A plant virus differentially alters DNA methylation in two cryptic species of a hemipteran vector

Bewick, A. J., Vogel, K. J., Moore, A. J. & Schmitz, R. J. Evolution of DNA methylation across insects. Mol. Biol. Evol. 34, 654–665 (2017).CAS 
PubMed 

Google Scholar 
Bewick, A. J. et al. Diversity of cytosine methylation across the fungal tree of life. Nat. Ecol. Evol. 3, 479–490 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Zhang, H., Lang, Z. & Zhu, J.-K. Dynamics and function of DNA methylation in plants. Nat. Rev. Mol. Cell Biol. 19, 489–506 (2018).Article 
CAS 
PubMed 

Google Scholar 
Arneson, A. et al. A mammalian methylation array for profiling methylation levels at conserved sequences. Nat. Commun. 13, 783 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Klose, R. J. & Bird, A. P. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 31, 89–97 (2006).Article 
CAS 
PubMed 

Google Scholar 
Zhu, H., Wang, G. & Qian, J. Transcription factors as readers and effectors of DNA methylation. Nat. Rev. Genet 17, 551–565 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Flores, K. et al. Genome-wide association between DNA methylation and alternative splicing in an invertebrate. BMC Genom. 13, 480 (2012).Article 
CAS 

Google Scholar 
Glastad, K. M., Gokhale, K., Liebig, J. & Goodisman, M. A. The caste- and sex-specific DNA methylome of the termite Zootermopsis nevadensis. Sci. Rep. 6, 37110 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yin, Y. et al. Impact of cytosine methylation on DNA binding specificities of human transcription factors. Science 356, eaaj2239 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Shukla, S. et al. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479, 74–79 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Zeng, J. et al. Divergent whole-genome methylation maps of human and chimpanzee brains reveal epigenetic basis of human regulatory evolution. Am. J. Hum. Genet. 91, 455–465 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Glastad, K. M. et al. Epigenetic regulator CoREST controls social behavior in ants. Mol. Cell 77, 338–351.e336 (2020).Article 
CAS 
PubMed 

Google Scholar 
Huh, I., Zeng, J., Park, T. & Yi, S. V. DNA methylation and transcriptional noise. Epigenetics Chromatin 6, 9 (2013).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Glastad, K. M., Hunt, B. G. & Goodisman, M. A. D. Epigenetics in insects: genome regulation and the generation of phenotypic diversity. Annu. Rev. Entomol. 64, 185–203 (2019).Article 
CAS 
PubMed 

Google Scholar 
Mukherjee, K. & Dobrindt, U. The emerging role of epigenetic mechanisms in insect defense against pathogens. Curr. Opin. Insect Sci. 49, 8–14 (2022).Article 
PubMed 

Google Scholar 
Mukherjee, K., Dubovskiy, I., Grizanova, E., Lehmann, R. & Vilcinskas, A. Epigenetic mechanisms mediate the experimental evolution of resistance against parasitic fungi in the greater wax moth Galleria mellonella. Sci. Rep. 9, 1626 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Gilbertson, R. L., Batuman, O., Webster, C. G. & Adkins, S. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu Rev. Virol. 2, 67–93 (2015).Article 
CAS 
PubMed 

Google Scholar 
Leke, W. N., Mignouna, D. B., Brown, J. K. & Kvarnheden, A. Begomovirus disease complex: emerging threat to vegetable production systems of West and Central Africa. Agric. Food Secur. 4, https://doi.org/10.1186/s40066-014-0020-2 (2015).Saurabh, S. et al. Tiny Flies: A mighty pest that threatens agricultural productivity-a case for next-generation control strategies of whiteflies. Insects 12, https://doi.org/10.3390/insects12070585 (2021).Domingo, E. & Perales, C. Viral quasispecies. PLoS Genet. 15, e1008271 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Pakkianathan, B. C. et al. Replication of Tomato yellow leaf curl virus in its whitefly vector, Bemisia tabaci. J. Virol. 89, 9791–9803 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Becker, N. et al. Rapid accumulation and low degradation: key parameters of Tomato yellow leaf curl virus persistence in its insect vector Bemisia tabaci. Sci. Rep. 5, 17696 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sanchez-Campos, S. et al. Tomato yellow leaf curl virus: no evidence for replication in the insect vector Bemisia tabaci. Sci. Rep. 6, 30942 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Rosen, R. et al. Persistent, circulative transmission of begomoviruses by whitefly vectors. Curr. Opin. Virol. 15, 1–8 (2015).Article 
PubMed 

