Genome-wide analysis of WD40 protein family and functional characterization of BvWD40-82 in sugar beet

Sugar beet is one of the most important sugar crops in the world. It contributes greatly to the global sugar production, but salt stress negatively affects the crop yield. WD40 proteins play important roles in plant growth and response to abiotic stresses through their involvement in a variety of biological processes, such as signal transduction, histone modification, ubiquitination, and RNA processing. The WD40 protein family has been well-studied in Arabidopsis thaliana, rice and other plants, but the systematic analysis of the sugar beet WD40 proteins has not been reported. In this study, a total of 177 BvWD40 proteins were identified from the sugar beet genome, and their evolutionary characteristics, protein structure, gene structure, protein interaction network and gene ontology were systematically analyzed to understand their evolution and function. Meanwhile, the expression patterns of BvWD40s under salt stress were characterized, and a BvWD40-82 gene was hypothesized as a salt-tolerant candidate gene. Its function was further characterized using molecular and genetic methods. The result showed that BvWD40-82 enhanced salt stress tolerance in transgenic Arabidopsis seedlings by increasing the contents of osmolytes and antioxidant enzyme activities, maintaining intracellular ion homeostasis and increasing the expression of genes related to SOS and ABA pathways. The result has laid a foundation for further mechanistic study of the BvWD40 genes in sugar beet tolerance to salt stress, and it may inform biotechnological applications in improving crop stress resilience.

[1]  X. Yao,et al.  Genome-wide identification of WD40 transcription factors and their regulation of the MYB-bHLH-WD40 (MBW) complex related to anthocyanin synthesis in Qingke (Hordeum vulgare L. var. nudum Hook. f.) , 2023, BMC Genomics.

[2]  Yao Chen,et al.  The mitochondrial ribosomal protein mRpL4 regulates Notch signaling , 2023, EMBO reports.

[3]  M. Černý,et al.  Abiotic Stress in Crop Production , 2023, International journal of molecular sciences.

[4]  Kun Xu,et al.  Physiological and molecular mechanism of ginger (Zingiber officinale Roscoe) seedling response to salt stress , 2023, Frontiers in Plant Science.

[5]  S. Isayenkov,et al.  The regulation of plant cell wall organisation under salt stress , 2023, Frontiers in Plant Science.

[6]  G. Xia,et al.  Allelic variation of TaWD40-4B.1 contributes to drought tolerance by modulating catalase activity in wheat , 2023, Nature Communications.

[7]  Haiying Tong,et al.  Insights into Adaptive Regulation of the Leaf-Petiole System: Strategies for Survival of Water Lily Plants under Salt Stress , 2023, International journal of molecular sciences.

[8]  Lu Long,et al.  The Na+/H+ antiporter GbSOS1 interacts with SIP5 and regulates salt tolerance in Gossypium barbadense. , 2023, Plant science : an international journal of experimental plant biology.

[9]  Shanshuo Zhu,et al.  Interplay between autophagy and proteasome during protein turnover. , 2023, Trends in plant science.

[10]  Y. Lan,et al.  Comprehensive analysis of MAPK gene family in Populus trichocarpa and physiological characterization of PtMAPK3-1 in response to MeJA induction. , 2023, Physiologia plantarum.

[11]  Sixue Chen,et al.  Functional Characterization of Sugar Beet M14 Antioxidant Enzymes in Plant Salt Stress Tolerance , 2022, Antioxidants.

[12]  Weisi Guo,et al.  Genome-wide characterization of the inositol transporters gene family in Populus and functional characterization of PtINT1b in response to salt stress. , 2022, International journal of biological macromolecules.

[13]  Z. Li,et al.  Genome-wide identification of WD40 superfamily in Cerasus humilis and functional characteristics of ChTTG1. , 2022, International journal of biological macromolecules.

[14]  Eryong Chen,et al.  OsABT Is Involved in Abscisic Acid Signaling Pathway and Salt Tolerance of Roots at the Rice Seedling Stage , 2022, International journal of molecular sciences.

[15]  M. Shariati,et al.  A comprehensive review of beetroot (Beta vulgaris L.) bioactive components in the food and pharmaceutical industries , 2022, Critical reviews in food science and nutrition.

[16]  Guiyan Yang,et al.  Identifying and expression analysis of WD40 transcription factors in walnut , 2022, The plant genome.

[17]  Wei-Jie Wang,et al.  RING finger and WD repeat domain 3 regulates proliferation and metastasis through the Wnt/β-catenin signalling pathways in hepatocellular carcinoma , 2022, World journal of gastroenterology.

