The B chromosomes exhibit diverse behaviour compared with conventional genetic models. The capacity of the B chromosome either to accumulate or to be eliminated in a tissue-specific manner is dependent on biological processes related to aberrant cell division(s), but here yet remains compatible with normal development. We studied B chromosome elimination in Sorghum purpureosericeum embryos through cryo-sections and demonstrated the B chromosome instability during plant growth using flow cytometry, molecular markers and fluorescent in situ hybridization techniques. Consequently, using B chromosome-specific probes we revealed the non-Mendelian inheritance of B chromosomes in developing pollen. We disclosed that the occurrence of the B chromosome is specific to certain tissues or organs. The distribution pattern is mainly caused by an extensive elimination that functions primarily during embryo development and persists throughout plant development. Furthermore, we described that B chromosome accumulation can occur either by nondisjunction at first pollen mitosis (PMI) or the initiation of extra nuclear division(s) during pollen development. Our study demonstrates the existence of a not-yet-fully described B chromosome drive process, which is likely under the control of the B chromosome.

Department of Cell Biology and Genetics Faculty of Science Palacky University Šlechtitelů 27 779 00 Olomouc Czech Republic

Institute of Experimental Botany of the Czech Academy of Sciences Centre of Plant Structural and Functional Genomics Šlechtitelů 31 779 00 Olomouc Czech Republic

Laboratory of Pollen Biology Institute of Experimental Botany of the Czech Academy of Sciences Rozvojová 263 165 02 Prague 6 Lysolaje Czech Republic

Leibniz Institute of Plant Genetics and Crop Plant Research 06466 Seeland OT Gatersleben Germany

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Alexander MP. 1969. Differential staining of aborted and non‐aborted pollen. Stain Technology 44: 117–122.

Baenziger H. 1962. Supernumerary chromosomes in diploid and tetraploid forms of crested wheatgrass. Canadian Journal of Botany 40: 549–561.

Becher H, Powell RF, Brown MR, Metherell C, Pellice J, Leitch IJ, Twyford AD. 2021. The nature of intraspecific and interspecific genome size variation in taxonomically complex eyebrights. Annals of Botany 128: 639–651.

Bednářová M, Karafiátová M, Hřibová E, Bartoš J. 2021. B chromosomes in genus Sorghum (Poaceae). Plants 10: 1–13.

Bernardino AC, Cabral‐de‐Mello DC, Machado CB, Palacios‐Gimenez OM, Santos N, Loreto VB. 2017. B chromosome variants of the grasshopper Xyleus discoideus angulatus are potentially derived from pericentromeric DNA. Cytogenetic and Genome Research 152: 213–221.

Biederman MK, Nelson MM, Asalone KC, Pedersen AL, Saldanha CJ, Bracht JR. 2018. Discovery of the first germline‐restricted gene by subtractive transcriptomic analysis in the zebra finch Taeniopygia guttata. Current Biology 28: 1620–1627.

Birchler JA. 2015. Promises and pitfalls of synthetic chromosomes in plants. Trends in Biotechnology 33: 189–193.

Birchler JA, Yang H. 2021. The supernumerary B chromosome of maize: drive and genomic conflict. Open Biology 11: 210197.

Borodin P, Chen A, Forstmeier W, Fouché S, Malinovskaya L, Pei Y, Reifová R, Ruiz‐Ruano F, Schlebusch SA, Sotelo‐Muňoz TA et al. 2022. Mendelian nightmares: the germline –restricted chromosome of songbirds. Chromosome Research 30: 255–272.

Chen J, Birchler JA, Houben A. 2022. The non‐Mendelian behaviour of plant B chromosomes. Chromosome Research 30: 229–239.

Cuevas A, Ravinet M, Sætre GP, Eroukhmanoff F. 2021. Intraspecific genomic variation and local adaptation in a young hybrid species. Molecular Ecology 30: 791–809.

Darlington CD, Thomas TRS, Thomas PT. 1941. Morbid mitosis and the activity of inert chromosomes in Sorghum. Proceedings of the Royal Society B: Biological Sciences 130: 127–150.

Doležel J, Binarová P, Lucretti S. 1989. Analysis of nuclear DNA content in plant cells by flow cytometry. Biologia Plantarum 31: 113–120.

Ebrahimzadegan R, Fuchs J, Chen J, Schubert V, Houben A, Mirzaghaderi G. 2023. Meiotic segregation and post‐meiotic drive of the Festuca pratensis B chromosome. Chromosome Research 31: 26.