Google Scholar 
Hogenhout, S. A., Ammar el, D., Whitfield, A. E. & Redinbaugh, M. G. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46, 327–359 (2008).Article 
CAS 
PubMed 

Google Scholar 
Eigenbrode, S. D., Bosque-Perez, N. A. & Davis, T. S. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu. Rev. Entomol. 63, 169–191 (2018).Article 
CAS 
PubMed 

Google Scholar 
Catto, M. A. et al. A review on transcriptional responses of interactions between insect vectors and plant viruses. Cells 11, 693 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Stafford, C. A., Walker, G. P. & Ullman, D. E. Hitching a ride: vector feeding and virus transmission. Commun. Integr. Biol. 5, 43–49 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Zhao, J. et al. A vector whitefly endocytic receptor facilitates the entry of begomoviruses into its midgut cells via binding to virion capsid proteins. PLoS Pathog. 16, e1009053 (2020).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Czosnek, H., Hariton-Shalev, A., Sobol, I., Gorovits, R. & Ghanim, M. The incredible journey of begomoviruses in their whitefly vector. Viruses 9, https://doi.org/10.3390/v9100273 (2017).Hsieh, C.-H., Wang, C.-H. & Ko, C.-C. Evidence from molecular markers and population genetic analyses suggests recent invasions of the Western North Pacific region by biotypes B and Q of Bemisia tabaci (Gennadius). Environ. Entomol. 36, 952–961 (2007).Article 
CAS 
PubMed 

Google Scholar 
Elfekih, S. et al. Genome-wide analyses of the Bemisia tabaci species complex reveal contrasting patterns of admixture and complex demographic histories. PLoS One 13, e0190555 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
MacLeod, N., Canty, R. J. & Polaszek, A. Morphology-based identification of Bemisia tabaci cryptic species puparia via embedded group-contrast convolution neural network analysis. Syst. Biol. 71, 1095–1109 (2022).Article 
CAS 
PubMed 

Google Scholar 
Brown, J. K., Paredes-Montero, J. R. & Stocks, I. C. The Bemisia tabaci cryptic (sibling) species group—imperative for a taxonomic reassessment. Curr. Opin. Insect Sci. 57, 101032 (2023).Article 
PubMed 

Google Scholar 
de Moraes, L. A. et al. Distribution and phylogenetics of whiteflies and their endosymbiont relationships after the Mediterranean species invasion in Brazil. Sci. Rep. 8, 14589 (2018).Article 
PubMed 
PubMed Central 

Google Scholar 
Hamon, A. & Salguero, V. Bemisia tabaci, Sweetpotato Whitefly in Florida (Homoptera: Aleyrodidae: Aleyrodinae). Fla. Dept. of Agric. & Consumer Ser. Entomology Circular No. 292. 2 p. (1987).Dennehy, T. J. et al. New challenges to management of whitefly resistance to insecticides in Arizona. University of Arizona Cooperative Extension, Vegetable Report. 31 pp. Series P-144. (eds D. N. Byrne and P. Baciewicz). https://cals.arizona.edu/pubs/crops/az1382/index.html (2005).Xie, W. et al. Genome sequencing of the sweetpotato whitefly Bemisia tabaci MED/Q. Gigascience 6, 1–7 (2017).Article 
PubMed 
PubMed Central 

Google Scholar 
Li, H. et al. Invasion genomics uncover complex introduction patterns of the globally invasive whitefly, Bemisia tabaciMED. Divers. Distrib. https://doi.org/10.1111/ddi.13751 (2023).Chen, W. et al. Genome of the African cassava whitefly Bemisia tabaci and distribution and genetic diversity of cassava-colonizing whiteflies in Africa. Insect Biochem Mol. Biol. 110, 112–120 (2019).Article 
CAS 
PubMed 

Google Scholar 
Chen, W. et al. The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol. 14, 110 (2016).Article 
PubMed 
PubMed Central 

Google Scholar 
Campbell, L. I. et al. Comparative evolutionary analyses of eight whitefly Bemisia tabaci sensu lato genomes: cryptic species, agricultural pests and plant-virus vectors. BMC Genom. 24, 408 (2023).Article 
CAS 

