Abstract
Parasitism evokes adaptive physiological changes in the host, many of which take place through gene expression changes. This response can be more or less local, depending on the organ or tissue affected by the parasite, or else systemic when the parasite affects the entire host body. The most extreme of the latter cases is intragenomic parasitism, where the parasite is present in all host nuclei as any other genomic element. Here, we show the molecular crosstalk between a parasitic chromosome (also named B chromosome) and the host genome, manifested through gene expression changes. The transcriptome analysis of 0B and 1B females of the grasshopper Eyprepocnemis plorans, validated by a microarray experiment performed on four B-lacking and five B-carrying females, revealed changes in gene expression for 188 unigenes being consistent in both experiments. Once discarded B-derived transcripts, there were 46 differentially expressed genes (30 up- and 16 downregulated) related with the adaptation of the host genome to the presence of the parasitic chromosome. Interestingly, the functions of these genes could explain some of the most important effects of B chromosomes, such as nucleotypic effects derived from the additional DNA they represent, chemical defense and detoxification, protein modification and response to stress, ovary function, and regulation of gene expression. Collectively, these changes uncover an intimate host-parasite interaction between A and B chromosomes during crucial steps of gene expression and protein function.
This is a preview of subscription content, access via your institution.
References
Akbari OS, Antoshechkin I, Hay BA, Ferree PM (2013) Transcriptome profiling of Nasonia vitripennis testis reveals novel transcripts expressed from the selfish B chromosome, paternal sex ratio. G3-Genes Genom Genet 3:1597–1605. https://doi.org/10.1534/g3.113.007583
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Bakkali M, Manrique-Poyato MI, López-León MD, Perfectti F, Cabrero J, Camacho JPM (2010) Effects of B chromosomes on egg fertility and clutch size in the grasshopper Eyprepocnemis plorans. J Orthop Res 19:197–203. https://doi.org/10.1665/034.019.0205
Banaei-Moghaddam AM, Meier K, Karimi-Ashtiyani R, Houben A (2013) Formation and expression of pseudogenes on the B chromosome of rye. Plant Cell 25:2536–2544. https://doi.org/10.1105/tpc.113.111856
Banaei-Moghaddam AM, Martis MM, Macas J, Gundlach H, Himmelbach A, Altschmied L, Mayer KFX, Houben A (2015) Genes on B chromosomes: old questions revisited with new tools. Biochim Biophys Acta 1849:64–70. https://doi.org/10.1016/j.bbagrm.2014.11.007
Barribeau SM, Sadd BM, du Plessis L, Schmid-Hempel P (2014) Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system. Proc Natl Acad Sci U S A 111:3496–3501. https://doi.org/10.1073/pnas.1318628111
Bennett MD (1971) The duration of meiosis. Proc R Soc Lond B Biol Sci 178:277–299. https://doi.org/10.1098/rspb.1971.0066
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Cabrero J, Alché JD, Camacho JPM (1987) Effects of B chromosomes on the activity of nucleolar organizer regions in the grasshopper Eyprepocnemis plorans: activation of a latent nucleolar organizer region on a B chromosome fused to an autosome. Genome 29:116–121. https://doi.org/10.1139/g87-020
Cabrero J, Manrique-Poyato MI, Camacho JPM (2006) Detection of B chromosomes in interphase hemolymph nuclei from living specimens of the grasshopper Eyprepocnemis plorans. Cytogenet Genome Res 114:66–69. https://doi.org/10.1159/000091930
