Abstract
Key message
Cytological observations of chromosome pairing showed that evolutionarily genome duplication might reshape non-homologous pairing during meiosis in haploid B. rapa.
Abstract
A vast number of flowering plants have evolutionarily undergone whole genome duplication (WGD) event. Typically, Brassica rapa is currently considered as an evolutionary mesohexaploid, which has more complicated genomic constitution among flowering plants. In this study, we demonstrated chromosome behaviors in haploid B. rapa to understand how meiosis proceeds in presence of a single homolog. The findings showed that a diploid-like chromosome pairing was generally adapted during meiosis in haploid B. rapa. Non-homologous chromosomes in haploid cells paired at a high-frequency at metaphase I, over 50% of examined meiocytes showed at least three pairs of bivalents then equally segregated at anaphase I during meiosis. The fluorescence immunostaining showed that the cytoskeletal configurations were mostly well-organized during meiosis. Moreover, the expressed genes identified at meiosis in floral development was rather similar between haploid and diploid B. rapa, especially the expression of known hallmark genes pivotal to chromosome synapsis and homologous recombination were mostly in haploid B. rapa. Whole-genome duplication evolutionarily homology of genomic segments might be an important reason for this phenomenon, which would reshape the first division course of meiosis and influence pollen development in plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: (National Center for Biotechnology Information (NCBI) BioProject number: PRJNA642307).
References
Armstrong KC, Keller WA (1981) Chromosome pairing in haploids of Brassica campestris. Theor Appl Genet 59:49–52. https://doi.org/10.1007/bf00275776
Armstrong KC, Keller WA (1982) Chromosome pairing in haploids of Brassica oleracea. Can J Genet Cytol 24:735–739. https://doi.org/10.1139/g82-079
Braynen J, Yang Y, Wei F, Cao G, Shi G, Tian B et al (2017) Transcriptome analysis of floral buds deciphered an irregular course of meiosis in polyploid Brasscia rapa. Front Plant Sci 8:768. https://doi.org/10.3389/fpls.2017.00768
Chen C, Xu Y, Ma H, Chong K (2005) Cell biological characterization of male meiosis and pollen development in rice. J Integr Plant Biol 47:734–744. https://doi.org/10.1111/j.1744-7909.2005.00102.x
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the Mesohexaploid Brassica rapa. Plant Cell 25:1541–1554. https://doi.org/10.1105/tpc.113.110486
Cifuentes M, Rivard M, Pereira L, Chelysheva L, Mercier R (2013) Haploid meiosis in Arabidopsis: double-strand breaks are formed and repaired but without synapsis and crossovers. PLoS ONE 8:e72431. https://doi.org/10.1371/journal.pone.0072431
Collins GB, Sadasivaiah RS (1972) Meiotic analysis of haploid and doubled haploid forms of Nicotiana otophora and N. tabacum. Chromosoma 38:387–404. https://doi.org/10.1007/BF00320158
Crane CF, Beversdorf WF, Bingham ET (1982) Chromosome pairing and associations at meiosis in haploid soybean (Glycine max). Can J Genet Cytol 24:293–300. https://doi.org/10.1139/g82-031
Forster BP, Heberle-Bors E, Kasha KJ, Touraev A (2007) The resurgence of haploids in higher plants. Trends Plant Sci 12:368–375. https://doi.org/10.1016/j.tplants.2007.06.007
Germanà MA (2011) Gametic embryogenesis and haploid technology as valuable support to plant breeding. Plant Cell Rep 30:839–857. https://doi.org/10.1007/s00299-011-1061-7 (PubMed: 21431908)
Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6:477–487. https://doi.org/10.1038/nrg1614
Gilles LM, Martinant JP, Rogowsky PM, Widiez T (2017) Haploid induction in plants. Curr Biol 27:R1095–R1097. https://doi.org/10.1016/j.cub.2017.07.055
Gillies CB (1974) The nature and extent of synaptonemal complex formation in haploid barley. Chromosoma 48:441–453. https://doi.org/10.1007/BF00290998
Gong Z, Liu X, Tang D, Yu H, Yi C, Cheng Z et al (2011) Non-homologous chromosome pairing and crossover formation in haploid rice meiosis. Chromosoma 120:47–60. https://doi.org/10.1007/s00412-010-0288-3
Grandont L, Cuñado N, Coriton O, Huteau V, Eber F, Chèvre AM et al (2014) Homoeologous chromosome sorting and progression of meiotic recombination in Brassica napus : ploidy does matter! Plant Cell 26:1448–1463. https://doi.org/10.1105/tpc.114.122788
Guha S, Maheshwari SC (1964) In vitro production of embryos from anthers of Datura. Nature 204:497. https://doi.org/10.1038/204497a0
Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FC (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500. https://doi.org/10.1101/gad.354705
Jacobowitz JR, Doyle WC, Weng JK (2019) PRX9 and PRX40 are extensin peroxidases essential for maintaining tapetum and microspore cell wall integrity during Arabidopsis anther development. Plant Cell 31:848–861. https://doi.org/10.1105/tpc.18.00907
Jacquier N, Gilles LM, Pyott DE, Martinant JP, Widiez T (2020) Puzzling out plant reproduction by haploid induction for innovations in plant breeding. Nature Plants 6:610–619. https://doi.org/10.1038/s41477-020-0664-9
