Analysis of lncRNAs in Lupinus mutabilis (Tarwi) and Their Potential Role in Drought Response

Lupinus mutabilis is a legume with high agronomic potential and available transcriptomic data for which lncRNAs have not been studied. Therefore, our objective was to identify, characterize, and validate the drought-responsive lncRNAs in L. mutabilis. To achieve this, we used a multilevel approach based on lncRNA prediction, annotation, subcellular location, thermodynamic characterization, structural conservation, and validation. Thus, 590 lncRNAs were identified by at least two algorithms of lncRNA identification. Annotation with the PLncDB database showed 571 lncRNAs unique to tarwi and 19 lncRNAs with homology in 28 botanical families including Solanaceae (19), Fabaceae (17), Brassicaceae (17), Rutaceae (17), Rosaceae (16), and Malvaceae (16), among others. In total, 12 lncRNAs had homology in more than 40 species. A total of 67% of lncRNAs were located in the cytoplasm and 33% in exosomes. Thermodynamic characterization of S03 showed a stable secondary structure with −105.67 kcal/mol. This structure included three regions, with a multibranch loop containing a hairpin with a SECIS-like element. Evaluation of the structural conservation by CROSSalign revealed partial similarities between L. mutabilis (S03) and S. lycopersicum (Solyc04r022210.1). RT-PCR validation demonstrated that S03 was upregulated in a drought-tolerant accession of L. mutabilis. Finally, these results highlighted the importance of lncRNAs in tarwi improvement under drought conditions.

[1]  R. Varshney,et al.  miRNAs for crop improvement. , 2023, Plant physiology and biochemistry : PPB.

[2]  Howard Y. Chang,et al.  Long non-coding RNAs: definitions, functions, challenges and recommendations , 2023, Nature Reviews Molecular Cell Biology.

[3]  Hui Zhang,et al.  Overexpression of lncRNA77580 Regulates Drought and Salinity Stress Responses in Soybean , 2023, Plants.

[4]  R. Varshney,et al.  Developing drought‐smart, ready‐to‐grow future crops , 2022, The plant genome.

[5]  R. Spitale,et al.  Probing the dynamic RNA structurome and its functions , 2022, Nature Reviews Genetics.

[6]  S. Nambeesan,et al.  Full-length fruit transcriptomes of southern highbush (Vaccinium sp.) and rabbiteye (V. virgatum Ait.) blueberry , 2022, BMC Genomics.

[7]  Walter N. Moss,et al.  Thermodynamic and structural characterization of an EBV infected B-cell lymphoma transcriptome , 2022, NAR genomics and bioinformatics.

[8]  Yiming Mao,et al.  Integrative analyses of prognosis, tumor immunity, and ceRNA network of the ferroptosis-associated gene FANCD2 in hepatocellular carcinoma , 2022, Frontiers in Genetics.

[9]  J. Tao,et al.  Analysis of herbivore-responsive long noncoding ribonucleic acids reveals a subset of small peptide-coding transcripts in Nicotiana tabacum , 2022, Frontiers in Plant Science.

[10]  G. Zolla,et al.  The micronutrient content in underutilized crops: the Lupinus mutabilis sweet case , 2022, Scientific Reports.

[11]  G. Zolla,et al.  Closing the Gap in the “ABC” Model in Legumes: A Review , 2022, LEGUME RESEARCH - AN INTERNATIONAL JOURNAL.

[12]  Wei Yuan,et al.  Global Identification of White Lupin lncRNAs Reveals Their Role in Cluster Roots under Phosphorus Deficiency , 2022, International journal of molecular sciences.

[13]  Ewelina M. Sokolowska,et al.  Identification and functional annotation of long intergenic non-coding RNAs in Brassicaceae , 2022, The Plant cell.

[14]  P. Kolatkar,et al.  Long Non-Coding RNA and RNA-Binding Protein Interactions in Cancer: Experimental and Machine Learning Approaches. , 2022, Seminars in cancer biology.

[15]  M. Hidalgo,et al.  Evaluación de la susceptibilidad in vitro a esparteína, en cuatro cepas de Mycobacterium tuberculosis , 2022, Revista Peruana de Medicina Experimental y Salud Pública.

[16]  A. Love,et al.  Transcriptomic Reprogramming, Alternative Splicing and RNA Methylation in Potato (Solanum tuberosum L.) Plants in Response to Potato Virus Y Infection , 2022, Plants.