Cabrero J, López-León MD, Ruíz-Estévez M et al (2014) B1 was the ancestor B chromosome variant in the western Mediterranean area in the grasshopper Eyprepocnemis plorans. Cytogenet Genome Res 142:54–58. https://doi.org/10.1159/000356052
Cabrero J, Martín-Peciña M, Ruiz-Ruano FJ, Gómez R, Camacho JPM (2018) Post-meiotic B chromosome expulsion, during spermiogenesis, in two grasshopper species. Chromosoma (in press 126:633–644. https://doi.org/10.1007/s00412-017-0627-8
Camacho JPM (2005) B chromosomes. In: Gregory TR (ed) The evolution of the genome. Elsevier, San Diego, pp 223–286
Camacho JPM, Carballo AR, Cabrero J (1980) The B-chromosome system of the grasshopper Eyprepocnemis plorans subsp. plorans (Charpentier). Chromosoma 80:163–176. https://doi.org/10.1007/BF00286298
Camacho JPM, Shaw MW, López-León MD, Pardo MC, Cabrero J (1997) Population dynamics of a selfish B chromosome neutralized by the standard genome in the grasshopper Eyprepocnemis plorans. Am Nat 149:1030–1050. https://doi.org/10.1086/286037
Camacho JPM, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc B 355:163–178. https://doi.org/10.1098/rstb.2000.0556
Camacho JPM, Bakkali M, Corral JM, Cabrero J, López-León MD, Aranda I, Martín-Alganza A, Perfectti F (2002) Host recombination is dependent on the degree of parasitism. Proc Biol Sci 269:2173–2177. https://doi.org/10.1098/rspb.2002.2135
Carchilan M, Kumke K, Mikolajewski S, Houben A (2009) Rye B chromosomes are weakly transcribed and might alter the transcriptional activity of A chromosome sequences. Chromosoma 118:607–616. https://doi.org/10.1007/s00412-009-0222-8
Carmello BO, Coan RLB, Cardoso AL, Ramos E, Fantinatti BEA, Marques DF, Oliveira RA, Valente GT, Martins C (2017) The hnRNP Q-like gene is retroinserted into the B chromosomes of the cichlid fish Astatotilapia latifasciata. Chromosom Res 25:277–290. https://doi.org/10.1007/s10577-017-9561-0
Carvalho BS, Irizarry RA (2010) A framework for oligonucleotide microarray preprocessing. Bioinformatics 26:2363–2367. https://doi.org/10.1093/bioinformatics/btq431
Fabian L, Forer A (2007) Possible roles of actin and myosin during anaphase chromosome movements in locust spermatocytes. Protoplasma 231:201–213. https://doi.org/10.1007/s00709-007-0262-y
Fabian L, Xia X, Venkitaramani DV, Johansen KM, Johansen J, Andrew DJ, Forer A (2007) Titin in insect spermatocyte spindle fibers associates with microtubules, actin, myosin and the matrix proteins skeletor, megator and chromator. J Cell Sci 120:2190–2204. https://doi.org/10.1242/jcs.03465
Fablet M (2014) Host control of insect endogenous retroviruses: small RNA silencing and immune response. Viruses 6:4447–4464. https://doi.org/10.3390/v6114447
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. https://doi.org/10.1093/nar/gkr367
Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152. https://doi.org/10.1093/bioinformatics/bts565
Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JYH, Zhang J (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80. https://doi.org/10.1186/gb-2004-5-10-r80
Goldstone JV, Hamdoun A, Cole BJ, Howard-Ashby M, Nebert DW, Scally M, Dean M, Epel D, Hahn ME, Stegeman JJ (2006) The chemical defensome: environmental sensing and response genes in the Strongylocentrotus purpuratus genome. Dev Biol 300:366–384. https://doi.org/10.1016/j.ydbio.2006.08.066
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. https://doi.org/10.1038/nbt.1883
Graphodatsky AS, Kukekova AV, Yudkin DV, Trifonov VA, Vorobieva NV, Beklemisheva VR, Perelman PL, Graphodatskaya DA, Trut LN, Yang F, Ferguson-Smith MA, Acland GM, Aguirre GD (2005) The proto-oncogene C-KIT maps to canid B-chromosomes. Chromosom Res 13:113–122. https://doi.org/10.1007/s10577-005-7474-9
