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Incomplete genome doubling enables to consistently enhance plant growth for maximum biomass production by altering multiple transcript co-expression networks in potato

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Abstract

Key message

Cytochimera potato plants, which mixed with diploid and tetraploid cells, could cause the highest and significantly increased biomass yield than the polyploid and diploid potato plants.

Abstract

Polyploidization is an important approach in crop breeding for agronomic trait improvement, especially for biomass production. Cytochimera contains two or more mixed cells with different levels of ploidy, which is considered a failure in whole genome duplication. Using colchicine treatment with diploid (Dip) potato (Solanum chacoense) plantlets, this study generated tetraploid (Tet) and cytochimera (Cyt) lines, which, respectively, contained complete and partial cells with genome duplication. Compared to the Dip potato, we observed remarkably enhanced plant growth and biomass yields in Tet and Cyt lines. Notably, the Cyt potato straw, which was generated from incomplete genome doubling, was of significantly higher biomass yield than that of the Tet with a distinctively altered cell wall composition. Meanwhile, we observed that one layer of the tetraploid cells (about 30%) in Cyt plants was sufficient to trigger a gene expression pattern similar to that of Tet, suggesting that the biomass dominance of Cyt may be related to the proportion of different ploidy cells. Further genome-wide analyses of co-expression networks indicated that down-regulation (against Dip) of spliceosomal-related transcripts might lead to differential alternative splicing for specifically improved agronomic traits such as plant growth, biomass yield, and lignocellulose composition in Tet and Cyt plants. In addition, this work examined that the genome of Cyt line was relatively stable after years of asexual reproduction. Hence, this study has demonstrated that incomplete genome doubling is a promising strategy to maximize biomass production in potatoes and beyond.

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Data availability

The RNA sequence is available from the National Centre for Biotechnology Information (NCBI) as BioProject ID PRJNA591474.

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Acknowledgements

This work was in part supported by the projects of National Natural Science Foundation of China (32070556, 32060503, 31571721, 31670296), the National 111 Project of Ministry of Education of China (B08032), the Inner Mongolia Science and Technology Project (2020GG0080) and Inner Mongolia Natural Science Foundation (2020ZD09).

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Authors and Affiliations

  1. Key Laboratory of Herbage and Endemic Crop Biotechnology, Ministry of Education, State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock, College of Life Science, Inner Mongolia University, Hohhot, 010021, Inner Mongolia, China

    Kanglu Zhao, Nengzhou Jin, Lei Wu, Zhijun Xu, Jinxuan Wang, Jing Dong & Zhiyong Xiong

  2. Biomass and Bioenergy Research Center, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Meysam Madadi, Youmei Wang, Yanting Wang & Liangcai Peng

  3. Laboratory of Biomass Engineering & Nanomaterial Application in Automobiles, College of Food Science & Chemical Engineering, Hubei University of Arts & Science, Xiangyang, China

    Meysam Madadi, Shang-wen Tang, Yanting Wang & Liangcai Peng

  4. College of Life Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Youmei Wang

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  1. Kanglu Zhao
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Contributions

KZ completed the major experiments of potato polyploidy identification and bioinformatic analysis, and wrote the manuscript; NJ, LW, Zhijun X, JW, and JD participated in the potato polyploidy selection and characterization; MM completed the most potato biomass process experiments; Youmei W, ST, and Yanting W participated in the tissue culture, biomass chemical analysis, and experiment discussion; LP supervised biomass process project and finalized the manuscript, and Zhiyong X designed and supervised the potato polyploidy project.

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Correspondence to Zhiyong Xiong.

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122_2021_3976_MOESM3_ESM.tif

Fig. S1 Identification of cell ploidy in the different organs (root, stem, leaf, and flower) of Dip, Tet-1, and Cyt-1 samples at the flowering stage by 5S rDNA FISH (red signals). Scale bar, 10 µm. (TIF 32961 KB)

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Zhao, K., Jin, N., Madadi, M. et al. Incomplete genome doubling enables to consistently enhance plant growth for maximum biomass production by altering multiple transcript co-expression networks in potato. Theor Appl Genet 135, 461–472 (2022). https://doi.org/10.1007/s00122-021-03976-y

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