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An allelic variant in the ACS7 gene promotes primary root growth in watermelon

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Abstract

Key message

Gene mining in a C. lanatus × C. amarus population revealed one gene, ACS7, linked to primary root elongation in watermelon.

Abstract

Watermelon is a xerophytic crop characterized by a long primary root and robust lateral roots. Therefore, watermelon serves as an excellent model for studying root elongation and development. However, the genetic mechanism underlying the primary root elongation in watermelon remains unknown. Herein, through bulk segregant analysis we identified a genetic locus, qPRL.Chr03, controlling primary root length (PRL) using two different watermelon species (Citrullus lanatus and Citrullus amarus) that differ in their root architecture. Fine mapping revealed that xaa-Pro dipeptidase and 1-aminocyclopropane-1-carboxylate synthase 7 (ACS7) are candidate regulators of the primary root growth. Allelic variation in the delimited region among 193 watermelon accessions indicated that the long-root alleles might only exist in C. amarus. Interestingly, the discrepancy in PRL among the C. amarus accessions was clearly associated with a nonsynonymous single nucleotide polymorphism variant within the ACS7 gene. The ACS7 expression and ethylene levels in the primary root tips suggested that ethylene is a negative regulator of root elongation in watermelon, as supported by the application of 1-aminocyclopropane-1-carboxylate (ACC, the ethylene precursor) or 2-aminoethoxyvinyl glycine (AVG, an ACS inhibitor). To the best of our knowledge, these findings provide the first description of the genetic basis of root elongation in watermelon. The detected markers of the ACS7 gene will facilitate marker-assisted selection for the PRL trait to improve water and nutrient use efficacy in watermelon and beyond.

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Acknowledgements

This work was supported by the National Key Research and Development Plan of China (2019YFD1000300, 2019YFD100190200, 2018YFD0201300), the Natural Science Foundation of Hainan Province (321MS064), the Natural Science Foundation of Zhejiang Province (LY21C150008), Science and technology innovation platform for the watermelon and melon breeding, reproduction, and spreading of Zhejiang Province (2020-KYY-NSFZ-0314), the Earmarked Fund for China Agriculture Research System (CARS-25-17), the Fundamental Research Funds for the Central Universities (2017QNA6016, +226-2022-00100), and the Key Science and Technology Program for Agricultural (Vegetable) New Variety Breeding of Zhejiang Province (2021C02065). We would like to thank Editage (www.editage.com) for English language editing.

Funding

This work was supported by the National Key Research and Development Plan of China (2019YFD1000300, 2019YFD100190200, 2018YFD0201300), the Natural Science Foundation of Hainan Province (321MS064), the Natural Science Foundation of Zhejiang Province (LY21C150008), Science and technology innovation platform for the watermelon and melon breeding, reproduction, and spreading of Zhejiang Province (2020-KYY-NSFZ-0314), the Earmarked Fund for China Agriculture Research System (CARS-25-17), the Fundamental Research Funds for the Central Universities (2017QNA6016, + 226-2022-00100), and the Key Science and Technology Program for Agricultural (Vegetable) New Variety Breeding of Zhejiang Province (2021C02065).

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  1. Laboratory of Germplasm Innovation and Molecular Breeding, Institute of Vegetable Science, Zhejiang University, Hangzhou, Zhejiang, People’s Republic of China

    Ahmed Mahmoud, Haoshun Zhao, Haiyang Yang, Nanqiao Liao, Abid Ali, Guy Kateta Malangisha, Yuyuan Ma, Kejia Zhang, Yimei Zhou, Yuelin Xia, Xiaolong Lyu, Jinghua Yang, Mingfang Zhang & Zhongyuan Hu

  2. Hainan Institute of Zhejiang University, Yazhou District, Sanya, 572025, People’s Republic of China

    Rui Qi, Jinghua Yang, Mingfang Zhang & Zhongyuan Hu

  3. Key Laboratory of Horticultural Plant Growth, Development & Quality Improvement, Ministry of Agriculture, Hangzhou, Zhejiang, People’s Republic of China

    Jinghua Yang, Mingfang Zhang & Zhongyuan Hu

  4. Agriculture Research Center, Horticulture Research Institute, 9 Gmaa St, Giza, 12619, Egypt

    Ahmed Mahmoud

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  1. Ahmed Mahmoud
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Contributions

ZH and MZ conceived and designed the study; AM conducted all experiments and wrote the manuscript; RQ, NQ, AA and GKM participated in results analysis; HZ, HY, YM, KZ, YZ, and YX helped perform parts of experiments; XL and JY participated in research discussion; all authors reviewed the manuscript.

Corresponding authors

Correspondence to Mingfang Zhang or Zhongyuan Hu.

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The authors declare no competing financial interests.

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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Communicated by Amnon Levi.

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Mahmoud, A., Qi, R., Zhao, H. et al. An allelic variant in the ACS7 gene promotes primary root growth in watermelon. Theor Appl Genet 135, 3357–3373 (2022). https://doi.org/10.1007/s00122-022-04173-1

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  • DOI: https://doi.org/10.1007/s00122-022-04173-1

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