Analysis of non-coding transcriptome in rice and maize uncovers roles of conserved lncRNAs associated with agriculture traits.

Long non-coding RNAs (lncRNAs) have recently been found to widely exist in eukaryotes and play important roles in key biological processes. To extend our knowledge of lncRNAs in crop plants we performed both non-directional and strand-specific RNA-sequencing experiments to profile non-coding transcriptomes of various rice and maize organs at different developmental stages. Analysis of more than 3 billion reads identified 22 334 long intergenic non-coding RNAs (lincRNAs) and 6673 pairs of sense and natural antisense transcript (NAT). Many lincRNA genes were associated with epigenetic marks. Expression of rice lincRNA genes was significantly correlated with that of nearby protein-coding genes. A set of NAT genes also showed expression correlation with their sense genes. More than 200 rice lincRNA genes had homologous non-coding sequences in the maize genome. Much more lincRNA and NAT genes were derived from conserved genomic regions between the two cereals presenting positional conservation. Protein-coding genes flanking or having a sense-antisense relationship to these conserved lncRNA genes were mainly involved in development and stress responses, suggesting that the associated lncRNAs might have similar functions. Integrating previous genome-wide association studies (GWAS), we found that hundreds of lincRNAs contain trait-associated SNPs (single nucleotide polymorphisms [SNPs]) suggesting their putative contributions to developmental and agriculture traits.

[1]  J. Rinn,et al.  Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression , 2009, Proceedings of the National Academy of Sciences.

[2]  Teddy Jégu,et al.  Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. , 2014, Molecular cell.

[3]  Mark H. Wright,et al.  Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa , 2011, Nature communications.

[4]  Peter J. Bradbury,et al.  Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population , 2011, Nature Genetics.

[5]  W. Huber,et al.  Differential expression analysis for sequence count data , 2010 .

[6]  Bjarni J. Vilhjálmsson,et al.  Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines , 2010 .

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

[8]  Peter J. Bradbury,et al.  Genome-wide association study of leaf architecture in the maize nested association mapping population , 2011, Nature Genetics.

[9]  Huifeng Jiang,et al.  De Novo Origination of a New Protein-Coding Gene in Saccharomyces cerevisiae , 2008, Genetics.

[10]  M. Takeichi,et al.  The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons , 2007, Journal of Cell Science.

[11]  Lior Pachter,et al.  Sequence Analysis , 2020, Definitions.

[12]  D. Haussler,et al.  Aligning multiple genomic sequences with the threaded blockset aligner. , 2004, Genome research.

[13]  Nathan M. Springer,et al.  Mendelian and Non-Mendelian Regulation of Gene Expression in Maize , 2013, PLoS genetics.

[14]  Jihua Ding,et al.  A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice , 2012, Proceedings of the National Academy of Sciences.

[15]  Y. Qi,et al.  Global Epigenetic and Transcriptional Trends among Two Rice Subspecies and Their Reciprocal Hybrids[W] , 2010, Plant Cell.

[16]  K. Taylor,et al.  Genome-Wide Association , 2007, Diabetes.

[17]  K. McGinnis,et al.  Computational Identification and Functional Predictions of Long Noncoding RNA in Zea mays , 2012, PloS one.

[18]  F. Collins,et al.  Potential etiologic and functional implications of genome-wide association loci for human diseases and traits , 2009, Proceedings of the National Academy of Sciences.

[19]  Dawn H. Nagel,et al.  The B73 Maize Genome: Complexity, Diversity, and Dynamics , 2009, Science.

[20]  Jingyuan Fu,et al.  Human Disease-Associated Genetic Variation Impacts Large Intergenic Non-Coding RNA Expression , 2013, PLoS genetics.

[21]  Peter J. Bradbury,et al.  The Genetic Architecture of Maize Flowering Time , 2009, Science.

[22]  Peter J. Bradbury,et al.  Maize HapMap2 identifies extant variation from a genome in flux , 2012, Nature Genetics.

[23]  E. Wang,et al.  Analysis and design of RNA sequencing experiments for identifying isoform regulation , 2010, Nature Methods.

[24]  Qian Qian,et al.  Control of tillering in rice , 2003, Nature.

[25]  Ben Lehner,et al.  In search of antisense. , 2004, Trends in biochemical sciences.

[26]  Dominic P. Norris,et al.  The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus , 1992, Cell.

[27]  Howard Y. Chang,et al.  Genome regulation by long noncoding RNAs. , 2012, Annual review of biochemistry.

[28]  D. Schwartz,et al.  Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data , 2013, Rice.

[29]  C. Wahlestedt,et al.  Regulatory roles of natural antisense transcripts , 2009, Nature Reviews Molecular Cell Biology.

[30]  M. McMullen,et al.  Genetic Properties of the Maize Nested Association Mapping Population , 2009, Science.

[31]  T. Mikkelsen,et al.  Genome-wide maps of chromatin state in pluripotent and lineage-committed cells , 2007, Nature.

