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Contents
November 2016
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VOLUME 6
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ISSUE 11
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www.g3journal.org
INVESTIGATIONS
3443–3453
Genomic Prediction of Single Crosses in the Early Stages of a Maize Hybrid Breeding Pipeline
Dnyaneshwar C. Kadam, Sarah M. Potts, Martin O. Bohn, Alexander E. Lipka, and Aaron J. Lorenz
Prediction of single-cross hybrid performance has been a major goal of plant breeders since the beginning
of hybrid breeding. The main objective of this study was to evaluate the potential of genomic prediction
for identifying superior single crosses early in the breeding pipeline. To accomplish these objectives, we
designed and analyzed a novel population of single-cross hybrids. Overall, our results suggest that genomic
prediction of the performance of single crosses made using random progenies from the early stages of the
breeding pipeline holds great potential to re-design hybrid breeding and increase its efficiency.
3455–3465
Proper Sterol Distribution Is Required for Candida albicans Hyphal Formation and Virulence
Paula McCourt, Hsing-Yin Liu, Josie E. Parker, Christina Gallo-Ebert, Melissa Donigan, Adam Bata,
Caroline Giordano, Steven L. Kelly, and Joseph T. Nickels Jr.
Arv1 is a highly conserved protein found in many pathogenic fungi. Arv1 proteins contain an Arv1
homology domain (AHD) containing a zinc-binding motif. Candida albicans strains lacking Arv1 are
avirulent. Here we present data that show that the AHD and zinc-binding domain are essential for C. albicans
virulence. We further show that Arv1 is required for maintaining proper sterol distribution during hyphal
formation and elongation. Thus we have presented novel data indicating that multiple domains of Arv1 are
required for virulence, and that maintaining proper sterol distribution is essential for pathogenicity.
3467–3474
Depletion of Shine-Dalgarno Sequences Within Bacterial Coding Regions Is Expression Dependent
Chuyue Yang, Adam J. Hockenberry, Michael C. Jewett, and Luís A. N. Amaral
Regulation of protein synthesis in bacteria involves a multitude of mechanisms affecting initiation,
elongation, and termination. Here, we investigate potential regulation related to the base-pairing
interaction between mRNAs and the anti-Shine-Dalgarno (aSD) sequence on elongating ribosomes. We
report a metric that quantifies the level of thermodynamic interaction between a gene and the
ribosomes, which can partially predict gene expression and growth rates in a diverse set of bacteria.
Including this mechanism into consideration when designing DNA for artificial protein synthesis in
bacteria may lead to enhanced expression vectors.
3475–3483
Multiple Transcript Properties Related to Translation Affect mRNA Degradation Rates in
Saccharomyces cerevisiae
Benjamin Neymotin, Victoria Ettorre, and David Gresham
Studies of individual mRNAs have shown that both cis and trans factors affect mRNA degradation rates.
However, the factors underlying transcriptome-wide variation in mRNA degradation rates are poorly
understood. We show that multiple transcript properties explain variation in mRNA degradation rates and
that a model incorporating these properties explains 50% of the genome-wide variance. Predictors of
mRNA degradation rates include transcript length, abundance, ribosome density, biased codon usage and
GC content of the third position in codons. Thus, a large fraction of variation in mRNA degradation rates
is determined by inherent properties of transcripts rather than specific regulatory mechanisms.
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3485–3495
First Draft Assembly and Annotation of the Genome of a California Endemic Oak Quercus lobata
Née (Fagaceae)
Victoria L. Sork, Sorel T. Fitz-Gibbon, Daniela Puiu, Marc Crepeau, Paul F. Gugger, Rachel Sherman,
Kristian Stevens, Charles H. Langley, Matteo Pellegrini, and Steven L. Salzberg
Oaks represent a valuable natural resource for multiple ecosystems of Northern Hemisphere with broad
interest in its genetics, ecology, conservation, and management. Here we present a genome assembly of
valley oak (Quercus lobata) using Illumina sequencing. Our assembly includes a draft nuclear genome,
a complete chloroplast genome, and annotation of both. The k-mer histograms indicate an approximate
diploid genome size of 700-740 Mb. A comparison with a recently published European oak (Quercus
robur) sequence indicates 93.1% similarity. The Q. lobata chloroplast genome shows 99% identity with
another North American oak, Q. rubra. Preliminary annotation yielded 61,773 predicted protein-coding
genes.
