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Contents June 2016 • VOLUME 6 • ISSUE 6 • www.g3journal.org INVESTIGATIONS 1491–1502 Sdt97: A Point Mutation in the 59 Untranslated Region Confers Semidwarfism in Rice Jiping Tong, Zhengshu Han, Aonan Han, Xuejun Liu, Shiyong Zhang, Binying Fu, Jun Hu, Jingping Su, Shaoqing Li, Shengjun Wang, and Yingguo Zhu Semi-dwarfism is an important agronomic trait in rice breeding programs. In this study, the authors identified the mutant gene by a map-based cloning method. Sequence of the candidate genes revealed that a base transversion from G to C occurred in the 59 untranslated region of Sdt97. qRT-PCR results confirmed that the transversion induced obvious change in the expression pattern of Sdt97 at different growth and developmental stages. Transgenic of Sdt97 resulted in the restoration of semi-dwarfism of the mutant phenotype or displayed a dwarfer phenotype compared with the mutant. These results indicate that the mutant gene Sdt97 confers semi-dwarfism in rice. 1503–1511 Several Critical Cell Types, Tissues, and Pathways Are Implicated in Genome-Wide Association Studies for Systemic Lupus Erythematosus Lu Liu, Xianyong Yin, Leilei Wen, Chao Yang, Yujun Sheng, Yan Lin, Zhengwei Zhu, Changbing Shen, Yinjuan Shi, Yajie Zheng, Sen Yang, Xuejun Zhang, and Yong Cui In both Eastern Asian and Caucasian populations, Liu et al. observed that the expression level of SLE GWAS implicated genes was significantly elevated in the xeroderma pigentosum B cells (P # 1.00 · 1026), CD141 monocytes (P # 2.74 · 1024) and CD191 B cells (P # 2.00 · 1026), and plasmacytoid dendritic cells (pDCs) (P # 9.00 · 1026). The authors revealed that the SLE GWAS associated variants were more likely to reside in the expression quantitative trait locus in B lymphocytes (q1/q0 ¼ 2.15, P ¼ 1.23 · 10244) and DNase I hypersensitivity sites (DHSs) in CD141 monocytes (q1/q0 ¼ 1.41, P ¼ 0.08). This study sheds light on several immune cells and responses, as well as the regulatory effect of common variants in the pathogenesis of SLE. 1513–1523 Interconnections Between RNA-Processing Pathways Revealed by a Sequencing-Based Genetic Screen for Pre-mRNA Splicing Mutants in Fission Yeast Amy Larson, Benjamin Jung Fair, and Jeffrey A. Pleiss In this study, the authors present the development and implementation of a sequencing based reverse genetic screen designed to identify the complement of non-essential genes that impact pre-mRNA splicing in the fission yeast Schizosaccharomyces pombe. They simultaneously queried 3000 mutant strains for their impact on the splicing efficiency of two endogenous pre-mRNAs. A total of 61 genes were identified whose deletions resulted in defects in splicing; enriched among these were factors encoding known or predicted components of the spliceosome, heterochromatic silencing, and 39 end processing. Genome-wide analysis of splicing confirms splicing defects for many of these factors, revealing novel connections between these pathways. Volume 6 | June 2016 | ii 1525–1534 Local Ancestry Inference in a Large US-Based Hispanic/Latino Study: Hispanic Community Health Study/Study of Latinos (HCHS/SOL) Sharon R. Browning, Kelsey Grinde, Anna Plantinga, Stephanie M. Gogarten, Adrienne M. Stilp, Robert C. Kaplan, M. Larissa Avilés-Santa, Brian L. Browning, and Cathy C. Laurie Local ancestry calls in admixed individuals are useful for a variety of purposes, including admixture mapping and investigating population structure. Browning et al. used the RFMix method to call local ancestry is a large US-based study of 12,793 Hispanic/Latino individuals. After local ancestry calling, the authors calculated ancestry-specific principal components in order to better understand the population structure in these individuals. 