[32]  Carolyn J. Brown,et al.  The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus , 1992, Cell.

[33]  Xuemei Chen,et al.  Small RNAs and their roles in plant development. , 2009, Annual review of cell and developmental biology.

[34]  D. Bartel,et al.  Conserved Function of lincRNAs in Vertebrate Embryonic Development despite Rapid Sequence Evolution , 2011, Cell.

[35]  D. Bartel,et al.  lincRNAs: Genomics, Evolution, and Mechanisms , 2013, Cell.

[36]  S. Karlin,et al.  Finding the genes in genomic DNA. , 1998, Current opinion in structural biology.

[37]  V. Bajic,et al.  On the classification of long non-coding RNAs , 2013, RNA biology.

[38]  James A. Cuff,et al.  A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells , 2006, Cell.

[39]  J. Mattick,et al.  Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. , 2005, Genome research.

[40]  M. Furuno,et al.  Competition between a noncoding exon and introns: Gomafu contains tandem UACUAAC repeats and associates with splicing factor-1 , 2011, Genes to cells : devoted to molecular & cellular mechanisms.

[41]  Agnes P Chan,et al.  Uneven chromosome contraction and expansion in the maize genome. , 2006, Genome research.

[42]  S. Blackshaw,et al.  articleThe long noncoding RNA RNCR 2 directs mouse retinal cell specification , 2010 .

[43]  Jonathan D. G. Jones,et al.  Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping , 2010, Proceedings of the National Academy of Sciences.

[44]  Michael F. Lin,et al.  Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. , 2012, Genome research.

[45]  Shin Heu,et al.  Experimental Validation of , 1991 .

[46]  Qifa Zhang,et al.  Genome-wide association studies of 14 agronomic traits in rice landraces , 2010, Nature Genetics.

[47]  Cisca Wijmenga,et al.  From genome-wide association studies to disease mechanisms: celiac disease as a model for autoimmune diseases , 2012, Seminars in Immunopathology.

[48]  X. Liu,et al.  Genome-Wide and Organ-Specific Landscapes of Epigenetic Modifications and Their Relationships to mRNA and Small RNA Transcriptomes in Maize[W] , 2009, The Plant Cell Online.

[49]  Cole Trapnell,et al.  Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. , 2011, Genes & development.

[50]  M. Freeling,et al.  How to usefully compare homologous plant genes and chromosomes as DNA sequences. , 2008, The Plant journal : for cell and molecular biology.

[51]  Ying Li,et al.  Hominoid-Specific De Novo Protein-Coding Genes Originating from Long Non-Coding RNAs , 2012, PLoS genetics.

[52]  Michael F. Lin,et al.  Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals , 2009, Nature.

[53]  Justin O Borevitz,et al.  Genome-wide association studies in plants: the missing heritability is in the field , 2011, Genome Biology.

[54]  S. Batalov,et al.  Antisense Transcription in the Mammalian Transcriptome , 2005, Science.

[55]  Paul Theodor Pyl,et al.  HTSeq—a Python framework to work with high-throughput sequencing data , 2014, bioRxiv.

[56]  T B Nesterova,et al.  Characterization of the genomic Xist locus in rodents reveals conservation of overall gene structure and tandem repeats but rapid evolution of unique sequence. , 2001, Genome research.

[57]  César A. Hidalgo,et al.  Proto-genes and de novo gene birth , 2012, Nature.

[58]  Peter J. Bradbury,et al.  Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize , 2011, Proceedings of the National Academy of Sciences.

[59]  Sean R. Davis,et al.  NCBI GEO: archive for functional genomics data sets—update , 2012, Nucleic Acids Res..

[60]  Huan Wang,et al.  Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis , 2014, Genome research.

[61]  S. Rastan,et al.  Requirement for Xist in X chromosome inactivation , 1996, Nature.

[62]  Laurent Duret,et al.  The Xist RNA Gene Evolved in Eutherians by Pseudogenization of a Protein-Coding Gene , 2006, Science.

[63]  Keyan Zhao,et al.  Genetic Architecture of Aluminum Tolerance in Rice (Oryza sativa) Determined through Genome-Wide Association Analysis and QTL Mapping , 2011, PLoS genetics.

[64]  Tim R. Mercer,et al.  Differentiating Protein-Coding and Noncoding RNA: Challenges and Ambiguities , 2008, PLoS Comput. Biol..

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

[66]  L. Qu,et al.  Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice , 2014, Genome Biology.

[67]  Joy Bergelson,et al.  Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature , 2010, PLoS genetics.

[68]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[69]  K. Struhl Transcriptional noise and the fidelity of initiation by RNA polymerase II , 2007, Nature Structural &Molecular Biology.

[70]  Udayan Mohanty,et al.  Compact and ordered collapse of randomly generated RNA sequences , 2005, Nature Structural &Molecular Biology.