Rice OsHSFA3 Gene Improves Drought Tolerance by Modulating Polyamine Biosynthesis Depending on Abscisic Acid and ROS Levels

Drought is a serious problem, which causes heavy yield losses for rice. Heat-shock factors (HSFs) had been implicated in tolerance to drought and high temperature. However, there has not been much functional characterization and mechanism clarification in rice. Previously, we found an HSF gene, OsHSFA3, was highly related with drought tolerance after screening from 10,000 different samples. Herein, we cloned the OsHSFA3 from rice and overexpressed it in Arabidopsis thaliana to study its regulatory mechanism of drought tolerance. Phenotypic and physiological assays of the transgenic Arabidopsis lines showed that overexpression of OsHSFA3 confers drought tolerance by reducing water loss and reactive oxygen species (ROS) levels, whereas it increases abscisic acid (ABA) levels. However, enzymatic antioxidants such as activity levels of superoxide dismutase, peroxidase and catalase were not significantly different between wild type and transgenic lines. Instead, we observed a significant increase in polyamine content, which was correlated with increased AtADC1, AtADC2, SPDS1 and SPMS expression levels. In silico and in vivo analyses confirmed that OsHSFA3 is a nuclear-localized gene. In addition, OsHSFA3 can bind to the promoter of AtADC1 and OsADC via a yeast one-hybrid assay. Overall, this study reveals that OsHSFA3 improves drought tolerance in Arabidopsis not only by increasing ABA levels, but also by modulating polyamine levels to maintain ROS homeostasis, therefore it could be a strong candidate to develop drought-tolerant rice cultivars.

[1]  Xueyong Li,et al.  Engineering Abiotic Stress Tolerance via CRISPR-Cas mediated genome editing. , 2020, Journal of experimental botany.

[2]  Shuxun Yu,et al.  The Cotton GhWRKY91 Transcription Factor Mediates Leaf Senescence and Responses to Drought Stress in Transgenic Arabidopsis thaliana , 2019, Front. Plant Sci..

[3]  Jae-Yean Kim,et al.  AtPR5K2, a PR5-Like Receptor Kinase, Modulates Plant Responses to Drought Stress by Phosphorylating Protein Phosphatase 2Cs , 2019, Front. Plant Sci..

[4]  P. Venditti,et al.  Physiological and Pathological Role of ROS: Benefits and Limitations of Antioxidant Treatment , 2019, International journal of molecular sciences.

[5]  M. Noman,et al.  Overexpression of GmCAMTA12 Enhanced Drought Tolerance in Arabidopsis and Soybean , 2019, International journal of molecular sciences.

[6]  A. Pareek,et al.  A unique bZIP transcription factor imparting multiple stress tolerance in Rice , 2019, Rice.

[7]  J. Chen,et al.  Analysis of Drought Tolerance and Associated Traits in Upland Cotton at the Seedling Stage , 2019, International journal of molecular sciences.

[8]  K. Dossa,et al.  Identification of putative drought-responsive genes in rice using gene co-expression analysis , 2019, Bioinformation.

[9]  K. Nahar,et al.  Polyamine Action under Metal/Metalloid Stress: Regulation of Biosynthesis, Metabolism, and Molecular Interactions , 2019, International journal of molecular sciences.

[10]  Muhammad Riaz,et al.  Ameliorative Effects of Biochar on Rapeseed (Brassica napus L.) Growth and Heavy Metal Immobilization in Soil Irrigated with Untreated Wastewater , 2019, Journal of Plant Growth Regulation.

[11]  A. Hussain,et al.  Combined use of Enterobacter sp. MN17 and zeolite reverts the adverse effects of cadmium on growth, physiology and antioxidant activity of Brassica napus , 2019, PloS one.

[12]  Kunbo Wang,et al.  Overexpression of Cotton a DTX/MATE Gene Enhances Drought, Salt, and Cold Stress Tolerance in Transgenic Arabidopsis , 2019, Front. Plant Sci..

[13]  S. Hussain,et al.  Interactive effects of drought and heat stresses on morpho-physiological attributes, yield, nutrient uptake and oxidative status in maize hybrids , 2019, Scientific Reports.

[14]  Yang Li,et al.  The cotton WRKY transcription factor (GhWRKY33) reduces transgenic Arabidopsis resistance to drought stress , 2019, Scientific Reports.

[15]  H. Nian,et al.  GmWRKY16 Enhances Drought and Salt Tolerance Through an ABA-Mediated Pathway in Arabidopsis thaliana , 2019, Front. Plant Sci..

[16]  Xueyong Li,et al.  DEGENERATED PANICLE AND PARTIAL STERILITY 1 ( DPS1 ) encodes a cystathionine b - synthase domain containing protein required for anther cuticle and panicle development in rice , 2019 .

[17]  Xueyong Li,et al.  Degenerated panicle and partial sterility 1 (DPS1) encodes a CBS domain containing protein required for anther cuticle and panicle development in rice. , 2019, The New phytologist.

[18]  S. Yang,et al.  Transcription factors WRKY11 and WRKY17 are involved in abiotic stress responses in Arabidopsis. , 2018, Journal of plant physiology.

[19]  Mehmood Ali Noor,et al.  Temperature Extremes in Cotton Production and Mitigation Strategies , 2018 .

[20]  S. Hussain,et al.  Chilling and Drought Stresses in Crop Plants: Implications, Cross Talk, and Potential Management Opportunities , 2018, Front. Plant Sci..

[21]  Mehmood Ali Noor,et al.  Mechanisms and molecular approaches for heat tolerance in rice (Oryza sativa L.) under climate change scenario , 2018 .