Google Scholar 
Xie, W. et al. The invasive MED/Q Bemisia tabaci genome: a tale of gene loss and gene gain. BMC Genom. 19, 68 (2018).Article 

Google Scholar 
Gautam, S. et al. Effects of host plants and their infection status on acquisition and inoculation of A plant virus by its hemipteran vector. Pathogens 12, https://doi.org/10.3390/pathogens12091119 (2023).Mugerwa, H. et al. Differential transcriptional responses in two old world Bemisia tabaci cryptic species post acquisition of old and new world begomoviruses. Cells 11, https://doi.org/10.3390/cells11132060 (2022).Li, Y., Mbata, G. N., Punnuri, S., Simmons, A. M. & Shapiro-Ilan, D. I. Bemisia tabaci on vegetables in the Southern United States: incidence, impact, and management. Insects 12, https://doi.org/10.3390/insects12030198 (2021).McKenzie, C. L., Sparks, A. N., Roberts, P., Oetting, R. D. & Osborne, L. S. Survey of Bemisia tabaci (Hemiptera: Aleyrodidae) in Agricultural Ecosystems in Georgia. J. Entomol. Sci. 55, https://doi.org/10.18474/0749-8004-55.2.163 (2020).Gautam, S. et al. Differential Transmission of Old and New World Begomoviruses by Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) Cryptic Species of Bemisia tabaci. Viruses 14, https://doi.org/10.3390/v14051104 (2022).Polston, J. E., De Barro, P. & Boykin, L. M. Transmission specificities of plant viruses with the newly identified species of the Bemisia tabaci species complex. Pest. Manag. Sci. 70, 1547–1552 (2014).Article 
CAS 
PubMed 

Google Scholar 
de Mendoza, A., Pflueger, J. & Lister, R. Capture of a functionally active methyl-CpG binding domain by an arthropod retrotransposon family. Genome Res. 29, 1277–1286 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Yu, X. et al. Sex-specific transcription and DNA methylation landscapes of the Asian citrus psyllid, a vector of huanglongbing pathogens. Evolution 77, 1203–1215 (2023).Article 
PubMed 

Google Scholar 
Sicat, J. P. A., Visendi, P., Sewe, S. O., Bouvaine, S. & Seal, S. E. Characterization of transposable elements within the Bemisia tabaci species complex. Mob. DNA 13, 12 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Zidi, M. et al. Genome-wide screening of transposable elements in the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), revealed insertions with potential insecticide resistance implications. Insects 13, https://doi.org/10.3390/insects13050396 (2022).Simao, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).Article 
CAS 
PubMed 

Google Scholar 
Gordon, S. P. et al. Widespread polycistronic transcripts in fungi revealed by single-molecule mRNA sequencing. PLoS One 10, e0132628 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Yi, S. V. & Goodisman, M. A. Computational approaches for understanding the evolution of DNA methylation in animals. Epigenetics 4, 551–556 (2009).Article 
CAS 
PubMed 

Google Scholar 
Bhattacharjee, B. & Hallan, V. Geminivirus-derived vectors as tools for functional genomics. Front. Microbiol. 13, 799345 (2022).Article 
PubMed 
PubMed Central 

Google Scholar 
Coates, B. S. Horizontal transfer of a non-autonomous Helitron among insect and viral genomes. BMC Genom. 16, 137 (2015).Article 

Google Scholar 
Kiser, L. M., Sokoloski, K. J. & Hardy, R. W. Interactions between capsid and viral RNA regulate Chikungunya virus translation in a host-specific manner. Virology 560, 34–42 (2021).Article 
CAS 
PubMed 

Google Scholar 
Ahlers, L. R. H. et al. Insulin potentiates JAK/STAT signaling to broadly inhibit flavivirus replication in insect vectors. Cell Rep. 29, 1946–1960.e1945 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Kemp, C. et al. Broad RNA interference-mediated antiviral immunity and virus-specific inducible responses in Drosophila. J. Immunol. 190, 650–658 (2013).Article 
CAS 
PubMed 

Google Scholar 
Dostert, C. et al. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat. Immunol. 6, 946–953 (2005).Article 
CAS 
PubMed 

