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Decoding allelic diversity, transcript variants and transcriptional complexity of CENH3 gene in Brassica oleracea var. botrytis

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Abstract

Histone proteins play a critical role in the primary organization of nucleosomes, which is the fundamental unit of chromatin. Among the five types of the histones, histone H3 has multiple variants, and the number differs among the species. Amongst histone H3 variants, centromeric histone H3 (CENH3) is crucial for centromere identification and proper chromosomal segregation during cell division. In the present study, we have identified 17 putative histone H3 genes of Brassica oleracea. Furthermore, we have done a detailed characterization of the CENH3 gene of B. oleracea. We showed that a single CENH3 gene exhibits allelic diversity with at least two alleles and alternative splicing pattern. Also, we have identified a CENH3 gene–specific co-dominant cleaved amplified polymorphic sequence marker SNP34(A/C) to distinguish CENH3 alleles and follow their expression in leaf and flower tissues. The gene structure analysis of the CENH3 gene revealed the conserved 5′–CAGCAG–3′ sequence at the intron 3–exon 4 junction in B. oleracea, which serves as an alternative splicing site with one-codon (alanine) addition/deletion. However, this one-codon alternative splicing feature is not conserved in the CENH3 genes of wild allied Brassica species. Our finding suggests that transcriptional complexity and alternative splicing might play a key role in the transcriptional regulation and function of the CENH3 gene in B. oleracea. Altogether, data generated from the present study can serve as a primary information resource and can be used to engineer CENH3 gene towards developing haploid inducer lines in B. oleracea.

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Data availability

All the genomic and transcript sequences generated through this study were available at GenBank, National Center for Biotechnology information (NCBI; https://www.ncbi.nlm.nih.gov/genbank/), with the accession number given in the “Materials and methods” section.

References

  • Abdallah D, Baraket G, Perez V, Ben Mustapha S, Salhi-Hannachi A, Hormaza JI (2019) Analysis of self-incompatibility and genetic diversity in diploid and hexaploid plum genotypes. Front Plant Sci 10:896

    Article  PubMed  PubMed Central  Google Scholar 

  • Adams KL, Wendel JF (2005) Allele-specific, bidirectional silencing of an alcohol dehydrogenase gene in different organs of interspecific diploid cotton hybrids. Genetics 171:2139–2142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akerman M, Mandel-Gutfreund Y (2006) Alternative splicing regulation at tandem 3′ splice sites. Nucleic Acids Res 34:23–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhatia R, Dey RR, Sood S, Sharma K, Parkash C, Kumar R (2017) Efficient microspore embryogenesis in cauliflower (Brassica oleracea var. botrytis L.) for development of plants with different ploidy level and their use in breeding programme. Sci Hortic 216:83–92

    Article  Google Scholar 

  • Birchler JA, Gao Z, Sharma A, Presting GG, Han F (2011) Epigenetic aspects of centromere function in plants. Curr Opin Plant Biol 14:217–222

    Article  CAS  PubMed  Google Scholar 

  • Black BE, Foltz DR, Chakravarthy S, Luger K, Woods VLJR (2004) Structural determinants for generating centromeric chromatin. Nature 430:578–582

    Article  CAS  PubMed  Google Scholar 

  • Blower MD, Karpen GH (2001) The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat Cell Biol 3:730–739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradley RK, Merkin J, Lambert NJ, Burge CB (2012) Alternative splicing of RNA triplets is often regulated and accelerates proteome evolution. PLoS Biol 10:e1001229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchwitz BJ, Ahmad K, Moore LL, Roth MB, Henikoff S (1999) A histone-H3-like protein in C. elegans. Nature 401:547–548

    Article  CAS  PubMed  Google Scholar 

  • Dunemann F, Schrader O, Budahn H, Houben A (2014) Characterization of centromeric histone H3 (CENH3) variants in cultivated and wild carrots (Daucus sp.). PLoS One 9:e98504