[17]  Byoung Ryong Jeong,et al.  Seleno-Amino Acids in Vegetables: A Review of Their Forms and Metabolism , 2022, Frontiers in Plant Science.

[18]  I. Ulitsky,et al.  Discovering functional motifs in long noncoding RNAs , 2022, Wiley interdisciplinary reviews. RNA.

[19]  Zhao-Yue Zhang,et al.  Towards a better prediction of subcellular location of long non-coding RNA , 2022, Frontiers of Computer Science.

[20]  R. Karamian,et al.  Identification of the Complex Interplay Between Nematode-Related lncRNAs and Their Target Genes in Glycine max L. , 2021, Frontiers in Plant Science.

[21]  Neeti Sanan‐Mishra,et al.  Non-Coding RNAs in Response to Drought Stress , 2021, International journal of molecular sciences.

[22]  K. Sanbonmatsu Getting to the bottom of lncRNA mechanism: structure–function relationships , 2021, Mammalian Genome.

[23]  Puwen Tan,et al.  RNALocate v2.0: an updated resource for RNA subcellular localization with increased coverage and annotation , 2021, Nucleic Acids Res..

[24]  M. Kumar,et al.  Metabolomics and Molecular Approaches Reveal Drought Stress Tolerance in Plants , 2021, International journal of molecular sciences.

[25]  Ting Wu,et al.  The Long Noncoding RNA MdLNC499 Bridges MdWRKY1 and MdERF109 Function to Regulate Early-Stage Light-Induced Anthocyanin Accumulation in Apple Fruit. , 2021, The Plant cell.

[26]  K. Siddique,et al.  Non-Coding RNAs in Legumes: Their Emerging Roles in Regulating Biotic/Abiotic Stress Responses and Plant Growth and Development , 2021, Cells.

[27]  T. Inada,et al.  Identification of a novel endogenous long non-coding RNA that inhibits selenoprotein P translation , 2021, Nucleic acids research.

[28]  Changning Liu,et al.  Data integration and evolutionary analysis of long non-coding RNAs in 25 flowering plants , 2021, BMC Genomics.

[29]  Siyu Han,et al.  Capsule-LPI: a LncRNA–protein interaction predicting tool based on a capsule network , 2021, BMC Bioinform..

[30]  M. Lodha,et al.  Functions of long non-coding RNA in Arabidopsis thaliana , 2021, Plant signaling & behavior.

[31]  K. Weeks SHAPE Directed Discovery of New Functions in Large RNAs. , 2021, Accounts of chemical research.

[32]  Hong-Bin Shen,et al.  lncLocator 2.0: a cell-line-specific subcellular localization predictor for long non-coding RNAs with interpretable deep learning , 2021, Bioinform..

[33]  Jiani Xing,et al.  LncRNA-Encoded Peptide: Functions and Predicting Methods , 2021, Frontiers in Oncology.

[34]  Sarah D. Diermeier,et al.  The lncRNA Toolkit: Databases and In Silico Tools for lncRNA Analysis , 2020, Non-coding RNA.

[35]  Jing Li,et al.  The computational approaches of lncRNA identification based on coding potential: Status quo and challenges , 2020, Computational and structural biotechnology journal.

[36]  Robert D. Finn,et al.  RNAcentral 2021: secondary structure integration, improved sequence search and new member databases , 2020, Nucleic Acids Res..

[37]  Nam-Hai Chua,et al.  PLncDB V2.0: a comprehensive encyclopedia of plant long noncoding RNAs , 2020, Nucleic Acids Res..

[38]  Xiaoqin Xia,et al.  A systematic evaluation of bioinformatics tools for identification of long noncoding RNAs , 2020, RNA.

[39]  S. Ramasamy,et al.  Effect of Abscisic acid and Selenium foliar sprays on drought mitigation in tomato (Solanum lycopersicum L.) , 2020 .

[40]  J. Espinoza,et al.  High Impact Weather Events in the Andes , 2020, Frontiers in Earth Science.

[41]  Xingli Ma,et al.  Genome-wide identification and analysis of long noncoding RNAs (lncRNAs) during seed development in peanut (Arachis hypogaea L.) , 2020, BMC Plant Biology.

[42]  D. Mathews,et al.  LinearPartition: linear-time approximation of RNA folding partition function and base-pairing probabilities , 2019, Bioinform..

[43]  T. Chan,et al.  Analysis of Soybean Long Non-Coding RNAs Reveals a Subset of Small Peptide-Coding Transcripts1[OPEN] , 2019, Plant Physiology.

