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Cytological and transcriptomic analyses provide insights into the pollen fertility of synthetic allodiploid Brassica juncea hybrids

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Abstract

Key message

Imbalanced chromosomes and cell cycle arrest, along with down-regulated genes in DNA damage repair and sperm cell differentiation, caused pollen abortion in synthetic allodiploid Brassica juncea hybrids.

Abstract

Interspecific hybridization is considered to be a major pathway for species formation and evolution in angiosperms, but the occurrence of pollen abortion in the hybrids is common, prompting us to recheck male gamete development in allodiploid hybrids after the initial combination of different genomes. Here, we investigated the several key meiotic and mitotic events during pollen development using the newly synthesised allodiploid B. juncea hybrids (AB, 2n = 2× = 18) as a model system. Our results demonstrated the partial synapsis and pairing of non-homologous chromosomes concurrent with chaotic spindle assembly, affected chromosome assortment and distribution during meiosis, which finally caused difference in genetic constitution amongst the final tetrads. The mitotic cell cycle arrest during microspore development resulted in the production of anucleate pollen cells. Transcription analysis showed that sets of key genes regulating cyclin (CYCA1;2 and CYCA2;3), DNA damage repair (DMC1, NBS1 and MMD1), and ubiquitin–proteasome pathway (SINAT4 and UBC) were largely downregulated at the early pollen meiosis stages, and those genes involved in sperm cell differentiation (DUO1, PIRL1, PIRL9 and LBD27) and pollen wall synthesis (PME48, VGDH11 and COBL10) were mostly repressed at the late pollen mitosis stages in the synthetic allodiploid B. juncea hybrids (AB). In conclusion, this study elucidated the related mechanisms affecting pollen fertility during male gametophyte development at the cytological and transcriptomic levels in the synthetic allodiploid B. juncea hybrids.

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Data availability

All morphological, cytological and transcriptomic analysis data are included in the manuscript materials. The original transcriptome sequencing data have been uploaded to GEO database, numbered as GSE193368.

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Funding

This work was financially supported by Henan Provincial Natural Science Foundation (No.202300410366), the Project of Henan Provincial Science & Technology (No. 232102111110, No.232102111114) and the Fostering Project for Basic Research of Zhengzhou University (No. JC21310015).

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  1. Boyang Wang and Niannian Liang have contributed equally to the work.

Authors and Affiliations

  1. Henan International Joint Laboratory of Crop Gene Resource and Improvements, School of Agricultural Sciences, Zhengzhou University, Zhengzhou, 450001, China

    Boyang Wang, Niannian Liang, Xiaohan Shen, Zhengqing Xie, Luyue Zhang, Baoming Tian, Jialin Guo & Fang Wei

  2. Institute of Horticulture, Henan Academy of Agricultural Sciences, Graduate T&R Base of Zhengzhou University, Zhengzhou, 450002, China

    Boyang Wang, Niannian Liang, Yuxiang Yuan, Xiaowei Zhang & Xiaochun Wei

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  1. Boyang Wang
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Contributions

FW and XW provided the materials used in the experiment and directed the entire experiment process and the revision of the manuscript; BW and NL performed the experiments and was a major contributor to the manuscript. BW and XS performed the experiments; NL and ZX analysis the data; BT, YY, LZ, JG, XZ and WC prepared the Figures. All authors read and approved the final manuscript.

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Correspondence to Fang Wei or Xiaochun Wei.

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Wang, B., Liang, N., Shen, X. et al. Cytological and transcriptomic analyses provide insights into the pollen fertility of synthetic allodiploid Brassica juncea hybrids. Plant Cell Rep 43, 23 (2024). https://doi.org/10.1007/s00299-023-03089-4

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