1535–1539 Genomic Signatures of Experimental Adaptation to Antimicrobial Peptides in Staphylococcus aureus Paul R. Johnston, Adam J. Dobson, and Jens Rolff Evolution of AMP resistance is considered unlikely or even impossible, yet selection with AMPs leads to resistance in several species of bacteria. Numerous studies have screened for loci that determine AMP susceptibility, but little is known about the genomic changes that accompany resistance evolution. Using genome re-sequencing, the authors of this study identified mutations that arise during experimental evolution of AMP resistance in Staphylococcus aureus. AMP-specific mutations were identified, and a transposon mutant library was used to verify that a number of the identified genes directly determine AMP susceptibility. This suggests that different routes to evolve resistance are favored within a controlled genetic background. 1541–1548 Identification and Characterization of a cis-Regulatory Element for Zygotic Gene Expression in Chlamydomonas reinhardtii Takashi Hamaji, David Lopez, Matteo Pellegrini, and James Umen Diploid and haploid specific gene expression programs play pivotal roles in controlling life cycle transitions in green algae and land plants. Hamaji et al. used the green alga Chlamydomonas reinhardtii to identify an 11-mer enhancer they termed ZYRE (zygotic response element) that was enriched in promoters and introns of early zygotic genes. Reporter assays confirmed that ZYRE is necessary and sufficient to confer zygotic expression under the control of the transcription factor GSP1. The authors propose that ZYRE is bound and regulated by GSP1-GSM1 heterodimers whose land plant KNOXBELL homeodomain protein homologs are key regulators of diploid phase gene expression and development. 1549–1562 Quantitative Trait Locus Analysis of Mating Behavior and Male Sex Pheromones in Nasonia Wasps Wenwen Diao, Mathilde Mousset, Gavin J. Horsburgh, Cornelis J. Vermeulen, Frank Johannes, Louis van de Zande, Michael G. Ritchie, Thomas Schmitt, and Leo W. Beukeboom The study by Diao et al. contributes to the understanding of the evolution of reproductive isolation, which is an important issue in speciation biology. The authors investigated the mating behavior of the youngest species pair in the speciation model system of Nasonia parasitoid wasps. They performed a quantitative trait locus (QTL) analysis of male and female mating signals with neutral and candidate gene single nucleotide polymorphisms (SNP) markers. The authors show quantitative differences in male sex pheromones between the species that affect female receptivity. Lack of female interspecific mate discrimination QTL points at a polygenic basis for female choice with strong environmental effects. 1563–1571 New Software for the Fast Estimation of Population Recombination Rates (FastEPRR) in the Genomic Era Feng Gao, Chen Ming, Wangjie Hu, and Haipeng Li The authors of this study introduce FastEPRR, an extremely fast open-source software package that uses machine learning to estimate the population recombination rate (¼) from intraspecific DNA polymorphism data. It is based on the finite-site model, and a method is proposed to consider the effect of variable recombination rates within windows. When and the number of sampled diploid individuals is large enough (), the variance of remains slightly smaller than that of . Since FastEPRR requires far less computation time, the authors expect FastEPRR to be widely used for establishing genetic maps and studying recombination hotspots in the population genomic era. iii | Contents 1573–1584 Patterns of Genome-Wide Variation in Glossina fuscipes fuscipes Tsetse Flies from Uganda Andrea Gloria-Soria, W. Augustine Dunn, Erich L. Telleria, Benjamin R. Evans, Loyce Okedi, Richard Echodu, Wesley C. Warren, Michael J. Montague, Serap Aksoy, and Adalgisa Caccone The tsetse fly Glossina fuscipes fuscipes (Gff) is a vector for human African trypanosomiasis. Gloria-Soria et al. identified 73,000 polymorphisms across its genome for population genomics and association studies. They provide the first estimate of linkage disequilibrium (LD) in Glossina, which is an order of magnitude greater than Drosophila, and used it to increase the power of statistical tests to identify genomic associations with two epidemiological traits. They found that in Gff modest sample sizes can reveal significant genetic associations, likely facilitated by strong selection pressures and the extent of genomic LD, and discuss the implications of this finding for future studies. 