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Downregulation of the expression of subgenomic chromosome A7 genes promotes plant height in resynthesized allopolyploid Brassica napus

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Abstract

Key message

Homoeolog expression bias and the gene dosage effect induce downregulation of genes on chromosome A7, causing a significant increase in the plant height of resynthesized allopolyploid Brassica napus.

Abstract

Gene expression levels in allopolyploid plants are not equivalent to the simple average of the expression levels in the parents and are associated with several non-additive expression phenomena, including homoeolog expression bias. However, hardly any information is available on the effect of homoeolog expression bias on traits. Here, we studied the effects of gene expression-related characteristics on agronomic traits using six isogenic resynthesized Brassica napus lines across the first ten generations. We found a group of genes located on chromosome A7 whose expression levels were significantly negatively correlated with plant height. They were expressed at significantly lower levels than their homoeologous genes, owing to allopolyploidy rather than inheritance from parents. Homoeolog expression bias resulted in resynthesized allopolyploids with a plant height similar to their female Brassica oleracea parent, but significantly higher than that of the male Brassica rapa parent. Notably, aneuploid lines carrying monosomic and trisomic chromosome A7 had the highest and lowest plant heights, respectively, due to changes in the expression bias of homoeologous genes because of alterations in the gene dosage. These findings suggest that the downregulation of the expression of homoeologous genes on a single chromosome can result in the partial improvement of traits to a significant extent in the nascent allopolyploid B. napus.

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Data availability

Raw data from this project are available on the NCBI Sequence Read Archive Project PRJNA577908.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant number 32070556 and 31871239), US National Science Foundation (2029959), Inner Mongolia Key Technology Research Plan (2020GG0080), and Inner Mongolia Natural Science Foundation (2020ZD09). The work was carried out at IMHPC (Inner Mongolia High Performance Computing Public Service Platform), and the calculations were performed on The Light of Huhhot. We appreciate the linguistic assistance provided by TopEdit (www.topeditsci.com) during the preparation of this manuscript.

Funding

Funding was provided by Natural Science Foundation of Inner Mongolia, (Grant Number: 2020ZD09).

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  1. Kanglu Zhao, Jing Dong, and Junxiong Xu have equally contributed.

Authors and Affiliations

  1. Key Laboratory of Herbage and Endemic Crop Biology, Ministry of Education, School of Life Sciences, Inner Mongolia University, Hohhot, 010070, China

    Kanglu Zhao, Jing Dong, Junxiong Xu, Yanbo Bai, Chunshen Long, Lei Wu & Zhiyong Xiong

  2. Institute of Ulanqab Agricultural and Forestry Sciences, Ulanqab, 012000, Inner Mongolia, China

    Yuhe Yin, Tuanrong Lin, Longqiu Fan & Yufeng Wang

  3. Department of Horticulture, Michigan State University, East Lansing, MI, 48824, USA

    Patrick P. Edger

  4. Genetics and Genome Sciences Program, Michigan State University, East Lansing, MI, 48824, USA

    Patrick P. Edger

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Contributions

KZ and ZX designed the research. KZ, YB, YY, CL, LW, TL, LF, and YW performed data analysis. JD and JX completed the cytogenetic experiment. KZ and JX wrote the manuscript. PPE and ZX finalized the manuscript.

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Correspondence to Patrick P. Edger or Zhiyong Xiong.

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122_2023_4510_MOESM1_ESM.tif

Supplementary file1 (TIF 44073 KB) Fig. S1 Cytogenetic karyotyping of EL100S10, EL200S5, and EL300S10. (a-c) For karyotype analysis, the A chromosomes are shown in lanes 1 and 2, and the C chromosomes are shown in lanes 3 and 4. The first round of FISH included 45S rDNA (white), 5S rDNA (yellow), BAC clone KBrB072L17 (green), and KBrH092N24 (red) probes, and the hybridization results are shown in lanes 1 and 3. The second round of FISH included CentBr1 (white), CentBr2 (green), and BAC BNIH 123L05 (red) probes containing C genome-specific repeated sequences, and the hybridization results are shown in lanes 2 and 4. (a) EL100S10 is an aneuploid with three A7, and one homoeologous C6 and two homoeologous C7 chromosomes. EL200S5 (b) and EL300S10 (c) are aneuploids with one A7 and two corresponding homoeologous C chromosomes.

122_2023_4510_MOESM2_ESM.tif

Supplementary file2 (TIF 44708 KB) Fig. S2 Cytogenetic karyotyping of EL200S1, EL1100S1, and EL1100S5. (a-c) For karyotype analysis, the A chromosomes are shown in lanes 1 and 2, and the C chromosomes are shown in lanes 3 and 4. The first round of FISH included 45S rDNA (white), 5S rDNA (yellow), BAC clone KBrB072L17 (green), and KBrH092N24 (red) probes, and the hybridization results are shown in lanes 1 and 3. The second round of FISH included CentBr1 (white), CentBr2 (green), and BAC BNIH 123L05 (red) probes containing C genome-specific repeated sequences, and the hybridization results are shown in lanes 2 and 4. (a) EL200S1 is an euploid with two normal A7 and two corresponding homoeologous C chromosomes. EL1100S1 (b) and EL1100S5 (c) are aneuploids with two normal A7 and two corresponding homoeologous C chromosomes.

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Zhao, K., Dong, J., Xu, J. et al. Downregulation of the expression of subgenomic chromosome A7 genes promotes plant height in resynthesized allopolyploid Brassica napus. Theor Appl Genet 137, 11 (2024). https://doi.org/10.1007/s00122-023-04510-y

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