Short Small RNAs and heterosis in maize Variation and inheritance of small RNAs in maize inbreds and F 1 hybrids

Short title: Small RNAs and heterosis in maize 1 2 Author for contact details: Nathan Springer, springer@umn.edu 3 4 Title: Variation and inheritance of small RNAs in maize inbreds and F1 hybrids 5 6 Peter A. Crisp, Reza Hammond, Peng Zhou, Brieanne Vaillancourt, Anna Lipzen, Chris 7 Daum, Kerrie Barry, Natalia de Leon, C. Robin Buell, Shawn M. Kaeppler, Blake C. 8 Meyers, Candice N. Hirsch, Nathan M. Springer 9 10 Department of Plant and Microbial Biology, University of Minnesota, St Paul, MN, 55108 11 Center for Bioinformatics and Computational Biology, University of Delaware, Newark, Delaware, 12 19711 13 Department of Plant Biology, Michigan State University, East Lansing, MI, 48824 14 US Department of Energy Joint Genome Institute, Walnut Creek, CA 94598 15 Department of Agronomy, University of Wisconsin-Madison, Madison, WI 53706 16 Donald Danforth Plant Science Center, St Louis, MO, 63132 17 Division of Plant Sciences, 52 Agriculture Lab, University of Missouri, Columbia, Missouri 65211 18 Department of Agronomy and Plant Genetics, University of Minnesota, St Paul, MN, 55108 19 20 ORCID IDs: PAC (0000-0002-3655-0130), RH (0000-0002-7375-8563), BV (0000-0002-679521 5173), CRB (0000-0002-6727-4677) SMK (0000-0002-5964-1668), BCM (0000-0003-343622 6097), CNH (0000-0002-8833-3023), NMS (0000-0002-7301-4759). 23 24 One-sentence summary 25 Characterizing different small RNA populations reveals the roles of development and genotype 26 in expression variation of in maize inbreds and their hybrids. 27 28 Author Contributions 29 N.S., C.H., B.M., S.K., C.R.B., N.dL. conceived the experiment. B.V., A.L., C.D., K.B. performed 30 the experiments. P.C., R.H., P.Z. analyzed the data. P.C. and N.S. wrote the manuscript with 31 contributions from all authors. All authors have read and approved the manuscript. N.S. agrees 32 to serve as the author responsible for contact and ensures communication. 33 34 DOE supported this work via JGI and GLBRC. PAC and NMS were supported by a grant from 35 NSF (IOS-1802848). RH and BCM were supported by a grant from NSF (IOS-1754097). 36 37 38 39 40 Plant Physiology Preview. Published on October 1, 2019, as DOI:10.1104/pp.19.00817

[1]  Alex B. Brohammer,et al.  Highly Genotype- and Tissue-specific Single-Parent Expression Drives Dynamic Gene Expression Complementation in Maize Hybrids , 2019, bioRxiv.

[2]  Nathan M. Springer,et al.  Dynamic Patterns of Gene Expression Additivity and Regulatory Variation throughout Maize Development. , 2019, Molecular plant.

[3]  Nathan M. Springer,et al.  The genomic ecosystem of transposable elements in maize , 2019, bioRxiv.

[4]  Alex B. Brohammer,et al.  Transposable elements contribute to dynamic genome content in maize , 2019, bioRxiv.

[5]  C. Spillane,et al.  Epigenetics and Heterosis in Crop Plants , 2019, Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications.

[6]  F. Hochholdinger,et al.  Heterosis in plants , 2018, Current Biology.

[7]  Small RNA-based prediction of hybrid performance in maize , 2018, BMC Genomics.

[8]  A. Melchinger,et al.  Parental Expression Variation of Small RNAs Is Negatively Correlated with Grain Yield Heterosis in a Maize Breeding Population , 2018, Front. Plant Sci..

[9]  Shengjun Li,et al.  The functions of plant small RNAs in development and in stress responses , 2017, The Plant journal : for cell and molecular biology.