[18]  M. Flaishman,et al.  Genome-Wide Analysis of Anthocyanin Biosynthesis Regulatory WD40 Gene FcTTG1 and Related Family in Ficus carica L. , 2022, Frontiers in Plant Science.

[19]  R. Ren,et al.  The E3 Ligase GmPUB21 Negatively Regulates Drought and Salinity Stress Response in Soybean , 2022, International journal of molecular sciences.

[20]  Weiwei Luo,et al.  WD repeat domain 62 (WDR62) promotes resistance of colorectal cancer to oxaliplatin through modulating mitogen-activated protein kinase (MAPK) signaling , 2022, Bioengineered.

[21]  Q. Qiu,et al.  Roles of TOR signaling in nutrient deprivation and abiotic stress. , 2022, Journal of plant physiology.

[22]  Yuan Zhang,et al.  RING Zinc Finger Proteins in Plant Abiotic Stress Tolerance , 2022, Frontiers in Plant Science.

[23]  A. Fernie,et al.  Convergent selection of a WD40 protein that enhances grain yield in maize and rice , 2022, Science.

[24]  Joo Young Lee,et al.  FBXW7-mediated ERK3 degradation regulates the proliferation of lung cancer cells , 2022, Experimental & Molecular Medicine.

[25]  H. Yoo,et al.  Proline-serine-threonine-repeat region of MDC1 mediates Chk1 phosphorylation and the DNA double-strand break repair. , 2021, The international journal of biochemistry & cell biology.

[26]  Shuai Gao,et al.  The F-box E3 ubiquitin ligase AtSDR is involved in salt and drought stress responses in Arabidopsis. , 2021, Gene.

[27]  Li-an Xu,et al.  Overexpression of the Ginkgo biloba WD40 gene GbLWD1-like improves salt tolerance in transgenic Populus. , 2021, Plant science : an international journal of experimental plant biology.

[28]  E. Septiningsih,et al.  OsCOP1 regulates embryo development and flavonoid biosynthesis in rice (Oryza sativa L.) , 2021, Theoretical and Applied Genetics.

[29]  Changle Ma,et al.  Regulation of Plant Responses to Salt Stress , 2021, International journal of molecular sciences.

[30]  A. Anand,et al.  Raffinose accumulation and preferential allocation of carbon (14 C) to developing leaves impart salinity tolerance in sugar beet. , 2021, Physiologia plantarum.

[31]  F. Azeem,et al.  Genomic analysis of WD40 protein family in the mango reveals a TTG1 protein enhances root growth and abiotic tolerance in Arabidopsis , 2021, Scientific Reports.

[32]  H. Koga,et al.  A novel WD40-repeat protein involved in formation of epidermal bladder cells in the halophyte quinoa , 2020, Communications biology.

[33]  Olfat Al-Harazi,et al.  Expression profiling of WD40 family genes including DDB1- and CUL4- associated factor (DCAF) genes in mice and human suggests important regulatory roles in testicular development and spermatogenesis , 2020, BMC genomics.

[34]  Jin-Yong Hu,et al.  Genome-wide identification of WD40 genes reveals a functional diversification of COP1-like genes in Rosaceae , 2020, Plant Molecular Biology.

[35]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[36]  G. Pandey,et al.  Plant protein phosphatases: What do we know about their mechanism of action? , 2020, The FEBS journal.

[37]  Shuai Liu,et al.  Systematic analysis of SmWD40s, and responding of SmWD40-170 to drought stress by regulation of ABA- and H2O2-induced stomal movement in Salvia miltiorrhiza bunge. , 2020, Plant physiology and biochemistry : PPB.

[38]  P. Schaap,et al.  The proppin Bcas3 and its interactor KinkyA localize to the early phagophore and regulate autophagy , 2020, Autophagy.

[39]  Charles S. P. Foster,et al.  Phylogenomic Insights into Deep Phylogeny of Angiosperms Based on Broad Nuclear Gene Sampling , 2020, Plant communications.

[40]  S. Almo,et al.  A binary arginine methylation switch on histone H3 Arginine 2 regulates its interaction with WDR5 , 2020, bioRxiv.

[41]  Nawwar Morelli A Peach , 2019, Cream City Review.

[42]  Chaozu He,et al.  AtKATANIN1 Modulates Microtubule Depolymerization and Reorganization in Response to Salt Stress in Arabidopsis , 2019, International journal of molecular sciences.

[43]  Jian‐Kang Zhu,et al.  Nucleocytoplasmic Trafficking of the Arabidopsis WD40 Repeat Protein XIW1 Regulates ABI5 Stability and Abscisic Acid Responses. , 2019, Molecular plant.