Gregory TR (2000) Nucleotypic effects without nuclei: genome size and erythrocyte size in mammals. Genome 43:895–901
Gregory TR (2002) A bird’s-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution 56:121–130. https://doi.org/10.1554/0014-3820(2002)056[0121:ABSEVO]2.0.CO;2
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512. https://doi.org/10.1038/nprot.2013.084
Henriques-Gil N, Arana P (1990) Origin and substitution of B chromosomes in the grasshopper Eyprepocnemis plorans. Evolution 44:747–753. https://doi.org/10.1111/j.1558-5646.1990.tb05952.x
Huang W, Du Y, Zhao X, Jin W (2016) B chromosome contains active genes and impacts the transcription of A chromosomes in maize (Zea mays L.). BMC Plant Biol 16(88):88. https://doi.org/10.1186/s12870-016-0775-7
John PCL, Jones RN (1970) Molecular heterogeneity of soluble proteins and histones in relationship to the presence of B-chromosomes in rye. Exp Cell Res 63:271–276. https://doi.org/10.1016/0014-4827(70)90213-2
Jones RN, Rees H (1982) B chromosomes. Academic Press, London
Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467. https://doi.org/10.1159/000084979
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25. https://doi.org/10.1186/gb-2009-10-3-r25
Lavine L, Gotoh H, Brent CS, Dworkin I, Emlen DJ (2015) Exaggerated trait growth in insects. Annu Rev Entomol 60:453–472. https://doi.org/10.1146/annurev-ento-010814-021045
Leach CR, Houben A, Field B, Pistrick K, Demidov D, Timmis JN (2005) Molecular evidence for transcription of genes on a B chromosome in Crepis capillaris. Genetics 171:269–278. https://doi.org/10.1534/genetics.105.043273
Leevers SJ, Weinkove D, MacDougall LK, Hafen E, Waterfield MD (1996) The Drosophila phosphoinositide 3-kinase Dp110 promotes cell growth. EMBO J 15:6584–6594
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323. https://doi.org/10.1186/1471-2105-12-323
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Lin CJ, Hu F, Dubruille R, Vedanayagam J, Wen J, Smibert P, Loppin B, Lai EC (2018) The hpRNA/RNAi pathway is essential to resolve intragenomic conflict in the Drosophila male germline. Dev Cell 46:316–326. https://doi.org/10.1016/j.devcel.2018.07.004
Liu Y, Zhou J, White KP (2013) RNA-seq differential expression studies: more sequence or more replication? Bioinformatics 30(3):301–304. https://doi.org/10.1093/bioinformatics/btt688
López-León MD, Cabrero J, Camacho JPM (1995) Changes in DNA methylation during development in the B chromosome NOR of the grasshopper Eyprepocnemis plorans. Heredity 74:296–302. https://doi.org/10.1038/hdy.1995.43
López-León MD, Cabrero J, Dzyubenko VV, Bugrov AG, Karamysheva TV, Rubtsov NB, Camacho JPM (2008) Differences in ribosomal DNA distribution on A and B chromosomes between eastern and western populations of the grasshopper Eyprepocnemis plorans plorans. Cytogenet Genome Res 121:260–265. https://doi.org/10.1159/000138894
Ma W, Gabriel TS, Martis MM, Gursinsky T, Schubert V, Vrána J, Doležel J, Grundlach H, Altschmied L, Scholz U, Himmelbach A, Behrens SE, Banaei-Moghaddam AM, Houben A (2017) Rye B chromosomes encode a functional Argonaute-like protein with in vitro slicer activities similar to its A chromosome paralog. New Phytol 213:916–928. https://doi.org/10.1111/nph.14110
Machado C, Andrew DJ (2000) D-Titin: a giant protein with dual roles in chromosomes and muscles. J Cell Biol 151:639–652. https://doi.org/10.1083/jcb.151.3.639
Marçais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764–770. https://doi.org/10.1093/bioinformatics/btr011