    Article  PubMed  PubMed Central  Google Scholar 

  • Earnshaw WC, Rothfield N (1985) Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma 91:313–321

    Article  CAS  PubMed  Google Scholar 

  • Ekwall K (2007) Epigenetic control of centromere behavior. Annu Rev Genet 47:63–81

    Article  Google Scholar 

  • Elisafenko EA, Evtushenko EV, Vershinin AV (2021) The origin and evolution of a two-component system of paralogous genes encoding the centromeric histone CENH3 in cereals. BMC Plant Biol 21:541. https://doi.org/10.1186/s12870-021-03264-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evtushenko EV, Elisafenko EA, Gatzkaya SS, Lipikhina YA, Houben A, Vershinin AV (2017) Conserved molecular structure of the centromeric histone CENH3 in Secale and its phylogenetic relationships. Sci Rep 7:17628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evtushenko EV, Elisafenko EA, Gatzkaya SS, Schubert V, Houben A, Vershinin AV (2021) Expression of two rye CENH3 variants and their loading into centromeres. Plants 10(10):2043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

  • Foroozani M, Holder DH, Deal RB (2022) Histone variants in the specialization of plant chromatin. Annu Rev Plant Biol 73

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Heckmann S, Lermontova I, Berckmans B, De Veylder L, Bäumlein H, Schubert I (2011) The E2F transcription factor family regulates CENH3 expression in Arabidopsis thaliana. Plant J 68:646–656

    Article  CAS  PubMed  Google Scholar 

  • Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293:1098–1110

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiller M, Szafranski R, Backofen K, Platzer M (2006) Alternative splicing at NAGNAG acceptors: simply noise or noise and more? PLoS Genet 2:1944–1946

    Article  CAS  Google Scholar 

  • Hirsch CD, Wu Y, Yan H, Jiang J (2009) Lineage-specific adaptive evolution of the centromeric protein CENH3 in diploid and allotetraploid Oryza species. Mol Biol Evol 26:2877–2885

    Article  CAS  PubMed  Google Scholar 

  • Hughes TA (2006) Regulation of gene expression by alternative untranslated regions. Trends Genet 22:119–122

    Article  CAS  PubMed  Google Scholar 

  • Iida K, Shionyu M, Suso Y (2008) Alternative splicing at NAGNAG acceptor sites shares common properties in land plants and mammals. Mol Biol Evol 25:709–718

    Article  CAS  PubMed  Google Scholar 

  • Ingouff M, Berger F (2010) Histone3 variants in plants. Chromosoma 119:27–33

    Article  CAS  PubMed  Google Scholar 

  • Ishii T, Juranic M, Maheshwari S, Bustamante FO, Vogt MM, Gamboa R, Dreissig S, Gursanscky N, How T, Fuchs J, Schubert V, Spriggs A, Vielle-Calzada JP, Comai L, Koltunow AMG, Houben A (2020) Unequal contribution of two paralogous centromeric histones to function the cowpea centromere. bioRxiv. https://doi.org/10.1101/2020.01.07.897074

    Book  Google Scholar 

  • Jones P, Binns D, Chang HY et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics. 30(9):1236–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalia P, Singh S, Parkash C, Dey SS (2016) Cole vegetables enhancing volume of vegetable basket. Indian Hortic 61:77–81

    Google Scholar 

  • Kapustin Y, Souvorov A, Tatusova T, Lipman D (2008) Splign: algorithms for computing spliced alignments with identification of paralogs. Biol Direct 3:20

    Article  PubMed  PubMed Central  Google Scholar 

  • Karimi-Ashtiyani R, Ishii T, Niessen M, Stein N, Heckmann S, Gurushidze M et al (2015) Point mutation impairs centromeric CENH3 loading and induces haploid plants. Proc Natl Acad Sci U.S.A. 112:11211–11216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasha KJ, Kao KN (1970) High frequency haploid production in barley (Hordeum vulgare L.). Nature 225:874–876