[44]  Olga Chernomor,et al.  IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era , 2019, bioRxiv.

[45]  Xi Wang,et al.  A WD40-Repeat Protein From the Recretohalophyte Limonium bicolor Enhances Trichome Formation and Salt Tolerance in Arabidopsis , 2019, Front. Plant Sci..

[46]  Liping Huang,et al.  An RNA-binding protein MUG13.4 interacts with AtAGO2 to modulate salinity tolerance in Arabidopsis. , 2019, Plant science : an international journal of experimental plant biology.

[47]  Wenjiao Zhu,et al.  Genome-wide identification and functional analysis of the WDR protein family in potato , 2019, 3 Biotech.

[48]  H. Xue,et al.  The ubiquitin-proteasome system in plant responses to environments. , 2019, Plant, cell & environment.

[49]  Mingliang Yu,et al.  Identification and characterization of WD40 superfamily genes in peach. , 2019, Gene.

[50]  Sixue Chen,et al.  Overexpression of a S-Adenosylmethionine Decarboxylase from Sugar Beet M14 Increased Araidopsis Salt Tolerance , 2019, International journal of molecular sciences.

[51]  Xin Hu,et al.  Genome-wide characterization of the cellulose synthase gene superfamily in Solanum lycopersicum. , 2019, Gene.

[52]  P. Carillo,et al.  Spatial and Temporal Profile of Glycine Betaine Accumulation in Plants Under Abiotic Stresses , 2019, Front. Plant Sci..

[53]  C. R. McClung,et al.  HOS15 Interacts with the Histone Deacetylase HDA9 and the Evening Complex to Epigenetically Regulate the Floral Activator GIGANTEA[OPEN] , 2019, Plant Cell.

[54]  L. Eichinger,et al.  The Role of ATG16 in Autophagy and The Ubiquitin Proteasome System , 2018, Cells.

[55]  Guang-xiao Yang,et al.  Genome-wide identification and analysis of WD40 proteins in wheat (Triticum aestivum L.) , 2018, BMC Genomics.

[56]  Dongping Zhang,et al.  OsRACK1A, encodes a circadian clock-regulated WD40 protein, negatively affect salt tolerance in rice , 2018, Rice.

[57]  Yan Guo,et al.  Unraveling salt stress signaling in plants. , 2018, Journal of integrative plant biology.

[58]  H. Salih,et al.  Genome-wide characterization, identification, and expression analysis of the WD40 protein family in cotton. , 2018, Genome.

[59]  S. Klinge,et al.  Assembly and structure of the SSU processome-a nucleolar precursor of the small ribosomal subunit. , 2018, Current opinion in structural biology.

[60]  M. Hülskamp,et al.  Physical, Functional and Genetic Interactions between the BEACH Domain Protein SPIRRIG and LIP5 and SKD1 and Its Role in Endosomal Trafficking to the Vacuole in Arabidopsis , 2017, Front. Plant Sci..

[61]  Wei Wang,et al.  TaPUB1, a Putative E3 Ligase Gene from Wheat, Enhances Salt Stress Tolerance in Transgenic Nicotiana benthamiana , 2017, Plant & cell physiology.

[62]  Sixue Chen,et al.  Overexpression of S-Adenosyl-l-Methionine Synthetase 2 from Sugar Beet M14 Increased Arabidopsis Tolerance to Salt and Oxidative Stress , 2017, International journal of molecular sciences.

[63]  N. Tuteja,et al.  Function of heterotrimeric G-protein γ subunit RGG1 in providing salinity stress tolerance in rice by elevating detoxification of ROS , 2017, Planta.

[64]  Yan Zhang,et al.  Naturally Occurring Off-Switches for CRISPR-Cas9 , 2016, Cell.

[65]  Dongping Zhang,et al.  Ability to Remove Na+ and Retain K+ Correlates with Salt Tolerance in Two Maize Inbred Lines Seedlings , 2016, Front. Plant Sci..

[66]  Hongbo Liu,et al.  OsPEX11, a Peroxisomal Biogenesis Factor 11, Contributes to Salt Stress Tolerance in Oryza sativa , 2016, Front. Plant Sci..

[67]  E. Hurt,et al.  Architecture of the 90S Pre-ribosome: A Structural View on the Birth of the Eukaryotic Ribosome , 2016, Cell.

[68]  Ian Sillitoe,et al.  Functional innovation from changes in protein domains and their combinations. , 2016, Current opinion in structural biology.

[69]  Xia Li,et al.  Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses , 2015, Plant Cell Reports.