3497–3506
Marker-Based Estimates Reveal Significant Nonadditive Effects in Clonally Propagated Cassava
(Manihot esculenta): Implications for the Prediction of Total Genetic Value and the Selection of
Varieties
Marnin D. Wolfe, Peter Kulakow, Ismail Y. Rabbi, and Jean-Luc Jannink
In clonally propagated crops, like cassava (Manihot esculenta), non-additive genetic effects (i.e.
dominance and epistasis) are exploited by selecting superior genetic individuals as varieties. We
quantified the amount and nature of non-additive genetic variation for key traits in a breeding
population of African cassava using genome-wide marker-based models. We found significant
non-additive genetic variation, especially for yield and showed that prediction of total genetic value
correlated more strongly to observed phenotypes than did additive value. Our results suggest genomic
prediction models can be used to improve the efficiency of variety identification and testing pipelines in
cassava.
3507–3515
Suitability of Different Mapping Algorithms for Genome-Wide Polymorphism Scans with Pool-Seq
Data
Robert Kofler, Anna Maria Langmüller, Pierre Nouhaud, Kathrin Anna Otte, and Christian Schlötterer
The cost-effectiveness of sequencing pools of individuals (Pool-Seq) provides the basis for its
popularity. The impact of the mapping tools has not yet been evaluated. We demonstrate a substantial
impact of the mapping tools leading to characteristic false positives in genome-wide scans. Out of
14 evaluated algorithms novoalign, bwa mem and clc4 are most suitable for mapping Pool-Seq data.
Nevertheless, no single algorithm is sufficient for avoiding all false positives. We show that the
intersection of the results of two mapping algorithms provides a simple, yet effective strategy to
eliminate false positives.
3517–3524
A Pedigree-Based Map of Recombination in the Domestic Dog Genome
Christopher L. Campbell, Claude Bhérer, Bernice E. Morrow, Adam R. Boyko, and Adam Auton
Recombination hotspots in most mammals depends on the hotspot localization protein PRDM9. In
dogs, however, this protein has been inactivated by mutation. How has the dog recombination
landscape been affected by the absence of PRDM9? The authors analyze crossover placement using
domestic dog pedigress. Dog recombination is remarkably similar to humans at the broad scale, but
appears to be unexpectedly concentrated into a smaller proportion of total sequence. Crossover in dogs
is also regulated by interference, similar to humans but an order of magnitude stronger. How has the
lack of PRDM9 altered the evolutionary path of the dog genome?
3525–3532
Effect of Two Lipoprotein (a)-Associated Genetic Variants on Plasminogen Levels and Fibrinolysis
Hong Wang, Chan E. Hong, Joshua P. Lewis, Yanbei Zhu, Xing Wang, Xin Chu, Joshua Backman,
Ziying Hu, Peixin Yang, Christopher D. Still, Glenn S. Gerhard, and Mao Fu
The two genetic variants of rs3798220 and rs10455872 are independently associated with Lp(a) levels
and cardiovascular disease. It is unclear whether or not the two variants are associated with markers of
thrombosis. The aims of this study are to evaluate the two Lp(a)-associated genetic variants are
associated with PLG and fibrinolysis. We measured plasma Lp(a), PLG and clot lysis time in OOA
subjects and PLG mRNA expression in liver samples. We found that two SNPs were significantly
associated with Lp(a) levels, but not with PLG and fibrinolysis. Lp(a)-associated genetic variants were
not major genetic determinants for thrombosis.
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3533–3540
Epidermal Growth Factor Receptor Cell Survival Signaling Requires Phosphatidylcholine
Biosynthesis
Matt Crook, Awani Upadhyay, Liyana J. Ido, and Wendy Hanna-Rose
Cells receive constant signals that determine their life and death. Perturbed signaling leads to both
insufficient and excessive death, contributing to cancer and neural pathogenesis. We use Caenorhabditis
elegans to study a cell death program called excitotoxicity induced by inappropriate ion channel
stimulation. We show that this death is counteracted by signaling from the epidermal growth factor
receptor. We perform a genetic screen that reveals that biosynthesis of phosphatidlycholine is important
for survival signaling. In fact, dietary supplementation with phosphatidlycholine appears to protect the
cells from the death-inducing insult. This work has implications for therapeutic intervention to prevent
excitotoxic death.