[22]  Mehmood Ali Noor,et al.  Identification of drought tolerant maize genotypes and seedling based morpho-physiological selection indices for crop improvement , 2018 .

[23]  F. Cheng,et al.  Relationship of ROS accumulation and superoxide dismutase isozymes in developing anther with floret fertility of rice under heat stress. , 2018, Plant physiology and biochemistry : PPB.

[24]  M. Margis-Pinheiro,et al.  Rice peroxisomal ascorbate peroxidase knockdown affects ROS signaling and triggers early leaf senescence. , 2017, Plant science : an international journal of experimental plant biology.

[25]  Xueyong Li,et al.  Arabidopsis E3 Ubiquitin Ligases PUB22 and PUB23 Negatively Regulate Drought Tolerance by Targeting ABA Receptor PYL9 for Degradation , 2017, International journal of molecular sciences.

[26]  F. Asch,et al.  Thermal stress impacts reproductive development and grain yield in rice. , 2017, Plant physiology and biochemistry : PPB.

[27]  Xiaosan Huang,et al.  PbrMYB21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene , 2017, Plant biotechnology journal.

[28]  J. F. Jiménez-Bremont,et al.  Hetero- and homodimerization of Arabidopsis thaliana arginine decarboxylase AtADC1 and AtADC2. , 2017, Biochemical and biophysical research communications.

[29]  Vivek Kumar,et al.  Abscisic Acid Signaling and Abiotic Stress Tolerance in Plants: A Review on Current Knowledge and Future Prospects , 2017, Front. Plant Sci..

[30]  Renee M. Brielmann,et al.  E2F coregulates an essential HSF developmental program that is distinct from the heat-shock response , 2016, Genes & development.

[31]  K. Shinozaki,et al.  Simultaneous Silencing of Two Arginine Decarboxylase Genes Alters Development in Arabidopsis , 2016, Front. Plant Sci..

[32]  etl,et al.  Genome wide analysis of heat shock transcription factor (HSF) family in chickpea and its comparison with Arabidopsis , 2016 .

[33]  Sung Chul Lee,et al.  Function of ABA in Stomatal Defense against Biotic and Drought Stresses , 2015, International journal of molecular sciences.

[34]  Ping Wu,et al.  The roots of future rice harvests , 2014, Rice.

[35]  Youzhi Ma,et al.  Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement in drought and heat stresses , 2014, BMC Genomics.

[36]  T. Berberich,et al.  POLYAMINE OXIDASE 1 from rice (Oryza sativa) is a functional ortholog of Arabidopsis POLYAMINE OXIDASE 5 , 2014, Plant signaling & behavior.

[37]  D. Hincha,et al.  Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought , 2014, Front. Plant Sci..

[38]  S. R. Voleti,et al.  Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits , 2013, Rice.

[39]  P. Khurana,et al.  A Seed Preferential Heat Shock Transcription Factor from Wheat Provides Abiotic Stress Tolerance and Yield Enhancement in Transgenic Arabidopsis under Heat Stress Environment , 2013, PloS one.

[40]  G. Luo,et al.  Over-expression of OsHsfA7 enhanced salt and drought tolerance in transgenic rice , 2013, BMB reports.

[41]  Youzhi Ma,et al.  Overexpression of TaHSF3 in Transgenic Arabidopsis Enhances Tolerance to Extreme Temperatures , 2013, Plant Molecular Biology Reporter.

[42]  Z. Zou,et al.  Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress. , 2012, Plant physiology and biochemistry : PPB.

[43]  B. Mueller‐Roeber,et al.  Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. japonica , 2012, AoB PLANTS.

[44]  A. Hameed,et al.  Heat Stress-Induced Cell Death, Changes in Antioxidants, Lipid Peroxidation, and Protease Activity in Wheat Leaves , 2011, Journal of Plant Growth Regulation.

[45]  Zhijin Zhang,et al.  Transcriptional Activation of OsDERF1 in OsERF3 and OsAP2-39 Negatively Modulates Ethylene Synthesis and Drought Tolerance in Rice , 2011, PloS one.

[46]  P. Khurana,et al.  Heat shock factors in rice (Oryza sativa L.): genome-wide expression analysis during reproductive development and abiotic stress , 2011, Molecular Genetics and Genomics.

[47]  Dabing Zhang,et al.  Rice MADS3 Regulates ROS Homeostasis during Late Anther Development[W][OA] , 2011, Plant Cell.

[48]  A. Tiburcio,et al.  Polyamine metabolic canalization in response to drought stress in Arabidopsis and the resurrection plant Craterostigma plantagineum , 2011, Plant signaling & behavior.

[49]  Jiang Ming-yi ABA up-regulates the expression of OsHsf genes in leaves of rice plants , 2010 .

[50]  M. Ashraf,et al.  Inducing drought tolerance in plants: recent advances. , 2010, Biotechnology advances.

[51]  Y. Kamiya,et al.  Measurement of abscisic acid and gibberellins by gas chromatography/mass spectrometry. , 2009, Methods in molecular biology.

[52]  Chuang Wang,et al.  Identification and expression analysis of OsHsfs in rice , 2009, Journal of Zhejiang University SCIENCE B.

[53]  Yonghua Wang,et al.  Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. , 2008, Journal of genetics and genomics = Yi chuan xue bao.

[54]  K. Toriyama,et al.  Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter , 2008, Plant Cell Reports.

[55]  K. Oda,et al.  Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis , 2008, Planta.

[56]  S. Tachibana,et al.  Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. , 2004, Plant & cell physiology.

[57]  K. Shinozaki,et al.  OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. , 2003, The Plant journal : for cell and molecular biology.

[58]  R. Mittler Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.