Genome-wide identification and characterization of ABA receptor PYL/RCAR gene family reveals evolution and roles in drought stress in Nicotiana tabacum

BackgroundAbscisic acid (ABA) is an important phytohormone for plant growth, development and responding to stresses such as drought, salinity, and pathogen infection. Pyrabactin Resistance 1 (PYR1)/PYR1-Like (PYL)/Regulatory Component of ABA Receptor (RCAR) (hereafter referred to as PYLs) has been identified as the ABA receptors. The PYL family members have been well studied in many plants. However, the members of PYL family have not been systematically identified at genome level in cultivated tobacco (Nicotiana tabacum) and its two ancestors. In this study, the phylogenic relationships, chromosomal distribution, gene structures, conserved motifs/regions, and expression profiles of NtPYLs were analyzed.ResultsWe identified 29, 11, 16 PYLs in the genomes of allotetraploid N. tabacum, and its two diploid ancestors N. tomentosiformis and N. sylvestris, respectively. The phylogenetic analysis revealed that NtPYLs can be divided into three subfamilies, and each NtPYL has one counterpart in N. sylvestris or N. tomentosiformis. Based on microarray analysis of NtPYL transcripts, four NtPYLs (from subfamily II, III), and five NtPYLs (from subfamily I) are highlighted as potential candidates for further functional characterization in N. tabacum seed development, response to ABA, and germination, and resistance to abiotic stresses, respectively. Interestingly, the expression profiles of members in the same NtPYL subfamily showed somehow similar patterns in tissues at different developmental stages and in leaves of seedlings under drought stress, suggesting particular NtPYLs might have multiple functions in both plant development and drought stress response.ConclusionsNtPYLs are highlighted for important functions in seed development, germination and response to ABA, and particular in drought tolerance. This work will not only shed light on the PYL family in tobacco, but also provides some valuable information for functional characterization of ABA receptors in N. tabacum.

[1]  Zhulong Chan.  Expression profiling of ABA pathway transcripts indicates crosstalk between abiotic and biotic stress responses in Arabidopsis. , 2012, Genomics.

[2]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[3]  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.

[4]  Jian-Kang Zhu,et al.  ABA receptors: the START of a new paradigm in phytohormone signalling. , 2010, Journal of experimental botany.

[5]  K. Jung,et al.  Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression , 2014, Journal of experimental botany.

[6]  E. Risseeuw,et al.  Characterization of Triticum aestivum Abscisic Acid Receptors and a Possible Role for These in Mediating Fusairum Head Blight Susceptibility in Wheat , 2016, PloS one.

[7]  E. Grill,et al.  Leveraging abscisic acid receptors for efficient water use in Arabidopsis , 2016, Proceedings of the National Academy of Sciences.

[8]  H. Xu,et al.  Thirsty plants and beyond: structural mechanisms of abscisic acid perception and signaling. , 2010, Current opinion in structural biology.

[9]  Yingfang Zhu,et al.  ABA receptor PYL9 promotes drought resistance and leaf senescence , 2016, Proceedings of the National Academy of Sciences.

[10]  Rodrigo Lopez,et al.  Clustal W and Clustal X version 2.0 , 2007, Bioinform..

[11]  M. Van Montagu,et al.  Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco , 2011, Proceedings of the National Academy of Sciences.

[12]  G. Phillips,et al.  Structural basis for selective activation of ABA receptors , 2010, Nature Structural &Molecular Biology.

[13]  Peter McCourt,et al.  Plant nuclear hormone receptors: a role for small molecules in protein-protein interactions. , 2010, Annual review of cell and developmental biology.

[14]  A. Mosquna,et al.  Non‐redundant functions of the dimeric ABA receptor BdPYL1 in the grass Brachypodium , 2017, The Plant journal : for cell and molecular biology.

[15]  Ke-Qin Zhang,et al.  Transcriptomic profile of tobacco in response to Phytophthora nicotianae infection , 2017, Scientific Reports.