3541–3551
The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila
Maternal-to-Zygotic Transition
Hua Luo, Xiao Li, Julie M. Claycomb, and Howard D. Lipshitz
During the Drosophila maternal-to-zygotic transition (MZT) Smaug binds to and directs degradation of
hundreds of maternal mRNAs. We show that zygotic production of over 70 species of miRNAs fails in
smaug mutants and that Smaug is also required for the synthesis and stability of a key miRISC
component, Argonaute 1. In smaug mutants, maternal mRNAs that are predicted targets of the
Smaug-dependent zygotic miRNAs fail to be cleared. Thus Smaug controls the MZT through direct
targeting of a subset of maternal mRNAs for degradation and, indirectly, through production of
miRISC, which controls clearance of a distinct subset of maternal mRNAs.
3553–3560
Temporal Expression of a Master Regulator Drives Synchronous Sporulation in Budding Yeast
Minghao Chia and Folkert J. van Werven
Budding yeast cells enter sporulation asynchronously, which makes it challenging to obtain stage
specific data using cell population based assays. Methods ensuring that cells enter sporulation
synchronously have been lacking. We find that cells undergo pre-meiotic DNA replication and meiosis
synchronously when the expression of the master regulator of sporulation, IME1, is induced at a specific
time during starvation. Thus temporal expression of IME1 is a key determinant for entry into
sporulation. The approach described here can be combined with other stage specific synchronization
methods may give new insights on this complex developmental program.
3561–3570
The Genetic Basis of Upland/Lowland Ecotype Divergence in Switchgrass (Panicum virgatum)
Elizabeth R. Milano, David B. Lowry, and Thomas E. Juenger
Switchgrass is a widespread native grass and economically valuable cellulosic biofuel crop. Two major
switchgrass ecotypes are a xeric northern climate upland, and a riparian southern lowland. We explore
the genetic architecture of ecotype divergence by mapping quantitative trait loci (QTL) for locally
adapted traits including flowering time, plant size, physiological processes, and disease resistance. We
use an outbred genetic cross to assemble a linkage map that encompasses ecotype variation. Our results
indicate that ecologically important traits in switchgrass have a complex genetic basis and that similar
loci may underlie divergence across the geographic range of the ecotypes.
3571–3580
Genome Sequencing of Chromosome 1 Substitution Lines Derived from Chinese Wild Mice Revealed
a Unique Resource for Genetic Studies of Complex Traits
Fuyi Xu, Tianzhu Chao, Yingming Liang, Kai Li, Shixian Hu, Maochun Wang, Yuxun Zhou,
Hongyan Xu, and Junhua Xiao
Taking the advantages of high genetic diversity and small haplotype blocks in wild mice, we have built
a population of Chinese wild mice derived chromosome 1 substitution lines. In this study, we identified
extensive genetic variants through whole genome sequencing of 18 lines of this population. The length
of the haplotype blocks very similar to that in human populations (, 100kb). There are also substantial
phenotypic variations between these lines and donor strain. All these findings suggest that this
population are very suitable for dissection the complex traits and could achieve a single gene mapping
resolution when conducting association studies.
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3581–3591
Divergent DNA Methylation Provides Insights into the Evolution of Duplicate Genes in Zebrafish
Zaixuan Zhong, Kang Du, Qian Yu, Yong E. Zhang, and Shunping He
We demonstrated that DNA methylation played a critical role in duplicate gene evolution in zebrafish.
Initially, we found promoter a methylation of duplicate genes generally decreased with evolutionary
time measured by synonymous substitution rate between paralogous duplicates (Ks). Importantly,
promoter methylation of duplicate genes was negatively correlated with gene expression. Interestingly,
for 665 duplicate gene pairs, one gene was consistently promoter methylated while the other was
unmethylated across nine different datasets we studied. Besides, Body-Methylated genes showed longer
length than body-unmethylated genes.
3593–3601
Predictive Model and Software for Inbreeding-Purging Analysis of Pedigreed Populations
Aurora García-Dorado, Jinliang Wang, and Eugenio López-Cortegano
Purging selection determines the true consequences of inbreeding on fitness and can be crucial in
evolution and conservation. However, its detection and evaluation is elusive. Here we extend
a previous model to predict fitness for individuals in arbitrary pedigrees, including overlapping
generations. Based on this model, we develop software that detects purging from pedigreed data
and estimates the parameters necessary to predict fitness. We derive the bias of the rate of
inbreeding depression estimated using linear analysis of log-fitness, and we also analyze the natural
exponential approach for untransformed fitness. The adequacy of this methodology is illustrated
using simulated data.