    Article  CAS  PubMed  Google Scholar 

  • Kawabe A, Nasuda S, Charlesworth D (2006) Duplication of centromeric histone H3 (HTR12) gene in Arabidopsis halleri and A. lyrata, plant species with multiple centromeric satellite sequences. Genetics 174:2021–2032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Stenberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuppu S, Ron M, Marimuthu MPA, Li G, Huddleson A, Siddeek MH, Terry J, Buchner R, Shabek N, Comai L, Britt AB (2020a) A variety of changes, including CRISPR/Cas9-mediated deletions, in CENH3 lead to haploid induction on outcrossing. Plant Biotechnol J. 18(10):2068–2080. https://doi.org/10.1111/pbi.13365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuppu S, Tan EH, Nguyen H, Rodgers A, Comai L, Chan SWL, Britt AB (2015) Point mutations in centromeric histone induce post-zygotic incompatibility and uniparental inheritance. PLoS Genet 11:e1005494

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuppu S, Ron M, Marimuthu MP, Li G, Huddleson A, Siddeek MH, Terry J, Buchner R, Shabek N, Comai L, Britt AB (2020b) A variety of changes, including CRISPR/Cas9-mediated deletions, in CENH3 lead to haploid induction on outcrossing. Plant Biotechnol J 18(10):2068–2080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kursel LE, Malik HS (2017) Recurrent gene duplication leads to diverse repertoires of centromeric histones in Drosophila species. Mol Biol Evol 34(6):1445–1462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lermontova I, Schubert V, Fuchs J, Klatte S, Macas J, Schubert I (2006) Loading of Arabidopsis centromeric histone CENH3 occurs mainly during G2 and requires the presence of the histone fold domain. Plant Cell 18:2443–2451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot MP, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Liu Y, Yang X et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930

    Article  CAS  PubMed  Google Scholar 

  • Lv J, Yu K, Wei J, Gui H, Liu C, Liang D, Wang Y, Zhou H, Carlin R, Rich R, Lu T (2020) Generation of paternal haploids in wheat by genome editing of the centromeric histone CENH3. Nat Biotechnol 38(12):1397–1401

    Article  CAS  PubMed  Google Scholar 

  • Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nat Struct Biol 10:882–889

    Article  CAS  PubMed  Google Scholar 

  • Malik HS, Henikoff S (2009) Major evolutionary transitions in centromere complexity. Cell 138:1067–1082

    Article  CAS  PubMed  Google Scholar 

  • Manchali S, Murthy KNC, Patil BS (2012) Crucial facts about health benefits of popular cruciferous vegetables. J Funct Foods 4:94–106

    Article  CAS  Google Scholar 

  • Masonbrink RE, Gallagher JP, Jareczek JJ, Renny-Byfield S, Grover CE, Gong L, Wendel JF (2014) CENH3 evolution in diploids and polyploids of three angiosperm genera. BMC Plant Biol 14:383

    Article  PubMed  PubMed Central  Google Scholar 

  • Matos I, Machado MP, Schartl M, Coelho MM (2019) Allele-specific expression variation at different ploidy levels in Squalius alburnoides. Sci Rep 9:3688

    Article  PubMed  PubMed Central  Google Scholar 

  • Mayr C (2016) Evolution and biological roles of alternative 3′UTRs. Trends Cell Biol 26:227–237

    Article  CAS  PubMed  Google Scholar 

  • McKinley KL, Cheeseman IM (2016) The molecular basis for centromere identity and function. Nat Rev Mol Cell Biol 17:16

    Article  CAS  PubMed  Google Scholar 

  • Mendiburo MJ, Padeken J, Fülöp S, Schepers A, Heun P (2011) Drosophila CENH3 is sufficient for centromere formation. Science 334:686–690

    Article  CAS  PubMed  Google Scholar 

  • Miao J, Frazier T, Huang L, Zhang X, Zhao B (2016) Identification and characterization of switch grass histone H3 and CENH3 genes. Front Plant Sci 7:979

