Genetic basis of sRNA quantitative variation analyzed using an experimental population derived from an elite rice hybrid

We performed a genetic analysis of sRNA abundance in flag leaf from an immortalized F2 (IMF2) population in rice. We identified 53,613,739 unique sRNAs and 165,797 sRNA expression traits (s-traits). A total of 66,649 s-traits mapped 40,049 local-sQTLs and 30,809 distant-sQTLs. By defining 80,362 sRNA clusters, 22,263 sRNA cluster QTLs (scQTLs) were recovered for 20,249 of all the 50,139 sRNA cluster expression traits (sc-traits). The expression levels for most of s-traits from the same genes or the same sRNA clusters were slightly positively correlated. While genetic co-regulation between sRNAs from the same mother genes and between sRNAs and their mother genes was observed for a portion of the sRNAs, most of the sRNAs and their mother genes showed little co-regulation. Some sRNA biogenesis genes were located in distant-sQTL hotspots and showed correspondence with specific length classes of sRNAs suggesting their important roles in the regulation and biogenesis of the sRNAs. DOI: http://dx.doi.org/10.7554/eLife.03913.001

[1]  Makoto Matsuoka,et al.  OsSPL14 promotes panicle branching and higher grain productivity in rice , 2010, Nature Genetics.

[2]  Jinping Hua,et al.  Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[3]  James C. Carrington,et al.  Specialization and evolution of endogenous small RNA pathways , 2007, Nature Reviews Genetics.

[4]  Felix Krueger,et al.  Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications , 2011, Bioinform..

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

[6]  L. Quintana-Murci,et al.  A genomic portrait of the genetic architecture and regulatory impact of microRNA expression in response to infection , 2014, Genome research.

[7]  Daoxiu Zhou,et al.  Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs , 2006, Plant Molecular Biology.

[8]  C. Bonilla,et al.  RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing. , 2005, Genes & development.

[9]  C. Helliwell,et al.  Regulation of flowering time and floral patterning by miR172. , 2011, Journal of experimental botany.

[10]  Caroline G. L. Lee,et al.  Single Nucleotide Polymorphisms Associated with MicroRNA Regulation , 2013, Biomolecules.

[11]  Liang-Hu Qu,et al.  Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching , 2013, Nature Biotechnology.

[12]  Qian Qian,et al.  Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice , 2010, Nature Genetics.

[13]  Qifa Zhang,et al.  Genetic dissection of an elite rice hybrid revealed that heterozygotes are not always advantageous for performance. , 2002, Genetics.

[14]  Jun S. Song,et al.  Chromatin structure analyses identify miRNA promoters , 2008 .

[15]  Johannes Schumacher,et al.  A systematic eQTL study of cis–trans epistasis in 210 HapMap individuals , 2011, European Journal of Human Genetics.

[16]  V. Chiang,et al.  Stress-responsive microRNAs in Populus. , 2008, The Plant journal : for cell and molecular biology.

[17]  C. Haley,et al.  A simple regression method for mapping quantitative trait loci in line crosses using flanking markers , 1992, Heredity.

[18]  D. Kliebenstein Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. , 2009, Annual review of plant biology.

[19]  W. Huber,et al.  which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. MAnorm: a robust model for quantitative comparison of ChIP-Seq data sets , 2011 .

[20]  Qifa Zhang,et al.  Genetic and molecular bases of rice yield. , 2010, Annual review of plant biology.

[21]  C. Helliwell,et al.  Epigenetics in plants-vernalisation and hybrid vigour. , 2011, Biochimica et biophysica acta.

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

[23]  C. Molony,et al.  Genetic analysis of genome-wide variation in human gene expression , 2004, Nature.

[24]  M. Laakso,et al.  Genetic regulation of human adipose microRNA expression and its consequences for metabolic traits. , 2013, Human molecular genetics.

[25]  Jinghua Xiao,et al.  An expression quantitative trait loci-guided co-expression analysis for constructing regulatory network using a rice recombinant inbred line population , 2014, Journal of experimental botany.

[26]  Robert A. Martienssen,et al.  RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond , 2013, Nature Reviews Genetics.