3603–3613
Genomic, Transcriptomic, and Proteomic Analysis Provide Insights Into the Cold Adaptation
Mechanism of the Obligate Psychrophilic Fungus Mrakia psychrophila
Yao Su, Xianzhi Jiang, Wenping Wu, Manman Wang, M. Imran Hamid, Meichun Xiang,
and Xingzhong Liu
This article is the first integrated study to reveal the cold adaptation mechanism of psychrophilic
fungi from genomic, transcriptomic and proteomic perspectives. It reveals special cold adaptation
strategies of eukaryotic microorganisms, including codon usage and alternative splicing. It also
predicts unfolded protein response induced at higher temperature may lead to death of fungi. It is
highlighted in this article that cold adaptation of psychrophiles is different from cold stress responses
of mesophiles. The result in this article provides important resource for the research of psychrophilic
fungi in future.
3615–3624
Transcriptome Analysis Reveals that Vitamin A Metabolism in the Liver Affects Feed Efficiency
in Pigs
Yunxia Zhao, Ye Hou, Fei Liu, An Liu, Lu Jing, Changzhi Zhao, Yu Luan, Yuanxin Miao,
Shuhong Zhao, and Xinyun Li
Here, 300 significantly differentially expressed transcripts, including 232 annotated genes, 28
cis-NATs, and 40 lncRNAs, were identified between the liver of high and low FE pigs. The key
genes of VA metabolism (CYP1A1, ALDH1A2, and RDH16), fatty acid biosynthesis (FASN, SCD,
CYP2J2, and ANKRD23), and steroid hormone metabolism (CYP1A1, HSD17B2, and UGT2B4)
were significantly up-regulated in the liver of high-FE pigs. VA metabolism in liver tissues plays
important roles in the regulation of FE in pigs by affecting energy metabolism, which may mediate
fatty acid biosynthesis and steroid hormone metabolism. LncRNAs and cis-NATs were also related
to FE in pigs.
3625–3633
Sequential Turnovers of Sex Chromosomes in African Clawed Frogs (Xenopus) Suggest Some
Genomic Regions Are Good at Sex Determination
Benjamin L. S. Furman and Ben J. Evans
Sex determination is crucial for reproduction and it is interesting, therefore, when control of
this fundamental process evolves rapidly. For example, there exists variation among species
of African clawed frogs (Xenopus) in the genetic control of sex determination. Here we extend
these findings by demonstrating that yet another sex determination system exists in Xenopus
in the species Xenopus borealis. We illustrate that genetic control of sex determination in
X. borealis is homologous to that of several other more distantly related species, including humans.
Strikingly, this new system is derived from an ancestral sex determining system that itself was
newly evolved.
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3635–3645
Advances in Understanding Mating Type Gene Organization in the Mushroom-Forming Fungus
Flammulina velutipes
Wei Wang, Lingdan Lian, Ping Xu, Tiansheng Chou, Irum Mukhtar, Aron Osakina,
Muhammad Waqas, Bingzhi Chen, Xinrui Liu, Fang Liu, Baogui Xie, and Arend F. van Peer
The initiation of sexual development in mushroom Flammulina velutipes is controlled by special genes
at two different, independent mating type (MAT) loci: HD and PR. We expanded our understanding of
the F. velutipes mating type system by analyzing the MAT loci from a series of strains. In conclusion, at
least three of the four MAT subloci seem to participate in mating and new HD and PR loci can be
generated through intra-locus recombination in F. velutipes.
3647–3653
Simple and Efficient Targeting of Multiple Genes Through CRISPR-Cas9 in Physcomitrella patens
Mauricio Lopez-Obando, Beate Hoffmann, Carine Géry, Anouchka Guyon-Debast, Evelyne Téoulé,
Catherine Rameau, Sandrine Bonhomme, and Fabien Nogué
CRISPR-Cas9 system has been adapted as an efficient tool for editing of single genes in a variety of
species. However, knocking out or modifying a single gene is sometime not sufficient, this is particularly
true for genes belonging to a common family or for genes showing redundant functions. Here, we report
a simple and robust CRISPR-Cas9 system, based on the co-delivery of multiple vectors for gene
knock-out of multiple genes, generating stable mutants in Physcomitrella patens. This tool brings new
perspectives to study the role of multiple gene families in this model plant and opens new prospects for
other plants.
