert poplar, Populus euphratica
    journal, July 2016


    Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses
    journal, October 2008


    Temperature as a potent driver of regional forest drought stress and tree mortality
    journal, September 2012

    • Park Williams, A.; Allen, Craig D.; Macalady, Alison K.
    • Nature Climate Change, Vol. 3, Issue 3
    • DOI: 10.1038/nclimate1693