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The branchless gene Clbl in watermelon encoding a TERMINAL FLOWER 1 protein regulates the number of lateral branches

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A SNP mutation in Clbl gene encoding TERMINAL FLOWER 1 protein is responsible for watermelon branchless.

Abstract

Lateral branching is one of the most important traits, which directly determines plant architecture and crop productivity. Commercial watermelon has the characteristics of multiple lateral branches, and it is time-consuming and labor-costing to manually remove the lateral branches in traditional watermelon cultivation. In our present study, a lateral branchless trait was identified in watermelon material WCZ, and genetic analysis revealed that it was controlled by a single recessive gene, which named as Clbl (Citrullus lanatus branchless). A bulked segregant sequencing (BSA-seq) and linkage analysis was conducted to primarily map Clbl on watermelon chromosome 4. Next-generation sequencing-aided marker discovery and a large mapping population consisting of 1406 F2 plants were used to further map Clbl locus into a 9011-bp candidate region, which harbored only one candidate gene Cla018392 encoding a TERMINAL FLOWER 1 protein. Sequence comparison of Cla018392 between two parental lines revealed that there was a SNP detected from C to A in the coding region in the branchless inbred line WCZ, which resulted in a mutation from alanine (GCA) to glutamate (GAA) at the fourth exon. A dCAPS marker was developed from the SNP locus, which was co-segregated with the branchless phenotype in both BC1 and F2 population, and it was further validated in 152 natural watermelon accessions. qRT-PCR and in situ hybridization showed that the expression level of Cla018392 was significantly reduced in the axillary bud and apical bud in branchless line WCZ. Ectopic expression of ClTFL1 in Arabidopsis showed an increased number of lateral branches. The results of this study will be helpful for better understanding the molecular mechanism of lateral branch development in watermelon and for the development of marker-assisted selection (MAS) for new branchless watermelon cultivars.

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Acknowledgements

This research was supported by the National Natural Science Foundation of China (31872133, 31972427, 316721787, 32102389), the Agricultural Science and Technology Innovation Program (CAAS-ASTIP-2021-ZFRI), the Project for Scientific and Technological Activities of Overseas Students of Henan Province, the Zhongyuan Youth Talent Support Program (ZYQR201912161), the Program for Science & Technology Innovation Talents in Universities of Henan Province (21HASTIT038), the China Agriculture Research System (CARS-25-03), the Key Scientific and Technological Project of Henan Province (202102110045) and the Science and Technology Innovation Fund of Henan Agricultural University (KJCX2021A14).

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  1. Junling Dou and Huihui Yang have contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Henan Agricultural University, 63 Nongye Road, Zhengzhou, 450002, China

    Junling Dou, Huihui Yang, Dongling Sun, Sen Yang, Shouru Sun, Huayu Zhu, Dongming Liu, Changsheng Ma & Luming Yang

  2. Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, 450009, China

    Junling Dou, Shengjie Zhao, Xuqiang Lu & Wenge Liu

  3. Henan Key Laboratory of Fruit and Cucurbit Biology, Zhengzhou, 450002, China

    Wenge Liu & Luming Yang

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  1. Junling Dou
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Contributions

J Dou, H Yang and D Sun performed phenotyping in segregating population and gene clone. S Zhao, X Lu, S Sun, C Ma and D Liu analyzed the experimental data. H Yang, S Yang and H Zhu contributed to in situ hybridization and ectopic expression. L Yang and W Liu conceived the research and designed the experiments. J Dou and L Yang wrote the manuscript. All authors reviewed and approved this submission.

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Correspondence to Wenge Liu or Luming Yang.

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Communicated by Hong-Qing Ling.

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122_2021_3952_MOESM1_ESM.jpg

Fig. S1 Validation of Clbl co-segregation dCAPS10 marker in BC1P2 population. Genotyping analysis revealed that 38 normal branching individuals were heterozygous plants (Het), whereas 31 branchless individuals were homozygous recessive plants (Null) (JPG 438 KB)

122_2021_3952_MOESM2_ESM.jpg

Fig. S2 Validation of Clbl co-segregation dCAPS10 marker in 152 natural watermelon accessions. Genotyping analysis revealed that all the 152 normal branching individuals were dominant homozygous plants (JPG 1617 KB)

Fig. S3 The allele diversity analysis of 32 watermelon accessions and branchless material WCZ (JPG 2462 KB)

Fig. S4 Network analysis of AtTFL1 proteins (JPG 629 KB)

122_2021_3952_MOESM5_ESM.jpg

Fig. S5 Conserved motif analysis of Cucurbitaceae TFL1 proteins. Total five distinct motifs were identified; motif 1 and motif 3 were identified encoding PEBP motif which was the typical motif of TFL1 protein family (JPG 3751 KB)

122_2021_3952_MOESM6_ESM.jpg

Fig. S6 The test of ClTFL1/Cltfl1 transcriptional auto-activation. a, b ClTFL1 has transcriptional auto-activation. c, d The mutant Cltfl1 did not have transcriptional auto-activation (JPG 708 KB)

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Dou, J., Yang, H., Sun, D. et al. The branchless gene Clbl in watermelon encoding a TERMINAL FLOWER 1 protein regulates the number of lateral branches. Theor Appl Genet 135, 65–79 (2022). https://doi.org/10.1007/s00122-021-03952-6

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