[27]  W. Peacock,et al.  The role of epigenetics in hybrid vigour. , 2013, Trends in genetics : TIG.

[28]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[29]  P. Zamore,et al.  Small silencing RNAs: an expanding universe , 2009, Nature Reviews Genetics.

[30]  Rachel B. Brem,et al.  Trans-acting regulatory variation in Saccharomyces cerevisiae and the role of transcription factors , 2003, Nature Genetics.

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

[32]  E. Sontheimer,et al.  Origins and Mechanisms of miRNAs and siRNAs , 2009, Cell.

[33]  M. Pellegrini,et al.  Transcriptome and methylome interactions in rice hybrids , 2012, Proceedings of the National Academy of Sciences.

[34]  Qi Feng,et al.  Parent-independent genotyping for constructing an ultrahigh-density linkage map based on population sequencing , 2010, Proceedings of the National Academy of Sciences.

[35]  Sheng-hua Wang,et al.  Genome-Wide Analysis Reveals Diversity of Rice Intronic miRNAs in Sequence Structure, Biogenesis and Function , 2013, PloS one.

[36]  Hang He,et al.  Epigenetic Variations in Plant Hybrids and Their Potential Roles in Heterosis Jgg , 2013 .

[37]  Anton J. Enright,et al.  Extent, Causes, and Consequences of Small RNA Expression Variation in Human Adipose Tissue , 2012, PLoS genetics.

[38]  W. Peacock,et al.  Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor , 2011, Proceedings of the National Academy of Sciences.

[39]  Cai-guo Xu,et al.  A global analysis of QTLs for expression variations in rice shoots at the early seedling stage. , 2010, The Plant journal : for cell and molecular biology.

[40]  Charles E. Vejnar,et al.  Identification of cis- and trans-regulatory variation modulating microRNA expression levels in human fibroblasts. , 2011, Genome research.

[41]  Karl W. Broman,et al.  A model selection approach for the identification of quantitative trait loci in experimental crosses , 2002 .

[42]  Jinghua Xiao,et al.  Gains in QTL Detection Using an Ultra-High Density SNP Map Based on Population Sequencing Relative to Traditional RFLP/SSR Markers , 2011, PloS one.

[43]  M. Pooggin How Can Plant DNA Viruses Evade siRNA-Directed DNA Methylation and Silencing? , 2013, International journal of molecular sciences.

[44]  Jinping Hua,et al.  Genetic composition of yield heterosis in an elite rice hybrid , 2012, Proceedings of the National Academy of Sciences.

[45]  Jingyuan Fu,et al.  Regulatory network construction in Arabidopsis by using genome-wide gene expression quantitative trait loci , 2007, Proceedings of the National Academy of Sciences.

[46]  Ji Wan,et al.  Structure and activity of putative intronic miRNA promoters. , 2010, RNA.

[47]  J. Zhai,et al.  Biogenesis and function of rice small RNAs from non-coding RNA precursors. , 2013, Current opinion in plant biology.

[48]  Cole Trapnell,et al.  Ultrafast and memory-efficient alignment of short DNA sequences to the human genome , 2009, Genome Biology.

[49]  Brian S. Yandell,et al.  A Model Selection Approach for the Identification of Quantitative Trait Loci in Experimental Crosses, Allowing Epistasis , 2002, Genetics.

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

[51]  Michelle T. Juarez,et al.  microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity , 2004, Nature.

[52]  Q. Qian,et al.  SEMI-ROLLED LEAF1 Encodes a Putative Glycosylphosphatidylinositol-Anchored Protein and Modulates Rice Leaf Rolling by Regulating the Formation of Bulliform Cells1[W][OA] , 2012, Plant Physiology.

[53]  Mark Stitt,et al.  RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics , 2012, Nucleic Acids Res..

[54]  Danny S. Park,et al.  Genetic architecture of microRNA expression: implications for the transcriptome and complex traits. , 2012, American journal of human genetics.

[55]  Jitendra P Khurana,et al.  Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA Polymerase gene families and their expression analysis during reproductive development and stress in rice , 2008, BMC Genomics.

[56]  R. Sunkar,et al.  The role of microRNAs and other endogenous small RNAs in plant stress responses. , 2008, Biochimica et biophysica acta.