Google Scholar 
Chen, L. L. et al. Identification of a nucleocapsid protein (VP35) gene of shrimp white spot syndrome virus and characterization of the motif important for targeting VP35 to the nuclei of transfected insect cells. Virology 293, 44–53 (2002).Article 
CAS 
PubMed 

Google Scholar 
Li, P. et al. Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors. PLoS Pathog. 15, e1007607 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Yang, C., Kang, L. & Zhao, Q. Comparative transcriptomic analysis of the l-4i silkworm (Lepidoptera: Bombyx mori) mutants and its wild-type strain P33 by RNA-Seq. Comp. Biochem Physiol. Part D. Genom. Proteom. 38, 100800 (2021).CAS 

Google Scholar 
Schmid, M., Steinlein, C., Yano, C. F. & Cioffi, M. B. Hypermethylated chromosome regions in nine fish species with heteromorphic sex chromosomes. Cytogenet. Genome Res. 147, 169–178 (2015).Article 
PubMed 

Google Scholar 
Field, L. M., Lyko, F., Mandrioli, M. & Prantera, G. DNA methylation in insects. Insect Mol. Biol. 13, 109–115 (2004).Article 
CAS 
PubMed 

Google Scholar 
Cunningham, C. B. et al. An association between Dnmt1 and Wnt in the production of oocytes in the whitefly Bemisia tabaci. Insect. Mol. Biol. https://doi.org/10.1111/imb.12893 (2024).Ylla, G. et al. Insights into the genomic evolution of insects from cricket genomes. Commun. Biol. 4, 733 (2021).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sun, D., Li, Q. & Yu, H. DNA methylation differences between male and female gonads of the oyster reveal the role of epigenetics in sex determination. Gene 820, 146260 (2022).Article 
CAS 
PubMed 

Google Scholar 
Marshall, H. et al. DNA methylation is associated with codon degeneracy in a species of bumblebee. Heredity 130, 188–195 (2023).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Elango, N., Hunt, B. G., Goodisman, M. A. & Yi, S. V. DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proc. Natl Acad. Sci. USA 106, 11206–11211 (2009).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Provataris, P., Meusemann, K., Niehuis, O., Grath, S. & Misof, B. Signatures of DNA methylation across insects suggest reduced DNA methylation levels in holometabola. Genome Biol. Evol. 10, 1185–1197 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Foret, S., Kucharski, R., Pittelkow, Y., Lockett, G. A. & Maleszka, R. Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genom. 10, 472 (2009).Article 

Google Scholar 
Kvist, J. et al. Pattern of DNA methylation in daphnia: evolutionary perspective. Genome Biol. Evol. 10, 1988–2007 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Weber, M. et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet 39, 457–466 (2007).Article 
CAS 
PubMed 

Google Scholar 
Jiang, N. et al. Conserved and divergent patterns of DNA methylation in higher vertebrates. Genome Biol. Evol. 6, 2998–3014 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Greenberg, M. V. C. & Bourc’his, D. The diverse roles of DNA methylation in mammalian development and disease. Nat. Rev. Mol. Cell Biol. 20, 590–607 (2019).Article 
CAS 
PubMed 

Google Scholar 
Fu, R., Huang, X., Chen, Y., Chen, Z. & Zhan, A. Interactive regulations of dynamic methylation and transcriptional responses to recurring environmental stresses during biological invasions. Front. Mar. Sci. 8, https://doi.org/10.3389/fmars.2021.800745 (2021).Bourque, G. et al. Ten things you should know about transposable elements. Genome Biol. 19, 199 (2018).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Malik, H. S. & Eickbush, T. H. Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res. 11, 1187–1197 (2001).Article 
CAS 
PubMed 

