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A recessive LRR-RLK gene causes hybrid breakdown in cotton

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Abstract

Key message

An LRR-RLK gene causing interspecific hybrid breakdown between Gossypium. anomalum and G. hirsutum was identified by deploying a map-based cloning strategy.

Abstract

The self-destructing symptoms of hybrid incompatibility in most cases are attributed to autoimmunity. The cloning of genes responsible for hybrid incompatibility in cotton is helpful to clarify the mechanisms underlying hybrid incompatibility and can break the barriers in distant hybridization. In this study, a temperature-dependent lethality was identified in CSSL11-9 (chromosome segment substitution line) with Gossypium anomalum chromosome segment on chromosome A11. Transcriptome analysis showed the differentially expressed genes related to autoimmune responses were highly enriched, suggesting that expression of CSSL11-9 plant lethal gene activated autoimmunity in the absence of any pathogen or external stimulus, inducing programmed cell death (PCD) and causing a lethal phenotype. The lethal phenotype was controlled by a pair of recessive genes and then fine mapped between JAAS3191-JAAS3050 interval, which covered 63.87 kb in G. hirsutum genome and 98.66 kb in G. anomalum. We demonstrated that an LRR-RLK gene designated as hybrid breakdown 1 (GoanoHBD1) was the causal gene underlying this locus for interspecific hybrid incompatibility between G. anomalum and G. hirsutum. Silencing this LRR-RLK gene could restore CSSL11-9 plants from a lethal to a normal phenotype. Our findings provide new insights into reproductive isolation and may benefit cotton breeding.

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Data availability

All data used in the current study are included in this published article or are available from the corresponding author on reasonable request.

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Funding

This work was supported by grants from the National Natural Science Foundation of China (32171986), the Jiangsu Provincial Key Research and Development Program (BE2022364), Jiangsu Collaborative Innovation Center for Modern Crop Production.

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Author notes

  1. Peng Xu and Jianwen Xu have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Cotton and Rapeseed (Nanjing), Ministry of Agriculture and Rural Affairs, The Institute of Industrial Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China

    Peng Xu, Jianwen Xu, Qi Guo, Zhenzhen Xu, Wei Ji, Huan Yu, Jihong Cai, Liang Zhao, Jun Zhao, Jianguang Liu, Xianglong Chen & Xinlian Shen

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  1. Peng Xu
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  2. Jianwen Xu
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  3. Qi Guo
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Contributions

Experiments were designed by XS. Experiments were performed by PX, JX, QG, ZX, JC, WJ, HY, LZ, JZ, JL, and XC. PX drafted the manuscript and XS revised the manuscript. All authors read and approved the final manuscript.

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Correspondence to Xinlian Shen.

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Communicated by Tianzhen Zhang.

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Supplementary Information

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Supplementary file1 (XLSX 12 KB)

122_2023_4427_MOESM2_ESM.tif

Supplementary file2 DAB staining of lethal plants (CSSL11-9) and normal plants (Su8289). (a), (b), (c), (d) DAB staining of Su8289 after 30 °C treatment for 0, 1, 3and 5 days (e), (f), (g), (h) DAB staining of CSSL11-9 after 30 °C treatment for 0, 1, 3 and 5 days (TIF 9161 KB)

Supplementary file3 Structure variations of GoanoHBD1 and GhHBD1 (TIF 29813 KB)

Supplementary file4 Amino acid alignment of GoanoHBD1 and GhHBD1 (TIF 15567 KB)

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Xu, P., Xu, J., Guo, Q. et al. A recessive LRR-RLK gene causes hybrid breakdown in cotton. Theor Appl Genet 136, 189 (2023). https://doi.org/10.1007/s00122-023-04427-6

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