1585–1595 Fungal Innate Immunity Induced by Bacterial Microbe-Associated Molecular Patterns (MAMPs) Simon Ipcho, Thomas Sundelin, Gitte Erbs, H. Corby Kistler, Mari-Anne Newman, and Stefan Olsson Innate immunity has been extensively studied in plants and animals. Although fungal hyphae constantly interact with bacteria in soil and many other environments, knowledge of fungal transcriptomic responses to bacterial presence is very limited. The hypothesis that fungi react to bacterial presence with responses resembling plants’ and animals’ innate immunity has not been investigated so far. The transcriptomics findings from this study show for the first time that a fungus reacts to purified bacterial microbe-associated molecular patterns (MAMPs), and it does so quickly and in a manner that resembles the innate immune responses of both animals and plants. 1597–1606 Comparative Genomics of Interreplichore Translocations in Bacteria: A Measure of Chromosome Topology? Supriya Khedkar and Aswin Sai Narain Seshasayee Chromosome compaction, besides helping pack genomic DNA within the limited confines of a cell, is intricately linked to cellular processes like replication and transcription. Chromosomes are not randomly compacted but adopt defined conformations. Chromosome conformation may also be influenced by its replication and by selection imposed by the organization of genes on the chromosome. Here, Khedkar and Seshasayee use comparative genomics to build translocation maps across many bacterial chromosomes. The authors show that these translocations rarely disrupt gene dosage or gene expression states and thereby obey constraints imposed by replication-dependent gene dosage effects. They suggest that these maps may help predict chromosome conformation as well. 1607–1616 A High-Resolution SNP Array-Based Linkage Map Anchors a New Domestic Cat Draft Genome Assembly and Provides Detailed Patterns of Recombination Gang Li, LaDeana W. Hillier, Robert A. Grahn, Aleksey V. Zimin, Victor A. David, Marilyn Menotti-Raymond, Rondo Middleton, Steven Hannah, Sher Hendrickson, Alex Makunin, Stephen J. O’Brien, Pat Minx, Richard K. Wilson, Leslie A. Lyons, Wesley C. Warren, and William J. Murphy Here the authors describe a high-resolution genetic linkage map of the domestic cat genome based on genotyping 453 domestic cats from several multi-generational pedigrees on the Illumina 63K SNP array. Their final sex-averaged maps span a total autosomal length of 4,464 cM, the longest described linkage map for any mammal, confirming length estimates from a previous microsatellite-based map. The linkage map was used to order and orient the scaffolds from a substantially more contiguous domestic cat genome assembly. 1617–1626 mRNA-Associated Processes and Their Influence on Exon-Intron Structure in Drosophila melanogaster Gildas Lepennetier and Francesco Catania Intracellular processes are known to affect several properties of messenger (m)RNAs in eukaryotic species. For example, capping strongly influences the lifetime of mRNAs as it renders these molecules resistant to the action of degrading enzymes. Another process, telescripting, prevents intruders that are able to affect protein length from accessing mRNAs. The authors’ findings suggest that mRNAassociated processes may perform more than these conventionally understood functions. More specifically, these processes may also actively influence the evolution of gene structure. This idea has farreaching implications for understanding the relative contribution of selection and intracellular forces to gene and protein evolution. Volume 6 | June 2016 | iv 1627–1633 The Immature Fiber Mutant Phenotype of Cotton (Gossypium hirsutum) Is Linked to a 22-bp Frame-Shift Deletion in a Mitochondria Targeted Pentatricopeptide Repeat Gene Gregory N. Thyssen, David D. Fang, Linghe Zeng, Xianliang Song, Christopher D. Delhom, Tracy L. Condon, Ping Li, and Hee Jin Kim The recessive immature fiber (im) gene reduces the degree of cotton fiber cell wall thickening in Gossypium hirsutum by a process that was previously shown to involve mitochondrial function. Here the authors present mapping-by-sequencing, which identified a 22-bp deletion in a pentatricopeptide repeat (PPR) gene that is completely linked to the phenotype in 2,837 F2 plants and is absent from all 163 cultivated varieties tested. This frame-shift mutation results in a transcript that cannot target a functional RNA-binding protein to mitochondria. Thus, PPR gene Gh_A03G0489 is a promising candidate gene at the im locus. 