[44]  Astrid Gall,et al.  Ensembl 2020 , 2019, Nucleic Acids Res..

[45]  Xuemei Chen,et al.  Plant Noncoding RNAs: Hidden Players in Development and Stress Responses. , 2019, Annual review of cell and developmental biology.

[46]  Kai Zhao,et al.  LinearFold: linear-time approximate RNA folding by 5'-to-3' dynamic programming and beam search , 2019, Bioinform..

[47]  Laura R. Ganser,et al.  The roles of structural dynamics in the cellular functions of RNAs , 2019, Nature Reviews Molecular Cell Biology.

[48]  E. Li,et al.  CNIT: a fast and accurate web tool for identifying protein-coding and long non-coding transcripts based on intrinsic sequence composition , 2019, Nucleic Acids Res..

[49]  G. Tartaglia,et al.  CROSSalive: a web server for predicting the in vivo structure of RNA molecules , 2019, bioRxiv.

[50]  Selene L. Fernandez-Valverde,et al.  Splicing conservation signals in plant long noncoding RNAs , 2019, bioRxiv.

[51]  Hongliang Zhu,et al.  Long Non-Coding RNAs: Rising Regulators of Plant Reproductive Development , 2019, Agronomy.

[52]  R. Smyth,et al.  The evolution of RNA structural probing methods: From gels to next‐generation sequencing , 2018, Wiley interdisciplinary reviews. RNA.

[53]  M. Hirai,et al.  Arabidopsis molybdenum cofactor sulfurase ABA3 contributes to anthocyanin accumulation and oxidative stress tolerance in ABA-dependent and independent ways , 2018, Scientific Reports.

[54]  D. Herschlag,et al.  The Story of RNA Folding, as Told in Epochs. , 2018, Cold Spring Harbor perspectives in biology.

[55]  Yanchun Liang,et al.  LncFinder: an integrated platform for long non-coding RNA identification utilizing sequence intrinsic composition, structural information and physicochemical property , 2018, Briefings Bioinform..

[56]  Hui Li,et al.  Genome-Wide Identification and Functional Prediction of Novel Drought-Responsive lncRNAs in Pyrus betulifolia , 2018, Genes.

[57]  Kotb Abdelmohsen,et al.  Cytoplasmic functions of long noncoding RNAs , 2018, Wiley interdisciplinary reviews. RNA.

[58]  C. Koncz,et al.  SELENOPROTEIN O is a chloroplast protein involved in ROS scavenging and its absence increases dehydration tolerance in Arabidopsis thaliana. , 2018, Plant science : an international journal of experimental plant biology.

[59]  Alexandros Armaos,et al.  A Method for RNA Structure Prediction Shows Evidence for Structure in lncRNAs , 2018, bioRxiv.

[60]  Shu Liu,et al.  Conservation analysis of long non-coding RNAs in plants , 2018, Science China Life Sciences.

[61]  P. Cui,et al.  A Nucleus-Localized Long Non-Coding RNA Enhances Drought and Salt Stress Tolerance[OPEN] , 2017, Plant Physiology.

[62]  Sibum Sung,et al.  Spatio-temporal analysis of coding and long noncoding transcripts during maize endosperm development , 2017, Scientific Reports.

[63]  Ge Gao,et al.  CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features , 2017, Nucleic Acids Res..

[64]  Shuxia Li,et al.  Genome-wide identification and functional prediction of cold and/or drought-responsive lncRNAs in cassava , 2017, Scientific Reports.

[65]  Michael Gribskov,et al.  Accurate Classification of RNA Structures Using Topological Fingerprints , 2016, PloS one.

[66]  James K. Hane,et al.  A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: insights into plant–microbe interactions and legume evolution , 2016, Plant biotechnology journal.

[67]  Mukesh Jain,et al.  Genome-wide analysis of long intergenic non-coding RNAs in chickpea and their potential role in flower development , 2016, Scientific Reports.

[68]  Rui Li,et al.  Understanding the Functions of Long Non-Coding RNAs through Their Higher-Order Structures , 2016, International journal of molecular sciences.

[69]  F. Nawaz,et al.  Selenium (Se) improves drought tolerance in crop plants--a myth or fact? , 2016, Journal of the science of food and agriculture.

[70]  Andreu Paytuví Gallart,et al.  GREENC: a Wiki-based database of plant lncRNAs , 2015, Nucleic Acids Res..

[71]  J. Rinn,et al.  Linking RNA biology to lncRNAs , 2015, Genome research.