[10]  B. Meyers,et al.  Characterization of Plant Small RNAs by Next Generation Sequencing. , 2017, Current protocols in plant biology.

[11]  Kevin L. Schneider,et al.  Improved maize reference genome with single-molecule technologies , 2017, Nature.

[12]  R. Martienssen,et al.  The expanding world of small RNAs in plants , 2015, Nature Reviews Molecular Cell Biology.

[13]  Robert J. Schmitz,et al.  RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome , 2015, Proceedings of the National Academy of Sciences.

[14]  Transposable elements, mRNA expression level and strand-specificity of small RNAs are associated with non-additive inheritance of gene expression in hybrid plants , 2015, BMC Plant Biology.

[15]  W. Peacock,et al.  Epigenetic Changes in Hybrids , 2015, Plant Physiology.

[16]  Xiaoyu Zhang,et al.  Accessible DNA and Relative Depletion of H3K9me2 at Maize Loci Undergoing RNA-Directed DNA Methylation[W][OPEN] , 2014, Plant Cell.

[17]  Xiangfeng Wang,et al.  Dynamic parent-of-origin effects on small interfering RNA expression in the developing maize endosperm , 2014, BMC Plant Biology.

[18]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[19]  W. Peacock,et al.  Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids , 2014, Proceedings of the National Academy of Sciences.

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

[21]  Z. Chen,et al.  Genomic and epigenetic insights into the molecular bases of heterosis , 2013, Nature Reviews Genetics.

[22]  J. Kendall,et al.  The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA , 2013, Genome research.

[23]  Nathan M. Springer,et al.  Progress toward understanding heterosis in crop plants. , 2013, Annual review of plant biology.

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

[25]  Xiaoyu Zhang,et al.  CHH islands: de novo DNA methylation in near-gene chromatin regulation in maize , 2013, Genome research.

[26]  Beibei Chen,et al.  Conservation and divergence of transcriptomic and epigenomic variation in maize hybrids , 2013, Genome Biology.

[27]  Y. Li,et al.  The Inheritance Pattern of 24 nt siRNA Clusters in Arabidopsis Hybrids Is Influenced by Proximity to Transposable Elements , 2012, PloS one.

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

[29]  Wei Zhang,et al.  Repeat associated small RNAs vary among parents and following hybridization in maize , 2012, Proceedings of the National Academy of Sciences.

[30]  Andrew R. Bassett,et al.  Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs , 2012, The EMBO journal.

[31]  Y. Qi,et al.  Genome-Wide Analysis of DNA Methylation and Gene Expression Changes in Two Arabidopsis Ecotypes and Their Reciprocal Hybrids , 2012 .

[32]  E. Noor,et al.  Wheat Hybridization and Polyploidization Results in Deregulation of Small RNAs , 2011, Genetics.

[33]  James C. Schnable,et al.  Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss , 2011, Proceedings of the National Academy of Sciences.

[34]  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.

[35]  Xiaopeng Zhu,et al.  Expression analysis of miRNAs and highly-expressed small RNAs in two rice subspecies and their reciprocal hybrids. , 2010, Journal of integrative plant biology.

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

[37]  David C. Schwartz,et al.  Detailed Analysis of a Contiguous 22-Mb Region of the Maize Genome , 2009, PLoS genetics.

[38]  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.

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

[40]  Kan Nobuta,et al.  Distinct size distribution of endogenous siRNAs in maize: Evidence from deep sequencing in the mop1-1 mutant , 2008, Proceedings of the National Academy of Sciences.

[41]  F. Hochholdinger,et al.  Towards the molecular basis of heterosis. , 2007, Trends in plant science.

[42]  Nathan M. Springer,et al.  Nonadditive Expression and Parent-of-Origin Effects Identified by Microarray and Allele-Specific Expression Profiling of Maize Endosperm1[W][OA] , 2007, Plant Physiology.

[43]  James A. Birchler,et al.  In Search of the Molecular Basis of Heterosis , 2003, The Plant Cell Online.