1635–1648 Multi-Population Selective Genotyping to Identify Soybean [Glycine max (L.) Merr.] Seed Protein and Oil QTLs Piyaporn Phansak, Watcharin Soonsuwon, David L. Hyten, Qijian Song, Perry B. Cregan, George L. Graef, and James E. Specht Selective genotyping (SG) is a resource-efficient QTL-detection tool wherein only the phenotypic extremes of single trait are genotyped in a bi-parental mapping population. SG is nominally used in one population at a time. The novelty of this study is that SG was concurrently applied to 48 F2 mapping populations. The authors’ research showed, as Navabi et al. (2009) predicted, that multi-population SG is a useful tool for surveying a large number of donor parent germplasm accessions exhibiting extreme SG-trait values to determine allelic status of each accession at the major QTLs controlling that trait. 1649–1659 Saccharomyces cerevisiae Tti2 Regulates PIKK Proteins and Stress Response Kyle S. Hoffman, Martin L. Duennwald, Jim Karagiannis, Julie Genereaux, Alexander S. McCarton, and Christopher J. Brandl Many molecular chaperones are highly abundant, are induced by proteotoxic stress, and assist the folding of a diverse set of client proteins. Here Hoffmann et al. show that in budding yeast even low levels of the essential co-chaperone Tti2 suffice for viability and that Tti2 is not induced upon heat stress. Their study suggests that Tti2 has a highly specific client repertoire that includes the key cell signaling molecules of the PIKK protein family, including Tor1, Mec1 and Tra1. Tti2 thus functions as a highly specialized yet essential molecular chaperone within protein quality control. 1661–1671 The Histone Variant H3.3 Is Enriched at Drosophila Amplicon Origins but Does Not Mark Them for Activation Neha P. Paranjape and Brian R. Calvi The histone variant H3.3 correlates with DNA replication origins in a number of organisms. In this manuscript, the authors tested the function of H3.3 at origins using a model system that is based on developmental gene amplification in the Drosophila ovary. They show that although H3.3 is highly enriched at amplicon origins, it is not required for their function. Their findings have broader impact for understanding the relationship between DNA replication and epigenome organization. Moreover, their results suggest that a defect in the initiation of DNA replication is not likely the cause of genome instability in H3.3 mutant pediatric glioblastomas. 1673–1685 A Genetic Map Between Gossypium hirsutum and the Brazilian Endemic G. mustelinum and Its Application to QTL Mapping Baohua Wang, Limei Liu, Dong Zhang, Zhimin Zhuang, Hui Guo, Xin Qiao, Lijuan Wei, Junkang Rong, O. Lloyd May, Andrew H. Paterson, and Peng W. Chee Among the seven tetraploid cotton species, little is known about transmission genetics and genome organization in Gossypium mustelinum. In this research, a G. hirsutum by G. mustelinum genetic map was constructed and compared to maps of other tetraploid cotton species, for which the authors proposed a parsimony-based evolutionary model since the divergence of tetraploid cottons from common ancestors. Quantitative trait locus (QTL) mapping of fiber elongation in advanced backcross populations demonstrated the value of the HM map. The HM map will serve as a valuable resource for QTL mapping and help clarify the evolutionary relationships between the tetraploid cotton genomes. 