3655–3662
In Silico Whole Genome Sequencer and Analyzer (iWGS): a Computational Pipeline to Guide the
Design and Analysis of de novo Genome Sequencing Studies
Xiaofan Zhou, David Peris, Jacek Kominek, Cletus P. Kurtzman, Chris Todd Hittinger,
and Antonis Rokas
High-throughput DNA sequencing technologies has revolutionized genomics. In particular, de novo
genome sequencing, which used to require international collaborative efforts, is now accessible to
single-investigator laboratories. However, the increasing diversity of sequencing platforms, data types,
and genome assembly algorithms makes determination of the optimal experimental design in de novo
genome sequencing studies challenging. Therefore, we developed iWGS (in silico Whole Genome
Sequencer and Analyzer), an automated pipeline for guiding the choice of appropriate sequencing
strategy and assembly protocols as well as for evaluation of alternative solutions by conducting
simulated de novo sequencing experiments on known genomes of similar characteristics.
3663–3670
Determinants in the LIN-12/Notch Intracellular Domain That Govern Its Activity and Stability
During Caenorhabditis elegans Vulval Development
Yuting Deng and Iva Greenwald
In this study, we identify determinants in the LIN-12 intracellular domain that govern its activity and
stability during Caenorhabditis elegans vulval development. Our analysis has revealed that there are
developmental differences in the requirement for the ubiquitin ligase SEL-10/Fbw7, that LIN-12(intra)
must be in the nuclear complex to be regulated appropriately, that the structure or conformation of the
carboxy terminal region influences the stability; it also suggests that there may be roles for the carboxy
terminal region and sel-10 that are independent of their roles in regulating LIN-12(intra) stability.
3671–3683
Transcriptome Profiling in Rat Inbred Strains and Experimental Cross Reveals Discrepant Genetic
Architecture of Genome-Wide Gene Expression
Pamela J. Kaisaki, Georg W. Otto, Karène Argoud, Stephan C. Collins, Robert H. Wallis,
Steven P. Wilder, Anthony C. Y. Yau, Christophe Hue, Sophie Calderari, Marie-Thérèse Bihoreau,
Jean-Baptiste Cazier, Richard Mott, and Dominique Gauguier
Gene expression operates through local and distant genetic regulations. We address questions of the
extent and architecture of gene expression regulation by distant factors through fat transcriptome
profiling in genetically heterogeneous F2 rats and in inbred congenic strains that capture contiguous
blocks of genetic polymorphisms. Gene expression changes outside polymorphic regions differ
qualitatively from those within, comprising two-fold expression changes, suggesting a switching
mechanism. Different series of polymorphisms regulate the expression of the same genes and pathways,
demonstrating redundant genetic control. Our data provide advances in our understanding of
widespread interactions in the control of genome expression and biological pathways.
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3685–3691
Non-Mendelian Dominant Maternal Effects Caused by CRISPR/Cas9 Transgenic Components in
Drosophila melanogaster
Chun-Chieh Lin and Christopher J. Potter
The CRISPR/Cas9 system is a versatile and powerful genomic editing tool. Using Drosophila
melanogaster containing transgenic Cas9 and guide RNAs, the authors find that maternal contributions
of these components can lead to both somatic and germline mutations even in progeny whose genomes
lack these components. This artificial mode of inheritance leads to dominant maternal effects. This
serves as a cautionary note for experiments or models utilizing CRISPR/Cas9 transgenics, and suggests
gene drive mechanisms relying on these components might rapidly accumulate resistance. The
CRISPR/Cas9 system, comprising the Cas9 endonuclease and gRNA, is a powerful tool for genomic
editing. Cas9 and gRNAs are now being inserted into the genome to control genomic editing. The
authors find that genomically integrated CRISPR/Cas9 components in D. melanogaster lead to somatic
and germline mutations even in progeny that lack these components in their genome. This is caused by
maternal deposition of Cas9 and gRNAs into the developing embryo. The authors suggest caution when
designing experiments using CRISPR/Cas9 components. Furthermore, gene drive mechanisms relying
on CRISPR/Cas9 might be inhibited by this dominant maternal effect.
