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Allelic variations of ClACO gene improve nitrogen uptake via ethylene-mediated root architecture in watermelon

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Abstract

Key message

The ClACO gene encoding 1-aminocyclopropane-1-carboxylate oxidase enabled highly efficient 15N uptake in watermelon.

Abstract

Nitrogen is one of the most essential nutrient elements that play a pivotal role in regulating plant growth and development for crop productivity. Elucidating the genetic basis of high nitrogen uptake is the key to improve nitrogen use efficiency for sustainable agricultural productivity. Whereas previous researches on nitrogen absorption process are mainly focused on a few model plants or crops. To date, the causal genes that determine the efficient nitrogen uptake of watermelon have not been mapped and remains largely unknown. Here, we fine-mapped the 1-aminocyclopropane-1-carboxylate oxidase (ClACO) gene associated with nitrogen uptake efficiency in watermelon via bulked segregant analysis (BSA). The variations in the ClACO gene led to the changes of gene expression levels between two watermelon accessions with different nitrogen uptake efficiencies. Intriguingly, in terms of the transcript abundance of ClACO, it was concomitant with significant differences in ethylene evolutions in roots and root architectures between the two accessions and among the different genotypic offsprings of the recombinant BC2F1(ZJU132)-18. These findings suggest that ethylene as a negative regulator altered nitrogen uptake efficiency in watermelon by controlling root development. In conclusion, our current study will provide valuable target gene for precise breeding of ‘green’ watermelon varieties with high-nitrogen uptake efficiencies.

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Data availability

The RNA-seq data have been deposited in NCBI Bioproject PRJNA960910. Other data generated in this study are included in this article and its supplementary information files.

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Acknowledgements

We thank Novogene for providing technical support of sequencing and Dr. **chang Zhang from Environment and Resources Experimental Teaching Center, Zhejiang University for the assistance of 15N content measurement.

Funding

This work was supported by Special Support Plan for high-level talents of Zhejiang Province (2021R51007), the Key Research Project of Ningbo Municipal Government (2021Z057) and the Earmarked Fund for China Agriculture Research System (CARS-25-17).

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Authors and Affiliations

  1. Laboratory of Germplasm Innovation and Molecular Breeding, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, China

    Kejia Zhang, Wei Gao, Yimei Zhou, Haoshun Zhao, Yuelin **a, Mengyi Zhang, **aolong Lyu, Zhongyuan Hu, **ghua Yang & Mingfang Zhang

  2. Hainan Institute of Zhejiang University, Yazhou District, Sanya, China

    Zhongyuan Hu, **ghua Yang & Mingfang Zhang

  3. Ningbo Weimeng Seed Company, Ningbo, China

    Yongming Bo

  4. Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Hangzhou, China

    Zhongyuan Hu, **ghua Yang & Mingfang Zhang

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  1. Kejia Zhang
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Contributions

MZ and KZ designed the project. KZ conducted most of the experiments; WG, YZ, HZ, YX and MZ performed some of the field work and measured the phenotypes. ZH, JY and YB performed some data analysis; KZ wrote the manuscript, MZ and XL revised it.

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Correspondence to Mingfang Zhang.

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Communicated by Yiqun Weng.

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122_2023_4448_MOESM1_ESM.docx

Fig. S1 The shoot dry weight and root dry weight of ZJU045, ZJU132 and reciprocal crossings of F1 hybrids. Fig. S2 The Manhattan plots on chromosome 1 and chromosome 4. Fig. S3 Fine map** of the candidate gene for 15N uptake efficiency. Fig. S4 Differential gene expression value of selected genes obtained by RNA-seq and qRT-PCR in roots and leaves of watermelon seedlings grown under hydroponic conditions for two weeks. Fig. S5 Transcriptome analysis of ZJU045 and ZJU132 seedlings in roots and leaves. Fig. S6 Cluster heatmap of 22 genes in the candidate region. Fig. S7 Genoty** analysis of the SNP (M16) in the promoter of ClACO among F2 population (DOCX 1362 kb)

122_2023_4448_MOESM2_ESM.xlsx

Table S1 15N accumulation per unit time among F2 individuals. Table S2 The sequence data summary of BSA project for each pool. Table S3 Number of SNPs and Indels from two parents and their F2 bulks in watermelon. Table S4 The QTL results of 15N uptake efficiency on 99% confidence intervals using ∆All index algorithms. Table S5 The QTL results of 15N uptake efficiency on 99% confidence intervals analyzed by G’ value algorithms. Table S6 The variations between ZJU045 and ZJU132 in candidate regions of chromosome 1 and chromosome 4. Table S7 The list of KASP markers used in this study. Table S8 The genotypes of some lines selected in the F2 population. Table S9 Gene information in candidate region. Table S10 The sequence data summary of transcriptome project for each sample. Table S11 Primer information used for PCR and cloning used in this study (XLSX 62 kb)

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Zhang, K., Gao, W., Zhou, Y. et al. Allelic variations of ClACO gene improve nitrogen uptake via ethylene-mediated root architecture in watermelon. Theor Appl Genet 136, 199 (2023). https://doi.org/10.1007/s00122-023-04448-1

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