    Article  PubMed  PubMed Central  Google Scholar 

  • Moraes IC, Lermontova I, Schubert I (2011) Recognition of A. thaliana centromeres by heterologous CENH3 requires high similarity to the endogenous protein. Plant Mol Biol 75:253–261

    Article  CAS  PubMed  Google Scholar 

  • Muiruri KS, Britt A, Amugune NO, Nguu EK, Chan S, Tripathi L (2017) Expressed centromere specific histone 3 (CENH3) variants in cultivated triploid and wild diploid bananas (Musa spp.). Front. Plant Sci 8:1034

    Google Scholar 

  • Müller S, Almouzni G (2014) A network of players in H3 histone variant deposition and maintenance at centromeres. Biochim Biophys Acta 1839:241–250

    Article  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagaki K, Cheng Z, Ouyang S, Talbert PB, Kim M, Jones KM, Henikoff S, Buell CR, Jiang J (2004) Sequencing of a rice centromere uncovers active genes. Nat Genet 36:138–145

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Kashihara K, Murata MA (2009) Centromere DNA sequence colocalized with a centromere-specific histone H3 in tobacco. Chromosoma 118:249–257

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Murata M (2005) Characterization of CENH3 and centromere-associated DNA sequences in sugarcane. Chromosome Res. 13:195–203

    Article  CAS  PubMed  Google Scholar 

  • Nagaki K, Yamamoto M, Yamaji N, Mukai Y, Murata M (2012) Chromosome dynamics visualized with an anti-centromeric histone H3 antibody in Allium. PLoS One 7:e51315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann P, Navratilova A, Schroeder-Reiter E, Koblizkova A, Steinbauerova V, Chocholova E, Novak P, Wanner G, Macas J (2012) Stretching the rules: monocentric chromosomes with multiple centromere domains. PLoS Genet 8:e1002777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neumann P, Pavlíková Z, Koblížková A, Fuková I, Jedličková V, Novák P, Macas J (2015) Centromeres off the hook: massive changes in centromere size and structure following duplication of CenH3 gene in Fabeae species. Mol Biol Evol 32:1862–1879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okada T, Endo M, Singh MB, Bhalla PL (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44:557–568

    Article  CAS  PubMed  Google Scholar 

  • Qanmber G, Ali F, Lu L, Mo H, Ma S, Wang Z, Yang Z (2019) Identification of histone H3 (HH3) genes in Gossypium hirsutum revealed diverse expression during ovule development and stress responses. Genes 10:355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pauli S, Rothnie HM, Chen G, He Xiaoyuan, HT (2004) The Cauliflower Mosaic Virus 35S Promoter Extends into the Transcribed Region. Journal of Virology 78(22):12120–12128. https://doi.org/10.1128/JVI.78.22.12120-12128.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravi M, Chan SW (2010) Haploid plants produced by centromere-mediated genome elimination. Nature. 464:615–618

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sanei M, Pickering R, Kumke K, Nasuda S, Houben A (2011) Loss of centromeric histone H3 (CENH3) from centromeres precedes uniparental chromosome elimination in interspecific barley hybrids. Proc Natl Acad Sci USA 108:E498–E505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena MS, Bajaj D, Kujur A, Das S, Badoni S, Kumar V, Singh M, Bansal KC, Tyagi AK, Parida SK (2014) Natural allelic diversity, genetic structure and linkage disequilibrium pattern in wild chickpea. PLoS One 9:e107484

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh BK, Singh B, Singh PM (2018) Breeding cauliflower: a review. Int J Veg Sci 24:158–184

    Article  Google Scholar 

  • Solovyev V, Kosarev P, Seledsov I, Vorobyev D (2006) Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol 7(Suppl 1):10.1–10.12

    Article  Google Scholar 

  • Stajič E, Kiełkowska A, Murovec J, Bohanec B (2019) Deep sequencing analysis of CRISPR/Cas9 induced mutations by two delivery methods in target model genes and the CENH3 region of red cabbage (Brassica oleracea var. capitata f. rubra). Plant Cell Tissue Organ Cult 139(2):227–235