Martín-Alganza A, Cabrero J, López-León MD, Perfectti F, Camacho JPM (1997) Supernumerary heterochromatin does not affect several morphological and physiological traits in the grasshopper Eyprepocnemis plorans. Hereditas 126(2):187–189. https://doi.org/10.1111/j.1601-5223.1997.00187.x
Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, Scholz U, Gundlach H, Wicker T, Simkova H, Novak P, Neumann P, Kubalakova M, Bauer E, Haseneyer G, Fuchs J, Dolezel J, Stein N, Mayer KFX, Houben A (2012) Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. Proc Natl Acad Sci U S A 109:13343–13346. https://doi.org/10.1073/pnas.1204237109
Morey JS, Ryan JC, Dolah FM (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8:175–193
Muñoz E, Perfectti F, Martín-Alganza A, Camacho JPM (1998) Parallel effects of a B chromosome and a mite that decrease female fitness in the grasshopper Eyprepocnemis plorans. Proc R Soc Lond B 265:1903–1909. https://doi.org/10.1098/rspb.1998.0518
Muñoz-Pajares AJ, Martínez-Rodríguez L, Teruel M, Cabrero J, Camacho JPM, Perfectti F (2011) A single, recent origin of the accessory B chromosome of the grasshopper Eyprepocnemis plorans. Genetics 187:853–863. https://doi.org/10.1534/genetics.110.122713
Navarro-Domínguez B, Cabrero J, Camacho JPM, López-León MD (2016) B-chromosome effects on Hsp70 gene expression does not occur at transcriptional level in the grasshopper Eyprepocnemis plorans. Mol Gen Genomics 291:1909–1917
Navarro-Domínguez B, Ruiz-Ruano FJ, Cabrero J, Corral JM, López-León MD, Sharbel TF, Camacho JPM (2017a) Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans. Sci Rep 7:45200. https://doi.org/10.1038/srep45200
Navarro-Domínguez B, Ruiz-Ruano FJ, Camacho JPM, Cabrero J, López-León MD (2017b) Transcription of a B chromosome CAP-G pseudogene does not influence normal Condensin Complex genes in a grasshopper. Sci Rep 7:17650. https://doi.org/10.1038/s41598-017-15894-5
Nishimura M, Tanaka S, Ihara F, Muroi Y, Yamagishi J, Furuoka H, Suzuki Y, Nishikawa Y (2015) Transcriptome and histopathological changes in mouse brain infected with Neospora caninum. Sci Rep 5:7936. https://doi.org/10.1038/srep07936
Nuismer SL, Otto SP (2005) Host–parasite interactions and the evolution of gene expression. PLoS Biol 3:e203. https://doi.org/10.1371/journal.pbio.0030203
Obbard DJ, Gordon KH, Buck AH, Jiggins FM (2009) The evolution of RNAi as a defence against viruses and transposable elements. Philos Trans R Soc Lond B Biol Sci 364:99–115. https://doi.org/10.1098/rstb.2008.0168
Pappu R, Ramirez-Carrozzi V, Sambandam A (2011) The interleukin-17 cytokine family: critical players in host defence and inflammatory diseases. Immunology 134:8–16. https://doi.org/10.1111/j.1365-2567.2011.03465.x
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, Heger A, Holm L, Sonnhammer ELL, Eddy SR, Bateman A, Finn RD (2011) The Pfam protein families database. Nucleic Acids Res 40(Database issue):D290–D301. https://doi.org/10.1093/nar/gkr1065
Ramos E, Cardoso AL, Brown J, Marques DF, Fantinatti BEA, Cabral-de-Mello DC, Oliveira RA, O’Neill RJ, Martins C (2017) The repetitive DNA element BncDNA, enriched in the B chromosome of the cichlid fish Astatotilapia latifasciata, transcribes a potentially noncoding RNA. Chromosoma 126:313–323. https://doi.org/10.1007/s00412-016-0601-x
Robertson G, Schein J, Chiu R, Corbett R, Field M, Jackman SD, Mungall K, Lee S, Okada HM, Qian JQ, Griffith M, Raymond A, Thiessen N, Cezard T, Butterfield YS, Newsome R, Chan SK, She R, Varhol R, Kamoh B, Prabhu AL, Tam A, Zhao YJ, Moore RA, Hirst M, Marra MA, Jones SJM, Hoodless PA, Birol I (2010) De novo assembly and analysis of RNA-seq data. Nat Methods 7:909–912. https://doi.org/10.1038/nmeth.1517