1687–1693 The Drosophila prage Gene, Required for Maternal Transcript Destabilization in Embryos, Encodes a Predicted RNA Exonuclease Jun Cui, Yun Wei Lai, Caroline V. Sartain, Rebecca M. Zuckerman, and Mariana F. Wolfner The Drosophila prage gene was previously shown to regulate the stability of maternal mRNAs in early embryos. Here, the authors identify the prage gene molecularly and show that it encodes a predicted RNA exonuclease. v | Contents 1695–1705 Synthetic Ligands of Cannabinoid Receptors Affect Dauer Formation in the Nematode Caenorhabditis elegans Pedro Reis Rodrigues, Tiffany K. Kaul, Jo-Hao Ho, Mark Lucanic, Kristopher Burkewitz, William B. Mair, Jason M. Held, Laura M. Bohn, and Matthew S. Gill The work of Reis-Rodrigues et al. elucidates the biology of dauer formation in Caenorhabditis elegans by showing a role for CB receptor ligands in affecting this important developmental process. The authors consider this study insightful not only in terms of further understanding a specific developmental phenotype but also conceptually, in their use of chemical screens to identify small molecule modulators of dauer formation, combined with genetic analysis. In addition, the finding that synthetic ligands of mammalian CB receptors have activity in an organism that lacks orthologs of CB receptors provides an opportunity for discovery of non-canonical actions of these compounds. 1707–1712 Evaluation of IRX Genes and Conserved Noncoding Elements in a Region on 5p13.3 Linked to Families with Familial Idiopathic Scoliosis and Kyphosis Cristina M. Justice, Kevin Bishop, Blake Carrington, Jim C. Mullikin, Kandice Swindle, Beth Marosy, Raman Sood, Nancy H. Miller, and Alexander F. Wilson The IRX1, IRX2 and IRX4 exons and the conserved non-coding elements in a linkage region were sequenced in 7 families with at least two individuals with kyphoscoliosis. No functional variants were identified. The strongest association was with rs12517904 (P ¼ 0.00004). The alternate allele of conserved non-coding rare variant, rs117273909, was only found in all individuals with kyphoscoliosis, and 2 of 3 individuals with scoliosis in one family. Zebrafish transgenesis performed with two overlapping fragments of 198 and 687 base pairs, containing either the wild type or alternate allele of rs117273909, suggests that this region acts as a regulatory element. 1713–1724 Genetic Interactions Between the Meiosis-Specific Cohesin Components, STAG3, REC8, and RAD21L Ayobami Ward, Jessica Hopkins, Matthew Mckay, Steve Murray, and Philip W. Jordan Using knockout mice we performed genetic analyses which demonstrate that cohesins containing STAG3 and REC8 are the main complex required for centromeric cohesion, and RAD21L cohesins are required for normal clustering of pericentromeric heterochromatin. Furthermore, the STAG3/REC8 and STAG3/RAD21L cohesins are the primary cohesins required for axis formation. 1725–1737 Binding Sites in the EFG1 Promoter for Transcription Factors in a Proposed Regulatory Network: A Functional Analysis in the White and Opaque Phases of Candida albicans Claude Pujol, Thyagarajan Srikantha, Yang-Nim Park, Karla J. Daniels, and David R. Soll ChIP-chip analysis has been used to identify 10 sites along the promoter of EFG1 of Candida albicans that bind six transcription factors, which have been incorporated into models of transcriptional networks that regulate the alternative white and opaque phenotype. EFG1 is differentially expressed in the alternative phases and regulates the white phenotype. The majority of individually targeted deletions and one combinatorial deletion of transcription factor binding sites had effects inconsistent with the differential expression of EFG1. Alternative explanations are considered. 1739–1749 Chromosome-Wide Impacts on the Expression of Incompatibilities in Hybrids of Tigriopus californicus Christopher S. Willett, Thiago G. Lima, Inna Kovaleva, and Lydia Hatfield Postzygotic reproductive isolation can cause dramatically skewed genotypic frequencies from Mendelian expectations in hybrids, caused by deleterious epistatic interactions. Two interesting findings emerge from this study of hybrid copepods about these interactions. First, sex-limited recombination influences whether regions of chromosomes are skewed or not, suggesting this factor could play an important part in early rounds of hybridization. Second, the deleterious interactions observed in this and previous studies appear to be inconsistent, suggesting that more complicated models of deleterious interactions may need to be considered beyond simple two-locus interactions. Volume 6 | June 2016 | vi 1751–1756 N-Ethyl-N-Nitrosourea (ENU) Mutagenesis Reveals an Intronic Residue Critical for Caenorhabditis elegans 39 Splice Site Function in Vivo Omar