3693–3700
Genomic Prediction of Resistance to Pasteurellosis in Gilthead Sea Bream (Sparus aurata) Using
2b-RAD Sequencing
Christos Palaiokostas, Serena Ferraresso, Rafaella Franch, Ross D. Houston, and Luca Bargelloni
Sea bream is one of the most important species for Mediterranean aquaculture industry, with annual
production .140,000 metric tons. Pasteurellosis is one of the primary disease problems faced by the
industry, causing high mortality levels in young fish. Our results show that genomic prediction using the
2b-RAD technique is superior to pedigree-based prediction of disease resistance in this population. This
study is of interest both for basic research on disease resistance and for application in aquaculture,
where use of genomic tools in selective breeding for disease resistance is of high economic interest for
many species.
3701–3709
Extensive Epigenetic Changes Accompany Terminal Differentiation of Mouse Hepatocytes After Birth
Matthew V. Cannon, Genay Pilarowski, Xiuli Liu, and David Serre
We show here that in vivo postnatal terminal differentiation of hepatocytes involves extensive epigenetic
reprogramming. These changes in DNA methylation occur predominately in enhancer regions of the
genome, highlighting the importance of the modulation of epigenetic marks in these areas during changes
in cell identity. The information presented points towards DNA methylation in enhancers as a key
regulatory mechanism in controlling cell fate specification across many different cell types.
3711–3724
Distinct and Overlapping Requirements for Cyclins A, B, and B3 in Drosophila Female Meiosis
Mohammed Bourouh, Rajdeep Dhaliwal, Ketki Rana, Sucheta Sinha, Zhihao Guo, and Andrew Swan
We find that the three mitotic cyclin partners of Cyclin dependent kinase I have unique as well as
overlapping roles in meiosis. Cyclin B is involved in multiple steps in meiosis and appears to function
largely non-redundantly. Cyclin A is required to achieve proper alignment of homologues in meiosis
I. Cyclin B3 is required in anaphase of both meiotic divisions and with Cyclin A is required to prevent
re-replication. Meanwhile all three mitotic cyclins contribute to meiotic maturation.
3725–3732
The Selective Maintenance of Allelic Variation Under Generalized Dominance
Hamish G. Spencer and Cuilodair Mitchell
Understanding why natural populations harbor multiple alleles is the central problem in population
genetics. Our simulation study shows that when fitnesses are largely determined by the primary effects
of alleles, less variation is maintained by selection than when genotypes have independent fitnesses.
3733–3747
Improvement of Predictive Ability by Uniform Coverage of the Target Genetic Space
Daniela Bustos-Korts, Marcos Malosetti, Scott Chapman, Ben Biddulph, and Fred van Eeuwijk
Training set construction is a major challenge in genomic prediction. Random sampling protocols lead
to low quality coverage of the total genetic space by the training set. We propose a training set
construction method that uniformly samples the genetic space spanned by the target population of
genotypes, increasing predictive ability. Training sets were constructed using uniform sampling,
stratified-uniform sampling, stratified sampling, and the CD method (Rincent et al., 2012).
Construction of the training set under uniform sampling led to larger predictive ability than under
stratified and random sampling. The results of our methods were similar to those of CD.
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3749–3755
A Simplified Strategy for Introducing Genetic Variants into Drosophila Compound Autosome Stocks
William D. Gilliland, Dennis P. May, Eileen M. Colwell, and James A. Kennison
We present a new method for crossing compound chromosomes that is more efficient than previous
methods, and show that we could use this method to do several crosses with compound chromosomes
that would not have been viable otherwise. This should make it easier to use these unusual
chromosomes in other experiments.
MUTANT SCREEN REPORT
3757–3764
CRISPR/Cas9-Mediated Genome Editing and Mutagenesis of EcChi4 in Exopalaemon carinicauda
Tianshu Gui, Jiquan Zhang, Fengge Song, Yuying Sun, Shijun Xie, Kuijie Yu, and Jianhai Xiang
In this research, we showed four major findings: (1) microinjection method was successfully constructed
in the embryos of Exopalaemon carinicauda; (2) exogenous mRNA was successfully expressed in
shrimp’s embryos; (3) the CRISPR/Cas9 system efficiently generated DSB (50%) to induce a wide
range of indels at the EcChi4 loci in the genome of E. carinicauda; (4) introduction of heritable genome
editing in E. carinicauda via CRISPR/Cas9 system.
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