Dynamic Patterns of Gene Expression Additivity and Regulatory Variation throughout Maize Development

Aguilar-Rangel, 2017, Allele specific expression analysis identifies regulatory variation associated with stress-related genes in the Mexican highland maize landrace Palomero Toluqueño, PeerJ, 5, e3737, 10.7717/peerj.3737 Albert, 2015, The role of regulatory variation in complex traits and disease, Nat. Rev. Genet., 16, 197, 10.1038/nrg3891 Anders, 2015, HTSeq—a Python framework to work with high-throughput sequencing data, Bioinformatics, 31, 166, 10.1093/bioinformatics/btu638 Baldauf, 2016, Nonsyntenic genes drive tissue-specific dynamics of differential, nonadditive, and allelic expression patterns in maize hybrids, Plant Physiol., 171, 1144 Baldauf, 2018, Single-parent expression is a general mechanism driving extensive complementation of non-syntenic genes in maize hybrids, Curr. Biol., 28, 431, 10.1016/j.cub.2017.12.027 Belting, 1998, Modification of expression and cis-regulation of Hoxc8 in the evolution of diverged axial morphology, Proc. Natl. Acad. Sci. U S A, 95, 2355, 10.1073/pnas.95.5.2355 Birchler, 2010, Heterosis, Plant Cell, 22, 2105, 10.1105/tpc.110.076133 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Brohammer, 2017, The limited role of differential fractionation in genome content variation and function in maize (Zea mays L.) inbred lines, Plant J., 93, 131, 10.1111/tpj.13765 Chen, 2005, Contribution of transcriptional regulation to natural variations in Arabidopsis, Genome Biol., 6, R32, 10.1186/gb-2005-6-4-r32 Cheng, 2018, Gene retention, fractionation and subgenome differences in polyploid plants, Nat. Plants, 4, 258, 10.1038/s41477-018-0136-7 Cookson, 2009, Mapping complex disease traits with global gene expression, Nat. Rev. Genet., 10, 184, 10.1038/nrg2537 Downs, 2013, A developmental transcriptional network for maize defines coexpression modules, Plant Physiol., 161, 1830, 10.1104/pp.112.213231 Eichten, 2011, Heritable epigenetic variation among maize inbreds, PLoS Genet., 7, e1002372, 10.1371/journal.pgen.1002372 Flint-Garcia, 2009, Heterosis is prevalent for multiple traits in diverse maize germplasm, PLoS One, 4, e7433, 10.1371/journal.pone.0007433 Frary, 2000, fw2.2: a quantitative trait locus key to the evolution of tomato fruit size, Science, 289, 85, 10.1126/science.289.5476.85 Freeling, 2015, Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences, Curr. Opin. Genet. Dev., 35, 110, 10.1016/j.gde.2015.11.002 Goff, 2011, A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding, New Phytol., 189, 923, 10.1111/j.1469-8137.2010.03574.x Goff, 2013, Heterosis in elite hybrid rice: speculation on the genetic and biochemical mechanisms, Curr. Opin. Plant Biol., 16, 221, 10.1016/j.pbi.2013.03.009 Gore, 2009, A first-generation haplotype map of maize, Science, 326, 1115, 10.1126/science.1177837 Gruber, 2012, Contrasting properties of gene-specific regulatory, coding, and copy number mutations in Saccharomyces cerevisiae: frequency, effects, and dominance, PLoS Genet., 8, e1002497, 10.1371/journal.pgen.1002497 Guo, 2004, Allelic variation of gene expression in maize hybrids, Plant Cell, 16, 1707, 10.1105/tpc.022087 Guo, 2006, Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis, Theor. Appl. Genet., 113, 831, 10.1007/s00122-006-0335-x Hansey, 2012, Maize (Zea mays L.) genome diversity as revealed by RNA-sequencing, PLoS One, 7, e33071, 10.1371/journal.pone.0033071 Hawkins, 2014, Variation in allelic expression associated with a recombination hotspot in Zea mays, Plant J., 79, 375, 10.1111/tpj.12537 Hirsch, 2014, Insights into the maize pan-genome and pan-transcriptome, Plant Cell, 26, 121, 10.1105/tpc.113.119982 Hochholdinger, 2007, Towards the molecular basis of heterosis, Trends Plant Sci., 12, 427, 10.1016/j.tplants.2007.08.005 Holloway, 2011, Genome-wide expression quantitative trait loci (eQTL) analysis in maize, BMC Genomics, 12, 336, 10.1186/1471-2164-12-336 Huang, 2017, Construction and optimization of large gene co-expression network in maize using RNA-seq data, Plant Physiol., 175, 568, 10.1104/pp.17.00825 Jiao, 2017, Improved maize reference genome with single-molecule technologies, Nature, 546, 524, 10.1038/nature22971 Kim, 2015, HISAT: a fast spliced aligner with low memory requirements, Nat. Methods, 12, 357, 10.1038/nmeth.3317 Kremling, 2018, Dysregulation of expression correlates with rare-allele burden and fitness loss in maize, Nature, 555, 520, 10.1038/nature25966 Lemmon, 2014, The role of cis regulatory evolution in maize domestication, PLoS Genet., 10, e1004745, 10.1371/journal.pgen.1004745 Li, 2010, Fast and accurate long-read alignment with Burrows-Wheeler transform, Bioinformatics, 26, 589, 10.1093/bioinformatics/btp698 Li, 2013, Mendelian and non-Mendelian regulation of gene expression in maize, PLoS Genet., 9, e1003202, 10.1371/journal.pgen.1003202 Libault, 2010, An integrated transcriptome atlas of the crop model Glycine max, and its use in comparative analyses in plants, Plant J., 63, 86 Lippman, 2007, Heterosis: revisiting the magic, Trends Genet., 23, 60, 10.1016/j.tig.2006.12.006 