Google Scholar 
Merel, V., Boulesteix, M., Fablet, M. & Vieira, C. Transposable elements in Drosophila. Mob. DNA 11, 23 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Strand, D. J. & McDonald, J. F. Copia is transcriptionally responsive to environmental stress. Nucleic Acids Res. 13, 4401–4410 (1985).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Merkling, S. H. et al. The heat shock response restricts virus infection in Drosophila. Sci. Rep. 5, 12758 (2015).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Wang, L. et al. Retrotransposon activation during Drosophila metamorphosis conditions adult antiviral responses. Nat. Genet. 54, 1933–1945 (2022).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Jiang, L. et al. Distinct functions of Bombyx mori peptidoglycan recognition protein 2 in immune responses to bacteria and viruses. Front. Immunol. 10, 776 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Badillo-Vargas, I. E. et al. Proteomic analysis of Frankliniella occidentalis and differentially expressed proteins in response to tomato spotted wilt virus infection. J. Virol. 86, 8793–8809 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Li, H. J., Zhang, H. H., Lu, J. B. & Zhang, C. X. Threonyl-tRNA synthetase gene, a potential target for RNAi-based control of three rice planthoppers. Pest Manag. Sci. 78, 4589–4598 (2022).Article 
CAS 
PubMed 

Google Scholar 
Gautam, S. et al. Virus-virus interactions in a plant host and in a hemipteran vector: Implications for vector fitness and virus epidemics. Virus Res. 286, 198069 (2020).Article 
CAS 
PubMed 

Google Scholar 
Ghosh, S., Bouvaine, S., Richardson, S. C. W., Ghanim, M. & Maruthi, M. N. Fitness costs associated with infections of secondary endosymbionts in the cassava whitefly species Bemisia tabaci. J. Pest Sci. (2004) 91, 17–28 (2018).Article 
PubMed 

Google Scholar 
De Barro, P. J. et al. Isolation and characterization of microsatellite loci in Bemisia tabaci. Mol. Ecol. Notes 3, 40–43 (2003).Article 
CAS 

Google Scholar 
Marchant, W. G., Gautam, S., Hutton, S. F. & Srinivasan, R. Tomato yellow leaf curl virus-resistant and -susceptible tomato genotypes similarly impact the virus population genetics. Front. Plant Sci. 11, 599697 (2020).Article 
PubMed 
PubMed Central 

Google Scholar 
Ewels, P., Magnusson, M., Lundin, S. & Kaller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048 (2016).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571–1572 (2011).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Xi, Y. & Li, W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinform. 10, 232 (2009).Article 

Google Scholar 
Akalin, A. et al. methylKit: a comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biol. 13, R87 (2012).Article 
PubMed 
PubMed Central 

Google Scholar 
Park, Y. & Wu, H. Differential methylation analysis for BS-seq data under general experimental design. Bioinformatics 32, 1446–1453 (2016).Article 
CAS 
PubMed 

Google Scholar 
Bulla, I. et al. Notos – a galaxy tool to analyze CpN observed expected ratios for inferring DNA methylation types. BMC Bioinform. 19, 105 (2018).Article 

Google Scholar 
Su, W., Ou, S., Hufford, M. B. & Peterson, T. A tutorial of EDTA: extensive de novo TE annotator. Methods Mol. Biol. 2250, 55–67 (2021).Article 
CAS 
PubMed 

Google Scholar 
Bell, E. A. et al. Transposable element annotation in non-model species: the benefits of species-specific repeat libraries using semi-automated EDTA and DeepTE de novo pipelines. Mol. Ecol. Resour. 22, 823–833 (2022).Article 
CAS 
PubMed 

Google Scholar 
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).Article 
CAS 
PubMed 

Google Scholar 
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 12, 323 (2011).Article 
CAS 

Google Scholar 
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).Article 
PubMed 
PubMed Central 

Google Scholar 
Anders, S., Reyes, A. & Huber, W. Detecting differential usage of exons from RNA-seq data. Genome Res. 22, 2008–2017 (2012).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Xu, L. et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 47, W52–W58 (2019).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).Article 
PubMed 
PubMed Central 

Google Scholar 
Emms, D. M. & Kelly, S. STRIDE: species tree root inference from gene duplication events. Mol. Biol. Evol. 34, 3267–3278 (2017).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).Article 
PubMed 
PubMed Central 

Google Scholar 
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).Article 
CAS 
PubMed 
PubMed Central 

Google Scholar 
Sievers, F. & Higgins, D. G. Clustal omega. Curr. Protoc. Bioinforma. 48, 3 13 11–13 13 16 (2014).
Google Scholar 
Rice, P., Longden, I. & Bleasby, A. EMBOSS: the European molecular biology open software suite. Trends Genet. 16, 276–277 (2000).Article 
CAS 
PubMed 

Google Scholar 
Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).Article 
CAS 
PubMed 

Google Scholar 

Hot Topics

Related Articles