Post-meiotic B chromosome expulsion, during spermiogenesis, in two grasshopper species
- 326 Downloads
Most supernumerary (B) chromosomes are parasitic elements carrying out an evolutionary arms race with the standard (A) chromosomes. A variety of weapons for attack and defense have evolved in both contending elements, the most conspicuous being B chromosome drive and A chromosome drive suppression. Here, we show for the first time that most microspermatids formed during spermiogenesis in two grasshopper species contain expulsed B chromosomes. By using DNA probes for B-specific satellite DNAs in Eumigus monticola and Eyprepocnemis plorans, and also 18S rDNA in the latter species, we were able to count the number of B chromosomes in standard spermatids submitted to fluorescence in situ hybridization, as well as visualizing B chromosomes inside most microspermatids. In E. plorans, the presence of B-carrying microspermatids in 1B males was associated with a significant decrease in the proportion of B-carrying standard spermatids. The fact that this decrease was apparent in elongating spermatids but not in round ones demonstrates that meiosis yields 1:1 proportions of 0B and 1B spermatids and hence that B elimination takes place post-meiotically, i.e., during spermiogenesis, implying a 5–25% decrease in B transmission rate. In E. monticola, the B chromosome is mitotically unstable and B number varies between cells within a same individual. A comparison of B frequency between round and elongating spermatids of a same individual revealed a significant 12.3% decrease. We conclude that B chromosome elimination during spermiogenesis is a defense weapon of the host genome to get rid of parasitic chromosomes.
KeywordsFISH Micronucleus Microspermatids Parasitic Satellite DNA
We thank M. Teruel and J.D. Alché for their help to obtain the electron microscope photograph in Fig. 2f. This study was supported by a grant from the Spanish Secretaría de Estado de Investigación, Desarrollo e Innovación (CGL2015-70750-P) and was partially performed by FEDER funds.
Compliance with ethical standards
Integrity of research
All experiments comply with the current Spanish laws.
Conflict of interest
The authors declare that they have no competing interests.
Human and animal rights and informed consent
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Avdulow NP (1933) On the additional chromosomes in maize. Bull Appl Bot Ser 2:101–130Google Scholar
- Cabrero J, López-León MD, Ruíz-Estévez M, Gómez R, Petitpierre E, Rufas JS, Massa B, Kamel Ben Halima M, Camacho JPM (2014) B1 was the ancestor B chromosome variant in the western Mediterranean area in the grasshopper Eyprepocnemis plorans. Cytogenet Genome Res 142:54–58. doi: 10.1159/000356052 CrossRefPubMedGoogle Scholar
- Camacho JPM, Cabrero J, López-León MD, Cabral-de-Mello DC, Ruiz-Ruano FJ (2015a) Grasshoppers (Orthoptera). In: Sharakhov IV (ed) Protocols for cytogenetic mapping of arthropod genomes. CRC Press, pp 381–438Google Scholar
- Fenech M, Kirsch-Volders M, Natarajan AT, Surralles J, Crott JW, Parry J, Norppa H, Eastmond DA, Tucker JD, Thomas P (2011) Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 26:125–132. doi: 10.1093/mutage/geq052 CrossRefPubMedGoogle Scholar
- Finch KA, Fonseka KGL, Abogrein A, Ioannou D, Handyside AH, Thornhill AR, Hickson N, Griffin DK (2008) Nuclear organization in human sperm: preliminary evidence for altered sex chromosome centromere position in infertile males. Hum Reprod 23:1263–1270. doi: 10.1093/humrep/den112 CrossRefPubMedGoogle Scholar
- Gernand D, Rutten T, Varshney A, Rubtsova M, Prodanovic S, Brüβ KCJ, Matzk F, Houben A (2005) Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation. Plant Cell 17:2431–2438. doi: 10.1105/tpc.105.034249 CrossRefPubMedPubMedCentralGoogle Scholar
- Gernand D, Rutten T, Pickering R, Houben A (2006) Elimination of chromosomes in Hordeum vulgare x H. bulbosum crosses at mitosis and interphase involves micronucleus formation and progressive heterochromatinization. Cytogenet Genome Res 114:169–174. doi: 10.1159/000093334 CrossRefPubMedGoogle Scholar
- Goday C, Esteban MR (2001) Chromosome elimination in sciarid flies. BioEssays 23:242–250. doi: 10.1002/1521-1878(200103)23:3<242::AID-BIES1034>3.0.CO;2-P CrossRefPubMedGoogle Scholar
- Milani D, Palacios-Gimenez OM, Cabral-de-Mello DC (2016) The U2 snDNA is a useful marker for B chromosome detection and frequency estimation in the grasshopper Abracris flavolineata. Cytogenet Genome Res (in press)Google Scholar
- Ruiz-Ruano FJ, Cabrero J, López-León MD, Camacho JPM (2016) Satellite DNA content illuminates the ancestry of a supernumerary (B) chromosome. Chromosoma (in press) doi: 10.1007/s00412-016-0611-8