[16]  K. Shinozaki,et al.  Genetics and Phosphoproteomics Reveal a Protein Phosphorylation Network in the Abscisic Acid Signaling Pathway in Arabidopsis thaliana , 2013, Science Signaling.

[17]  Yuan-Yue Shen,et al.  FaPYR1 is involved in strawberry fruit ripening. , 2011, Journal of experimental botany.

[18]  Jie Ren,et al.  Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress , 2011, Journal of experimental botany.

[19]  R. Matyášek,et al.  Genome evolution in allotetraploid Nicotiana , 2004 .

[20]  Chuangye Yan,et al.  Structural insights into the mechanism of abscisic acid signaling by PYL proteins , 2009, Nature Structural &Molecular Biology.

[21]  Chuangye Yan,et al.  Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol , 2009 .

[22]  Jian-Kang Zhu,et al.  Control of Plant Water Use by ABA Induction of Senescence and Dormancy: An Overlooked Lesson from Evolution. , 2017, Plant & cell physiology.

[23]  S. Cutler,et al.  Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonist-bound conformation , 2011, Proceedings of the National Academy of Sciences.

[24]  Yingfang Zhu,et al.  Reciprocal Regulation of the TOR Kinase and ABA Receptor Balances Plant Growth and Stress Response. , 2018, Molecular cell.

[25]  Chuangye Yan,et al.  Single Amino Acid Alteration between Valine and Isoleucine Determines the Distinct Pyrabactin Selectivity by PYL1 and PYL2* , 2010, The Journal of Biological Chemistry.

[26]  Jiahong Zhu,et al.  Identification and characterization of the abscisic acid (ABA) receptor gene family and its expression in response to hormones in the rubber tree , 2017, Scientific Reports.

[27]  Qingyun Bu,et al.  Characterization and Functional Analysis of Pyrabactin Resistance-Like Abscisic Acid Receptor Family in Rice , 2015, Rice.

[28]  S. Cutler,et al.  Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. , 2009, The Plant journal : for cell and molecular biology.

[29]  E. Nambara,et al.  Abscisic acid biosynthesis and catabolism. , 2005, Annual review of plant biology.

[30]  S. F. Yan,et al.  The molecular basis of ABA-independent inhibition of PP2Cs by a subclass of PYL proteins. , 2011, Molecular cell.

[31]  Adam Round,et al.  The abscisic acid receptor PYR1 in complex with abscisic acid , 2009, Nature.

[32]  Y. Fujita,et al.  Structural basis of abscisic acid signalling , 2009, Nature.

[33]  Jian-Kang Zhu,et al.  Interactions between soybean ABA receptors and type 2C protein phosphatases , 2013, Plant Molecular Biology.

[34]  Yizhou Wang,et al.  PYR/PYL/RCAR Abscisic Acid Receptors Regulate K+ and Cl− Channels through Reactive Oxygen Species-Mediated Activation of Ca2+ Channels at the Plasma Membrane of Intact Arabidopsis Guard Cells1[W][OPEN] , 2013, Plant Physiology.

[35]  Jia Li,et al.  Contrasting transcriptional responses of PYR1/PYL/RCAR ABA receptors to ABA or dehydration stress between maize seedling leaves and roots , 2016, BMC Plant Biology.

[36]  Thomas Hofmann,et al.  Combinatorial interaction network of abscisic acid receptors and coreceptors from Arabidopsis thaliana , 2017, Proceedings of the National Academy of Sciences.

[37]  Xiaohong Zhu,et al.  The ABA Receptor PYL8 Promotes Lateral Root Growth by Enhancing MYB77-Dependent Transcription of Auxin-Responsive Genes , 2014, Science Signaling.

[38]  Guang-xiao Yang,et al.  Brachypodium distachyon BdPP2CA6 Interacts with BdPYLs and BdSnRK2 and Positively Regulates Salt Tolerance in Transgenic Arabidopsis , 2017, Front. Plant Sci..

[39]  E. Grill,et al.  Closely related receptor complexes differ in their ABA selectivity and sensitivity. , 2010, The Plant journal : for cell and molecular biology.