Li J, Zhang J, Li H, Niu H, Xu Q, Jiao Z et al (2019) The major factors causing the microspore abortion of genic male sterile mutant nwms1 in wheat (Triticum aestivum L.). IJMS 20:6252. https://doi.org/10.3390/ijms20246252
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Loidl J, Nairz K, Klein F (1991) Meiotic chromosome synapsis in a haploid yeast. Chromosoma 100:221–228. https://doi.org/10.1007/BF00344155
Longhese MP, Bonetti D, Guerini I, Manfrini N, Clerici M (2009) DNA double-strand breaks in meiosis: checking their formation, processing and repair. DNA Repair 8:1127–1138. https://doi.org/10.1016/j.dnarep.2009.04.005
Martinez M, Cuadrado C, Laurie DA, Romero C (2005) Synaptic behaviour of hexaploid wheat haploids with different effectiveness of the diploidizing mechanism. Cytogenet Genome Res 109:210–214. https://doi.org/10.1159/000082402
Miller MP, Amon A, Unal E (2013) Meiosis I: when chromosomes undergo extreme makeover. Curr Opin Cell Biol 25:687–696. https://doi.org/10.1016/j.ceb.2013.07.009
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628. https://doi.org/10.1038/nmeth.1226
Nicolas SD, Le Mignon G, Eber F, Coriton O, Monod H, Clouet V et al (2007) Homeologous recombination plays a major role in chromosome rearrangements that occur during meiosis of Brassica napus haploids. Genetics 175:487–503. https://doi.org/10.1534/genetics.106.062968
Nicolas SD, Leflon M, Liu Z, Eber F, Chelysheva L, Coriton O et al (2008) Chromosome “speed dating” during meiosis of polyploid Brassica hybrids and haploids. Cytogenet Genome Res 120:331–338. https://doi.org/10.1159/000121082
Peterson R, Slovin JP, Chen C (2010) A simplified method for differential staining of aborted and non-aborted pollen grains. Int J Plant Biol 1:e13. https://doi.org/10.4081/pb.2010.e13
Pradillo M, Varas J, Oliver C, Santos JL (2014) On the role of AtDMC1, AtRAD51 and its paralogs during Arabidopsis meiosis. Front Plant Sci 5:23. https://doi.org/10.3389/fpls.2014.00023
Sadasivaiah R, Kasha K (1971) Meiosis in haploid barley—an interpretation of non-homologous chromosome associations. Chromosoma 263:247–263. https://doi.org/10.1007/BF00326277
Seeliger K, Dukowic-Schulze S, Wurz-Wildersinn R, Pacher M, Puchta H (2012) BRCA2 is a mediator of RAD51- and DMC1-facilitated homologous recombination in Arabidopsis thaliana. New Phytol 193:364–375. https://doi.org/10.1111/j.1469-8137.2011.03947.x
Sen SK (1970) Synaptonemal complexes in haploid Petunia and Antirrhinum sp. Sci Nature 57:550. https://doi.org/10.1007/BF00625339
Wang Y, Copenhaver GP (2018) Meiotic recombination: mixing it up in plants. Annu Rev Plant biol 69: 13.1–13.33. https://doi.org/10.1146/annurev-arplant-042817-040431
Wang X, Wang H, Wang J, Sun R, Wu J, Liu S et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039. https://doi.org/10.1038/ng.919
Xin Q, Shen Y, Li X, Lu W, Wang X, Han X et al (2016) MS5 mediates early meiotic progression and its natural variants may have applications for hybrid production in Brassica napus. Plant Cell 28:1263–1278. https://doi.org/10.1105/tpc.15.01018
Xu N, Gao XQ, Zhao XY, Zhu DZ, Zhou LZ, Zhang XS (2011) Arabidopsis AtVPS15 is essential for pollen development and germination through modulating phosphatidylinositol 3-phosphate formation. Plant Mol Biol 77:251–260. https://doi.org/10.1007/s11103-011-9806-9
Yang Y, Wei F, Braynen J, Wei X, Tian B, Shi G et al (2019) Cytological and proteomic analyses of floral buds reveal an altered atlas of meiosis in autopolyploid Brassica rapa. Cell Biosci 9:49. https://doi.org/10.1186/s13578-019-0313-z
Yang Y, Yan G, Li Z, Yuan J, Wei X, Wei F et al (2020) Cytological atlas at meiosis reveals insights into pollen fertility in synthetic Brassica allotriploids between allotetraploid B. carinata and diploid B. rapa. Plant Physiol Bioch 148:237–245. https://doi.org/10.1016/j.plaphy.2020.01.003
Acknowledgements
This work was financially supported by the Program for Science & Technology Innovation Talents in Universities of Henan Province (No.19HASTIT014), Henan Provincial Science Foundation of China (No. 202300410366) and Youth Innovation Project of Key discipline of Zhengzhou University (No. XKZDQN202002).
Author information
Authors and Affiliations
Contributions
FW and BT conceived and instructed the study, GC and GS participated in the experiments, XW and XZ bred the plant materials, JY performed the experiments and data analysis, JY and YY wrote the manuscript, XS and ZH assisted with materials identification, JB assisted with analysis of bioinformatics. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
No human or animal participants were involved in this research.
Additional information
Communicated by Jinghua Yang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yuan, J., Shi, G., Yang, Y. et al. Non-homologous chromosome pairing during meiosis in haploid Brassica rapa. Plant Cell Rep 40, 2421–2434 (2021). https://doi.org/10.1007/s00299-021-02786-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-021-02786-2