A. Itani, Stephane Flibotte, Kathleen J. Dumas, Chunfang Guo, Thomas Blumenthal, and Patrick J. Hu Most Caenorhabditis elegans forward genetic screens are conducted using ethyl methanesulfonate (EMS) as a mutagen, based on its predilection for generating G-to-A and C-to-T transitions. Here Itani et al. characterize dp664, an intronic T-to-G point mutation within a conserved 39 splice site octamer motif of the daf-12 gene that was isolated in a N-ethyl-N-nitrosourea (ENU) mutagenesis screen. dp664 causes loss of daf-12 function by abrogating mRNA splicing. This mutant exemplifies the power of using ENU as a mutagen to study the roles of octamer motifs as well as AU- and AT-rich motifs in nucleic acid function and regulation in vivo. 1757–1766 Genome Sequence and Analysis of a Stress-Tolerant, Wild-Derived Strain of Saccharomyces cerevisiae Used in Biofuels Research Sean J. McIlwain, David Peris, Maria Sardi, Oleg V. Moskvin, Fujie Zhan, Kevin S. Myers, Nicholas M. Riley, Alyssa Buzzell, Lucas S. Parreiras, Irene M. Ong, Robert Landick, Joshua J. Coon, Audrey P. Gasch, Trey K. Sato, and Chris Todd Hittinger More than 100 strains of the baker’s yeast Saccharomyces cerevisiae have had their genomes sequenced, but most genome assemblies do not fully cover the regions near the ends of chromosomes where novel genes generally reside. Here McIlwain et al. present the near-complete genome sequence of a stresstolerant strain of S. cerevisiae developed for the production of cellulosic biofuels from plant biomass. Unlike most industrial strains, this strain was recently derived from a wild isolate. The authors show that the ends of its chromosomes contain several novel genes that are predicted to encode functions related to stress tolerance and carbon metabolism. 1767–1776 Fine-Scale Crossover Rate Variation on the Caenorhabditis elegans X Chromosome Max R. Bernstein and Matthew V. Rockman The distribution of meiotic crossovers in nematode C. elegans is anomalous among model organisms. The dramatic rate heterogeneity that manifests as hotspots in most species is apparently absent in the autosomes of these worms. Here, an enormous new panel of recombinant Near-Isogenic Lines of C. elegans extends that finding to the worms’ X chromosomes, which behave differently from autosomes during meiosis. Despite the absence of hotspots, subtle crossover rate heterogeneity is associated with features of the DNA sequence and structure. 1777–1785 A Comprehensive Toolbox for Genome Editing in Cultured Drosophila melanogaster Cells Stefan Kunzelmann, Romy Böttcher, Ines Schmidts, and Klaus Förstemann The authors of this study presented a thoroughly optimized and highly scalable PCR-based approach for genome editing in cultured Drosophila cells. A comprehensive set of template vectors allows insertion of tags suitable for protein detection, expression quantification, live cell fluorescence microscopy and also heterologous expression control. All tags and two independent selection markers can be used with a single set of reagents. Kunzelmann et al. provided single-cell based quantification of the editing frequencies observed at several loci. Efficiencies of .80% can be reached with 60 nt of sequence homology in each PCR primer; long homology arms (targeting vector for one locus) do not result in higher yields. MUTANT SCREEN REPORT 1787–1792 Site-Directed Genome Knockout in Chicken Cell Line and Embryos Can Use CRISPR/Cas Gene Editing Technology Qisheng Zuo, Yinjie Wang, Shaoze Cheng, Chao Lian, Beibei Tang, Fei Wang, Zhenyu Lu, Yanqing Ji, Ruifeng Zhao, Wenhui Zhang, Kai Jin, Jiuzhou Song, Yani Zhang, and Bichun Li The authors of this study evaluated the gene knockout efficiency of this technique in somatic founder cells, non-founder ESCs, and embryos of Suqin yellow chickens. The knockout efficiency in the study was 15%–27%. It was the first CRISPR/Cas9-based gene knockout experiment in the domestic chicken. The technology and cell numbers were limiting factors for high gene knockout efficiency. Nevertheless, the authors’ results support the application of CRISPR/Cas9 for gene editing in the domestic chicken, providing a new method for characterizing gene function in this species. vii | Contents