    Article  Google Scholar 

  • Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M (1995) A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev 9:573–586

    Article  CAS  PubMed  Google Scholar 

  • Stroud H, Otero S, Desvoyes B, Ramírez-Parra E, Jacobsen SE, Gutierrez C (2012) Genome-wide analysis of histone H3.1 and H3.3 variants in Arabidopsis thaliana. Proc Natl Acad Sci U S A 109:5370–5375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun D, Wang C, Zhang X, Zhang W, Jiang H, Yao X, Liu L, Wen Z, Niu G, Shan X (2019) Draft genome sequence of cauliflower (Brassica oleracea L. var. botrytis) provides new insights into the C genome in Brassica species. Hortic Res 6:82

    Article  PubMed  PubMed Central  Google Scholar 

  • Takahashi K, Chen ES, Yanagida M (2000) Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast. Science 288:2215–2219

    Article  CAS  PubMed  Google Scholar 

  • Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S (2002) Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell 14:1053–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tek AL, Kara Öztürk SD (2020) High allelic diversity of the centromere-specific histone H3 (CENH3) in the legume sainfoin (Onobrychis viciifolia). Mol Biol Rep 47:8789–8795. https://doi.org/10.1007/s11033-020-05926-1

    Article  CAS  PubMed  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wang G, He Q, Liu F, Cheng Z, Talber PB, Jin W (2011) Characterization of CENH3 proteins and centromere-associated DNA sequences in diploid and allotetraploid Brassica species. Chromosoma 120:353–365

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Zong M, Liu D, Wu Y, Tian S, Han S, Guo N, Duan M, Miao L, Liu F (2022) Efficient generation of targeted point mutations in the Brassica oleracea var. botrytis genome via a modified CRISPR/Cas9 system. Hortic Plant J 8:527–530

    Article  Google Scholar 

  • Wang N, Gent JI, Dawe RK (2021) Haploid induction by a maize cenh3 null mutant. Sci Adv 7(4):eabe2299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watts A, Bhadouria J, Kumar V, Bhat SR (2016) Assessment of Arabidopsis thaliana CENH3 promoter in Brassica juncea for development of haploid inducer lines. Indian J Exp Biol 54:425–430

    PubMed  Google Scholar 

  • Zhong C, Marshall J, Topp C (2002) Centromeric retroelements and satellites interact with maize kinetochore protein CENH3. Plant Cell 14:2825–2836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu W, Giangrande PH, Nevins JR (2004) E2Fs link the control of G1/S and G2/M transcription. EMBO J 23:4615–4626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins by. Academic Press, New York, pp 97–166

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Acknowledgements

We are very grateful to Dr. S. R. Bhat, Emeritus Scientist, ICAR-NIPB, New Delhi, India, for providing useful comments and suggestions which helped in improving the manuscript.

Funding

The DST-SERB, Government of India (ECR/2016/001788), provided financial assistance for the project.

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  1. Ritesh Kumar Raipuria and Anshul Watts contributed equally to this work.

Authors and Affiliations

  1. ICAR-National Institute for Plant Biotechnology, Pusa Campus, New Delhi, 110012, India

    Ritesh Kumar Raipuria, Anshul Watts & Ramcharan Bhattacharya

  2. Division of Vegetable Science, ICAR-Indian Agricultural Research Institute, Pusa Campus, New Delhi, 110012, India

    Brij Bihari Sharma

  3. Division of Plant Physiology, ICAR-Indian Agricultural Research Institute, Pusa Campus, New Delhi, 110012, India

    Archana Watts

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Raipuria, R.K., Watts, A., Sharma, B.B. et al. Decoding allelic diversity, transcript variants and transcriptional complexity of CENH3 gene in Brassica oleracea var. botrytis. Protoplasma 260, 1149–1162 (2023). https://doi.org/10.1007/s00709-023-01837-7

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