[72]  J. A. Chekanova,et al.  Long non-coding RNAs and their functions in plants. , 2015, Current opinion in plant biology.

[73]  J. Pires,et al.  Positionally-conserved but sequence-diverged: identification of long non-coding RNAs in the Brassicaceae and Cleomaceae , 2015, BMC Plant Biology.

[74]  William Stafford Noble,et al.  The MEME Suite , 2015, Nucleic Acids Res..

[75]  D. Bartel,et al.  Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. , 2015, Cell reports.

[76]  E. Trotta,et al.  On the Normalization of the Minimum Free Energy of RNAs by Sequence Length , 2014, PloS one.

[77]  C. Brooks,et al.  Hierarchy of RNA functional dynamics. , 2014, Annual review of biochemistry.

[78]  N. Vorsa,et al.  The American cranberry mitochondrial genome reveals the presence of selenocysteine (tRNA-Sec and SECIS) insertion machinery in land plants. , 2014, Gene.

[79]  Steven R. Eichten,et al.  Genome-wide discovery and characterization of maize long non-coding RNAs , 2014, Genome Biology.

[80]  Robert P. Davey,et al.  Sequencing quality assessment tools to enable data-driven informatics for high throughput genomics , 2013, Front. Genet..

[81]  Y. Zhang,et al.  In vivo genome-wide profiling of RNA secondary structure reveals novel regulatory features , 2013, Nature.

[82]  H. Steinbrenner,et al.  Selenium homeostasis and antioxidant selenoproteins in brain: implications for disorders in the central nervous system. , 2013, Archives of biochemistry and biophysics.

[83]  M. Axtell Classification and comparison of small RNAs from plants. , 2013, Annual review of plant biology.

[84]  Hsiao-Lin V. Wang,et al.  The Role of the Arabidopsis Exosome in siRNA–Independent Silencing of Heterochromatic Loci , 2013, PLoS genetics.

[85]  N. Chua,et al.  Genome-Wide Analysis Uncovers Regulation of Long Intergenic Noncoding RNAs in Arabidopsis[C][W] , 2012, Plant Cell.

[86]  M. Abe,et al.  Regulation of reproductive development by non-coding RNA in Arabidopsis: to flower or not to flower , 2012, Journal of Plant Research.

[87]  B. Faircloth,et al.  Primer3—new capabilities and interfaces , 2012, Nucleic acids research.

[88]  P. Stadler,et al.  ViennaRNA Package 2.0 , 2011, Algorithms for Molecular Biology : AMB.

[89]  S. Butcher,et al.  The molecular interactions that stabilize RNA tertiary structure: RNA motifs, patterns, and networks. , 2011, Accounts of chemical research.

[90]  B. Jiménez,et al.  Influence of germination with different selenium solutions on nutritional value and cytotoxicity of lupin seeds. , 2009, Journal of agricultural and food chemistry.

[91]  Yong Zhang,et al.  CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine , 2007, Nucleic Acids Res..

[92]  P. Svoboda,et al.  Hairpin RNA: a secondary structure of primary importance , 2006, Cellular and Molecular Life Sciences CMLS.

[93]  M. Ishitani,et al.  The Arabidopsis LOS5/ABA3 Locus Encodes a Molybdenum Cofactor Sulfurase and Modulates Cold Stress– and Osmotic Stress–Responsive Gene Expression , 2001, The Plant Cell Online.

[94]  J. Sabina,et al.  Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. , 1999, Journal of molecular biology.

[95]  OUP accepted manuscript , 2022, Briefings In Bioinformatics.

[96]  Fundamentals of RNA Structure and Function , 2022, Learning Materials in Biosciences.

[97]  OUP accepted manuscript , 2021, Briefings In Bioinformatics.

[98]  Ming Chen,et al.  Computational Identification of miRNAs and Temperature-Responsive lncRNAs From Mango (Mangifera indica L.) , 2020, Frontiers in Genetics.

[99]  M. Rao Long Non Coding RNA Biology , 2017, Advances in Experimental Medicine and Biology.

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

[101]  V. Gladyshev,et al.  SECIS elements in the coding regions of selenoprotein transcripts are functional in higher eukaryotes , 2006 .

[102]  Robert Giegerich,et al.  RNAshapes: an integrated RNA analysis package based on abstract shapes. , 2006, Bioinformatics.

[103]  Lingling Wang,et al.  Genome-wide identi fi cation, characterization, and functional analysis of lncRNAs in Hevea brasiliensis , 2022 .