Escriba MC, Giardini MC, Goday C. 2011. Histone H3 phosphorylation and nondisjunction of the maternal X chromosomes during male meiosis in sciarid flies. Journal of Cell Sciences 124: 1715–1725.

Escriba MC, Goday C. 2013. Histone H3 phosphorylation and elimination of paternal X chromosomes at early cleavages in sciarid flies. Journal of Cell Sciences 126: 3214–3222.

Fahn A. 1990. Plant anatomy, 4th edn. Oxford, UK: Pergamon Press.

Fröst S. 1957. The inheritance of accessory chromosomes in Centauria scabiosa. Hereditas 43: 403–422.

Fröst S. 1969. The inheritance of accessory chromosomes in plants, especially in Ranunculus acris and Pheleum nodosum. Hereditas 61: 317–326.

Goday C, Esteban MR. 2001. Chromosome elimination in sciarid flies. BioEssay 23: 242–250.

Gutiérrez ML, Rodríguez‐González R, Fuentes I, Gálvez‐Prada F, Kovařík A, Garcia S. 2023. First update to B‐Chrom: a database on B‐chromosomes. In: Garcia S, Nualart N, eds. Plant genomic and cytogenetic databases. Methods in molecular biology, vol. 2703. New York, NY, USA: Humana, 227–236.

Häkansson A. 1954. Transmission of accessory chromosomes in Poa alpina. Hereditas 40: 523–526.

Hariprasanna K, Patil JV. 2015. Sorghum: origin, classification, biology and improvement. In: Madhusudhana R, Rajendrakumar P, Patil J, eds. Sorghum molecular breeding. New Delhi, India: Springer, 3–20.

Houben A. 2017. B chromosomes – a matter of chromosome drive. Frontiers in Plant Science 15: 210.

Houben A, Ma W, Banaei‐Moghaddam AM. 2021. The B chromosome of rye. In: Rabanus‐Wallace MT, Stein N, eds. The Rye genome. Compendium of plant genomes. Cham, Switzerland: Springer, 63–76.

Janaki‐Ammal EK. 1940. Chromosome diminuition in plant. Nature 146: 839–840.

Jones RN, Gonzáles‐Sanchez M, Gonzáles‐García M, Vega JM, Puertas MJ. 2008. Chromosomes with a life of their own. Cytogenetic and Genome Research 120: 265–280.

Jones RN, Rees H. 1982. B chromosomes. London, UK: Academic Press.

Karafiátová M, Bartoš J, Kopecký D, Ma L, Sato K, Houben A, Stein N, Doležel J. 2013. Mapping nonrecombining regions in barley using multicolor FISH. Chromosome Research 21: 739–751.

Karafiátová M, Bednářová M, Said M, Čížková J, Holušová K, Blavet N, Bartoš J. 2021. B chromosome of Sorghum purpureosericeum reveals the first pieces of its sequence. Journal of Experimental Botany 72: 1606–1616.

Kato A, Lamb JC, Birchler JA. 2004. Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proceedings of the National Academy of Sciences, USA 101: 13554–13559.

Lie Y, Fu X, Thao M, Zhang W, Li B, An D, Li J, Zhang A, Liu R, Liu X. 2018. A genome‐wide transcriptome dynamics during early spike development in bread wheat. Scientific Reports 8: 15338.

Lynch M, Marinov GK. 2015. The bioenergetic costs of a gene. Proceedings of the National Academy of Sciences, USA 112: 15690–15695.

Majka J, Glombik M, Doležalová A, Kneřová J, Ferreira MTM, Zwierzykowski Z, Duchoslav M, Studer B, Doležel J, Bartoš J et al. 2023. Both male and female meiosis contribute to non‐Mendelian inheritance of parental chromosomes in interspecific plant hybrids (Lolium × Festuca). New Phytologist 238: 624–636.

MsLeisch J. 1954. B‐chormosomes in Ranunculus ficaria. Annual Report – John Innes Horticultural Institution 45: 21–22.

Müntzing A, Nygren A. 1955. A new diploid variety of Poa alpina accessory chromosomes at meiosis. Hereditas 41: 405–422.

Němečková A, Koláčková V, Vrána J, Doležel J, Hřibová E. 2020. DNA replication and chromosome positioning throughout the interphase in three‐dimensional space of plant nuclei. Journal of Experimental Botany 71: 6262–6272.