[40]  Ji Wang,et al.  Genome-wide identification of ABA receptor PYL family and expression analysis of PYLs in response to ABA and osmotic stress in Gossypium , 2017, PeerJ.

[41]  J. Schroeder,et al.  Evolution of Abscisic Acid Synthesis and Signaling Mechanisms , 2011, Current Biology.

[42]  Brian F. Volkman,et al.  Agrochemical control of plant water use using engineered abscisic acid receptors , 2015, Nature.

[43]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[44]  Chuangye Yan,et al.  Identification and Characterization of ABA Receptors in Oryza sativa , 2014, PloS one.

[45]  M. Chase,et al.  Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. , 2011, Molecular biology and evolution.

[46]  Beom-Gi Kim,et al.  A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. , 2012, Journal of experimental botany.

[47]  C. Valon,et al.  Abscisic acid signal off the STARting block. , 2011, Molecular plant.

[48]  Katharine E. Hubbard,et al.  Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions. , 2010, Genes & development.

[49]  Chuangye Yan,et al.  Molecular basis for the selective and ABA-independent inhibition of PP2CA by PYL13 , 2013, Cell Research.

[50]  Jian‐Kang Zhu,et al.  Interaction network of core ABA signaling components in maize , 2018, Plant Molecular Biology.

[51]  S. Cutler,et al.  In vitro Reconstitution of an ABA Signaling Pathway , 2009, Nature.

[52]  T. Ying,et al.  Transcriptomic Analysis Reveals Possible Influences of ABA on Secondary Metabolism of Pigments, Flavonoids and Antioxidants in Tomato Fruit during Ripening , 2015, PloS one.

[53]  S. Cutler,et al.  Identification and Mechanism of ABA Receptor Antagonism , 2010, Nature Structural &Molecular Biology.

[54]  Hilde van der Togt,et al.  Publisher's Note , 2003, J. Netw. Comput. Appl..

[55]  Hui Su,et al.  Genome-wide analysis of PYL-PP2C-SnRK2s family in Camellia sinensis , 2020, Bioengineered.

[56]  Y. Fujita,et al.  Structure and function of abscisic acid receptors. , 2013, Trends in plant science.

[57]  S. Cutler,et al.  A Gate-Latch-Lock Mechanism for Hormone Signaling by Abscisic Acid Receptors , 2009, Nature.

[58]  Joseph R. Ecker,et al.  An ABA-increased interaction of the PYL6 ABA receptor with MYC2 Transcription Factor: A putative link of ABA and JA signaling , 2016, Scientific Reports.

[59]  J. Giraudat,et al.  Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. , 1994, Science.

[60]  Y. Wang,et al.  Overexpression of Poplar Pyrabactin Resistance-Like Abscisic Acid Receptors Promotes Abscisic Acid Sensitivity and Drought Resistance in Transgenic Arabidopsis , 2016, PLoS ONE.

[61]  S. Cutler,et al.  Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance , 2014, Journal of experimental botany.

[62]  S. Cutler,et al.  Abscisic acid: emergence of a core signaling network. , 2010, Annual review of plant biology.

[63]  E. Koonin,et al.  Adaptations of the helix‐grip fold for ligand binding and catalysis in the START domain superfamily , 2001, Proteins.

[64]  Jian‐Kang Zhu,et al.  The ABA receptor PYL9 together with PYL8 plays an important role in regulating lateral root growth , 2016, Scientific Reports.

[65]  Kenichi Hitomi,et al.  Structural Mechanism of Abscisic Acid Binding and Signaling by Dimeric PYR1 , 2009, Science.

[66]  E. Grill,et al.  Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors , 2009, Science.

[67]  H. Xue,et al.  EL1-like Casein Kinases Suppress ABA Signaling and Responses by Phosphorylating and Destabilizing the ABA Receptors PYR/PYLs in Arabidopsis. , 2018, Molecular plant.

[68]  Viswanathan Chinnusamy,et al.  Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. , 2003, Journal of experimental botany.

[69]  J. Noel,et al.  Co-evolution of Hormone Metabolism and Signaling Networks Expands Plant Adaptive Plasticity , 2016, Cell.