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. https://doi.org/10.1093/bioinformatics/btp616
Ruiz-Estévez M, López-León MD, Cabrero J, Camacho JPM (2012) B-chromosome ribosomal DNA is functional in the grasshopper Eyprepocnemis plorans. PLoS One 7:e36600. https://doi.org/10.1371/journal.pone.0036600
Ruiz-Estévez M, López-León MD, Cabrero J, Camacho JPM (2013) Ribosomal DNA is active in different B chromosome variants of the grasshopper Eyprepocnemis plorans. Genetica 141:337–345. https://doi.org/10.1007/s10709-013-9733-6
Ruiz-Estévez M, Badisco L, Broeck JV, Perfectti F, López-León MD, Cabrero J, Camacho JPM (2014) B chromosomes showing active ribosomal RNA genes contribute insignificant amounts of rRNA in the grasshopper Eyprepocnemis plorans. Mol Gen Genomics 289:1209–1216. https://doi.org/10.1007/s00438-014-0880-y
Ruiz-Ruano FJ, Ruiz-Estévez M, Rodríguez-Pérez J, López-Pino JL, Cabrero J, Camacho JPM (2011) DNA amount of X and B chromosomes in the grasshoppers Eyprepocnemis plorans and Locusta migratoria. Cytogenet Genome Res 134:120–126. https://doi.org/10.1159/000324690
Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864. https://doi.org/10.1093/bioinformatics/btr026
Schurch NJ, Schofield P, Gierliński M, Cole C, Sherstnev A, Singh V, Wrobel N, Gharbi K, Simpson GG, Owen-Hughes T, Blaxter M, Barton GJ (2016) How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use? RNA 22:839–851. https://doi.org/10.1261/rna.053959.115
Smit AFA, Hubley R, Green P (1996-2010) RepeatMasker Open-3.0. http://www.repeatmasker.org/faq.html#faq3
Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S (eds) Bioinformatics and computational biology solutions using R and bioconductor, Statistics for Biology and Health. Springer, New York, pp 397–420. https://doi.org/10.1007/0-387-29362-0_23
Soumana IH, Tchicaya B, Simo G, Geiger A (2014) Comparative gene expression of Wigglesworthia inhabiting non-infected and Trypanosoma brucei gambiense-infected Glossina palpalis gambiensis flies. Front Microbiol 5(620). https://doi.org/10.3389/fmicb.2014.00620
Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4(41):41. https://doi.org/10.1186/1471-2105-4-41
Teruel M, Cabrero J, Perfectti F, Camacho JPM (2007) Nucleolus size variation during meiosis and NOR activity of a B chromosome in the grasshopper Eyprepocnemis plorans. Chromosom Res 15:755–765. https://doi.org/10.1007/s10577-007-1159-5
Teruel M, Cabrero J, Perfectti F, Alché JD, Camacho JPM (2009) Abnormal spermatid formation in the presence of the parasitic B24 chromosome in the grasshopper Eyprepocnemis plorans. Sex Dev 3:284–289. https://doi.org/10.1159/000253307
Teruel M, Cabrero J, Perfectti F, Camacho JPM (2010) B chromosome ancestry revealed by histone genes in the migratory locust. Chromosoma 119:217–225. https://doi.org/10.1007/s00412-009-0251-3
Teruel M, Sørensen JG, Loeschcke V, Cabrero J, Perfectti F, Camacho JPM (2011) Level of heat shock proteins decreases in individuals carrying B-chromosomes in the grasshopper Eyprepocnemis plorans. Cytogenet Genome Res 132:94–99. https://doi.org/10.1159/000319621
Trifonov VA, Dementyeva PV, Larkin DM, O’Brien PCM, Perelman PL, Yang F, Ferguson-Smith MA, Graphodatsky AS (2013) Transcription of a protein-coding gene on B chromosomes of the Siberian roe deer (Capreolus pygargus). BMC Biol 11:90. https://doi.org/10.1186/1741-7007-11-90