Liu, 2017, Distant eQTLs and non-coding sequences play critical roles in regulating gene expression and quantitative trait variation in maize, Mol. Plant, 10, 414, 10.1016/j.molp.2016.06.016 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Marcon, 2017, Stability of single-parent gene expression complementation in maize hybrids upon water deficit stress, Plant Physiol., 173, 1247, 10.1104/pp.16.01045 Mazaheri, 2019, Genome-wide association analysis of stalk biomass and anatomical traits in maize, BMC Plant Biol., 10.1186/s12870-019-1653-x McKenna, 2010, The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res., 20, 1297, 10.1101/gr.107524.110 Metzger, 2016, Contrasting frequencies and effects of cis- and trans-regulatory mutations affecting gene expression, Mol. Biol. Evol., 33, 1131, 10.1093/molbev/msw011 Meyer, 2007, Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern, Plant Mol. Biol., 63, 381, 10.1007/s11103-006-9095-x Palovaara, 2017, Transcriptome dynamics revealed by a gene expression atlas of the early Arabidopsis embryo, Nat. Plants, 3, 894, 10.1038/s41477-017-0035-3 Paschold, 2012, Complementation contributes to transcriptome complexity in maize (Zea mays L.) hybrids relative to their inbred parents, Genome Res., 22, 2445, 10.1101/gr.138461.112 Paschold, 2014, Nonsyntenic genes drive highly dynamic complementation of gene expression in maize hybrids, Plant Cell, 26, 3939, 10.1105/tpc.114.130948 Robinson, 2010, A scaling normalization method for differential expression analysis of RNA-seq data, Genome Biol., 11, R25, 10.1186/gb-2010-11-3-r25 Schadt, 2003, Genetics of gene expression surveyed in maize, mouse and man, Nature, 422, 297, 10.1038/nature01434 Schaefer, 2014, Discovering functional modules across diverse maize transcriptomes using COB, the co-expression browser, PLoS One, 9, e99193, 10.1371/journal.pone.0099193 Schmid, 2005, A gene expression map of Arabidopsis thaliana development, Nat. Genet., 37, 501, 10.1038/ng1543 Schnable, 2015, Genome evolution in maize: from genomes back to genes, Annu. Rev. Plant Biol., 66, 329, 10.1146/annurev-arplant-043014-115604 Schnable, 2011, Genes identified by visible mutant phenotypes show increased bias toward one of two subgenomes of maize, PLoS One, 6, e17855, 10.1371/journal.pone.0017855 Schnable, 2013, Progress toward understanding heterosis in crop plants, Annu. Rev. Plant Biol., 64, 71, 10.1146/annurev-arplant-042110-103827 Schnable, 2011, Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss, Proc. Natl. Acad. Sci. U S A, 108, 4069, 10.1073/pnas.1101368108 Schnable, 2012, Genome-wide analysis of syntenic gene deletion in the grasses, Genome Biol. Evol., 4, 265, 10.1093/gbe/evs009 Sekhon, 2011, Genome-wide atlas of transcription during maize development, Plant J., 66, 553, 10.1111/j.1365-313X.2011.04527.x Springer, 2007, Allelic variation and heterosis in maize: how do two halves make more than a whole?, Genome Res., 17, 264, 10.1101/gr.5347007 Springer, 2007, Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize, Plant Cell, 19, 2391, 10.1105/tpc.107.052258 Stelpflug, 2016, An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development, Plant Genome, 9, 10.3835/plantgenome2015.04.0025 Stupar, 2006, Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid, Genetics, 173, 2199, 10.1534/genetics.106.060699 Stupar, 2008, Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis, BMC Plant Biol., 8, 33, 10.1186/1471-2229-8-33 Sun, 2018, Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes, Nat. Genet., 50, 1289, 10.1038/s41588-018-0182-0 Swanson-Wagner, 2006, All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents, Proc. Natl. Acad. Sci. U S A, 103, 6805, 10.1073/pnas.0510430103 Swanson-Wagner, 2009, Paternal dominance of trans-eQTL influences gene expression patterns in maize hybrids, Science, 326, 1118, 10.1126/science.1178294 Swanson-Wagner, 2010, Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor, Genome Res., 20, 1689, 10.1101/gr.109165.110 Swanson-Wagner, 2012, Reshaping of the maize transcriptome by domestication, Proc. Natl. Acad. Sci. U S A, 109, 11878, 10.1073/pnas.1201961109 Walley, 2016, Integration of omic networks in a developmental atlas of maize, Science, 353, 814, 10.1126/science.aag1125 Wang, 1999, The limits of selection during maize domestication, Nature, 398, 236, 10.1038/18435 Wang, 2010, A dynamic gene expression atlas covering the entire life cycle of rice, Plant J., 61, 752, 10.1111/j.1365-313X.2009.04100.x Waters, 2013, Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species, Proc. Natl. Acad. Sci. U S A, 110, 19639, 10.1073/pnas.1309182110 Waters, 2017, Natural variation for gene expression responses to abiotic stress in maize, Plant J., 89, 706, 10.1111/tpj.13414 Wimalanathan, 2018, Maize GO annotation—methods, evaluation, and review (maize-GAMER), Plant Direct, 2, e00052, 10.1002/pld3.52 Wittkopp, 2004, Evolutionary changes in cis and trans gene regulation, Nature, 430, 85, 10.1038/nature02698 Zhu, 2016, Integration of summary data from GWAS and eQTL studies predicts complex trait gene targets, Nat. Genet., 48, 481, 10.1038/ng.3538