Nygren A. 1957. Poa timoleontis Heldr., a new diploid species of the section Bolbophorum and Gr. with accessory chromosomes only in meiosis. Kungliga Lantbrukshögskolans Annaler 23: 489–495.

Östergren G, Frost S. 1962. Elimination of accessory chromosomes from the roots in Haplopappus gracilis. Hereditas 48: 363–366.

Pereira HS, Delgado M, Viegas W, Rato JM, Barao A, Caperta AD. 2017. Rye (Secale cereal) supernumerary (B) chromosomes associated with heat tolerance during early stahes of male sporogenesis. Annals of Botany 119: 325–337.

Plowman A, Bougourd S. 1994. Selectively advantageous effects of B chromosomes on germination behaviour in Allium schoenoprasum L. Heredity 72: 587–593.

Rees H. 1974. B chromosomes. Science Progress 61: 535–554.

Reynolds TL. 1997. Pollen embryogenesis. Plant Molecular Biology 33: 1–10.

Roman H. 1947. Mitotic nondisjunction in the case of interchanges involving the B‐type chromosome in maize. Genetics 32: 391–409.

Roman H. 1948. Directed fertilization in maize. Proceedings of the National Academy of Sciences, USA 34: 36–42.

Ruban A, Schmutzer T, Wu DD, Fuchs J, Boudichevskaia A, Rubtsova M, Pistrick K, Melzer M, Himmelbach A, Schubert V et al. 2020. Supernumerary B chromosomes of Aegilops speltoides undergo precise elimination in roots early in embryo development. Nature Communications 11: 2764.

Said M, Hřibová E, Danilova TV, Karafiátová M, Čížková J, Friebe B, Doležel J, Gill BS, Vrána J. 2018. The Agropyron cristatum karyotype, chromosome structure and cross‐genome homeoology as revealed by fluorescence in situ hybridization with tandem repeats and wheat single‐gene probes. Theoretical and Applied Genetics 131: 2213–2227.

Sánchez L. 2014. Sex‐determining mechanisms in insects based on imprinting and elimination of chromosomes. Sexual Development 8: 83–103.

Schmid M, Ziegler CG, Steinlein C, Nanda I, Haaf T. 2002. Chromosome banding in Amphibia: XXIV. The B chromosomes of Gastrotheca espeletia (Anura, Hylidae). Cytogenetic and Genome Research 97: 205–218.

Schoenmakers S, Wassenaar E, Laven JS, Grootegoed JA, Baarends WM. 2010. Meiotic silencing and fragmentation of the male germline restricted chromosome in zebra finch. Chromosoma 119: 311–324.

Stevens JP, Bougourd SM. 1994. Unstable B‐chromosomes in a European population of Allium schoenoprasum L. (Liliaceae). Biological Journal of the Linnean Society 52: 357–363.

Steward FC. 1970. From cultured cells to whole plants: the induction and control of their growth and morphogenesis. Proceedings of the Royal Society of London. Series B. Biological Sciences 175: 1–30.

Touraev A, Ilham A, Vicente O, Heberle‐Bors E. 1996. Stress induced microspore embryogenesis in tobacco – an optimized systems for molecular studies. Plant Cell Reports 15: 561–565.

Vasil IK. 1984. Cell culture and somatic cell genetics of plants. Vol 1. Laboratory procedures and their applications. New York, NY, USA: New York Academic Press.

Walla A, Wilma van Esse G, Kirschner GK, Guo G, Brünje A, Finkemeier I, Simon R, von Korff M. 2020. An Acyl‐CoA N‐acyltransferase regulates meristem phase change and plant architecture in barley. Plant Physiology 3: 1088–1109.

Wang J, Davis RE. 2015. Programmed DNA elimination in extra‐cellular organism. Current Opinion in Genetics & Development 27: 26–34.

Wu DD, Ruban A, Fuchs J, Macas J, Novák P, Vaio M, Zhou YH, Houben A. 2019. Nondisjunction and unequal spindle organization accompany the drive of Aegilops speltoides B chromosomes. New Phytologist 223: 1340–1352.

Wu TP. 1984. B–chromosomes in Sorghum purpureosericeum. Proceedings of National Science Council, Republic of China 8: 198–209.

Zufall RA, Robinson T, Katz LA. 2005. Evolution of developmentally regulated genome rearrangements in eukaryots. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 304: 448–455.