[70]  A. Pareek,et al.  Histone chaperones in Arabidopsis and rice: genome-wide identification, phylogeny, architecture and transcriptional regulation , 2015, BMC Plant Biology.

[71]  Davide Heller,et al.  STRING v10: protein–protein interaction networks, integrated over the tree of life , 2014, Nucleic Acids Res..

[72]  Yongsheng Liu,et al.  The tomato DWD motif-containing protein DDI1 interacts with the CUL4-DDB1-based ubiquitin ligase and plays a pivotal role in abiotic stress responses. , 2014, Biochemical and biophysical research communications.

[73]  Zhonghai Ren,et al.  Genome-wide analysis of the WD-repeat protein family in cucumber and Arabidopsis , 2014, Molecular Genetics and Genomics.

[74]  R. Ravindhran,et al.  Characterisation and determination of in vitro antioxidant potential of betalains from Talinum triangulare (Jacq.) Willd. , 2013, Food chemistry.

[75]  S. Eddy,et al.  Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions , 2013, Nucleic acids research.

[76]  A. K. Mishra,et al.  Structure and regulatory networks of WD40 protein in plants , 2012, Journal of Plant Biochemistry and Biotechnology.

[77]  Guoxing Chen,et al.  OsLIS-L1 encoding a lissencephaly type-1-like protein with WD40 repeats is required for plant height and male gametophyte formation in rice , 2012, Planta.

[78]  Y. Ouyang,et al.  Genomic survey, expression profile and co-expression network analysis of OsWD40 family in rice , 2012, BMC Genomics.

[79]  Jeremy D. DeBarry,et al.  MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity , 2012, Nucleic acids research.

[80]  P. Genschik,et al.  MSI4/FVE interacts with CUL4–DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis , 2011, Proceedings of the National Academy of Sciences.

[81]  R. Russell,et al.  WD40 proteins propel cellular networks. , 2010, Trends in biochemical sciences.

[82]  L. Feldman,et al.  A rapid TRIzol‐based two‐step method for DNA‐free RNA extraction from Arabidopsis siliques and dry seeds , 2010, Biotechnology journal.

[83]  D. Bassham,et al.  Autophagy is required for tolerance of drought and salt stress in plants , 2009, Autophagy.

[84]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[85]  Toni Gabaldón,et al.  trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses , 2009, Bioinform..

[86]  Mineko Konishi,et al.  Identification of novel meristem factors involved in shoot regeneration through the analysis of temperature-sensitive mutants of Arabidopsis. , 2009, The Plant journal : for cell and molecular biology.

[87]  Thomas D. Schmittgen,et al.  Analyzing real-time PCR data by the comparative CT method , 2008, Nature Protocols.

[88]  X. Deng,et al.  Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 Forms a Nuclear E3 Ubiquitin Ligase with DDB1 and CUL4 That Is Involved in Multiple Plant Developmental Processes[W] , 2008, The Plant Cell Online.

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

[90]  V. Sundaresan,et al.  SLOW WALKER1, Essential for Gametogenesis in Arabidopsis, Encodes a WD40 Protein Involved in 18S Ribosomal RNA Biogenesis , 2005, The Plant Cell Online.

[91]  J. McIntosh,et al.  Mcl1p Is a Polymerase α Replication Accessory Factor Important for S-Phase DNA Damage Survival , 2005, Eukaryotic Cell.

[92]  Jill Herschleb,et al.  Functional Analysis of the RING-Type Ubiquitin Ligase Family of Arabidopsis1[w] , 2005, Plant Physiology.

[93]  Steven B Cannon,et al.  The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana , 2004, BMC Plant Biology.

[94]  P. Shannon,et al.  Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks , 2003 .

[95]  R. Roberts,et al.  Human Genome and Diseases:¶WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases , 2001, Cellular and Molecular Life Sciences CMLS.

[96]  F. McNally,et al.  Two domains of p80 katanin regulate microtubule severing and spindle pole targeting by p60 katanin. , 2000, Journal of cell science.

[97]  Temple F. Smith,et al.  The WD repeat: a common architecture for diverse functions. , 1999, Trends in biochemical sciences.

[98]  J. Mornon,et al.  Functional and structural characterization of the prp3 binding domain of the yeast prp4 splicing factor. , 1998, Journal of molecular biology.

[99]  Raman Nambudripad,et al.  The ancient regulatory-protein family of WD-repeat proteins , 1994, Nature.

[100]  M. Iqbal,et al.  Physicochemical Characteristics and Yield of Sugar Beet (Beta vulgaris L.) Cv. “California-Kws” Influenced with Irrigation Intervals , 2019, Sarhad Journal of Agriculture.