UniProt Consortium (2014) Activities at the universal protein resource (UniProt). Nucleic Acids Res 42(Database issue):D191–D198. https://doi.org/10.1093/nar/gkt1140
Valente GT, Conte MA, Fantinatti BE et al (2014) Origin and evolution of B chromosomes in the cichlid fish Astatotilapia latifasciata based on integrated genomic analyses. Mol Biol Evol 31:2061–2072. https://doi.org/10.1093/molbev/msu148
Valente GT, Nakajima RT, Fantinatti BEA, Marques DF, Almeida RO, Simões RP, Martins C (2017) B chromosomes: from cytogenetics to systems biology. Chromosoma 126:73–81. https://doi.org/10.1007/s00412-016-0613-6
Van Vugt JJ, de Nooijer S, Stouthamer R, de Jong H (2005) NOR activity and repeat sequences of the paternal sex ratio chromosome of the parasitoid wasp Trichogramma kaykai. Chromosoma 114:410–419. https://doi.org/10.1007/s00412-005-0026-4
Wang X, Fang X, Yang P, Jiang X, Jiang F, Zhao D, Li B, Cui F, Wei J, Ma C, Wang Y, He J, Luo Y, Wang Z, Guo X, Guo W, Wang X, Zhang Y, Yang M, Hao S, Chen B, Ma Z, Yu D, Xiong Z, Zhu Y, Fan D, Han L, Wang B, Chen Y, Wang J, Yang L, Zhao W, Feng Y, Chen G, Lian J, Li Q, Huang Z, Yao X, Lv N, Zhang G, Li Y, Wang J, Wang J, Zhu B, Kang L (2014) The locust genome provides insight into swarm formation and long-distance flight. Nat Commun 5(2957):2957. https://doi.org/10.1038/ncomms3957
Weinkove D, Neufeld TP, Twardzik T, Waterfield MD, Leevers SJ (1999) Regulation of imaginal disc cell size, cell number and organ size by Drosophila class IA phosphoinositide 3-kinase and its adaptor. Curr Biol 9:1019–1029. https://doi.org/10.1016/S0960-9822(99)80450-3
Wu S, Zhu Z, Fu L, Niu B, Li W (2011) WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics 12(444). https://doi.org/10.1186/1471-2164-12-444
Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M, Kuroiwa A, Hirai H, Hirai Y, Matsuda Y, Okada N (2011) B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet 7:e1002203. https://doi.org/10.1371/journal.pgen.1002203
Zhou Q, Zhu HM, Huang QF, Xuan ZL, Zhang GJ, Zhao L, Ding Y, Roy S, Vicoso B, Ruan J, Zhang Y, Zhao RP, Mu B, Min JM, Zhang QH, Li JW, Luo YL, Liang ZH, Ye C, Li RQ, Zhang XQ, Wang J, Wang W, Bachtrog D (2012) Deciphering neo-sex and B chromosome evolution by the draft genome of Drosophila albomicans. BMC Genomics 13:109. https://doi.org/10.1186/1471-2164-13-109
Zurita S, Cabrero J, López-León MD, Camacho JPM (1998) Polymorphism regeneration for a neutralized selfish B chromosome. Evolution 52:274–277. https://doi.org/10.1111/j.1558-5646.1998.tb05163.x
Acknowledgments
We thank Rubén Martín-Blázquez and Mohammed Bakkali for their collaboration on the Illumina transcriptome reads sequencing and first assembly, Marco Pellino for his help on the microarray hybridization step, and Álvaro Enciso for informatics support.
Funding
This study was funded by the Spanish Ministerio de Economía y Competitividad (CGL2015-70750-P) and was partially performed by FEDER funds. Navarro-Domínguez was supported by a FPI fellowship from the Spanish Ministerio de Ciencia e Innovación (BES-2010-030016).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All experiments comply with the current Spanish laws.
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights and informed consent
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Navarro-Domínguez, B., Martín-Peciña, M., Ruiz-Ruano, F.J. et al. Gene expression changes elicited by a parasitic B chromosome in the grasshopper Eyprepocnemis plorans are consistent with its phenotypic effects. Chromosoma 128, 53–67 (2019). https://doi.org/10.1007/s00412-018-00689-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-018-00689-y