Heterotrimeric Gα-subunit regulates flower and fruit development in CLAVATA signaling pathway in cucumber

Abstract

Flowers and fruits are the reproductive organs in plants and play essential roles in natural beauty and the human diet. CLAVATA (CLV) signaling has been well characterized as regulating floral organ development by modulating shoot apical meristem (SAM) size; however, the signaling molecules downstream of the CLV pathway remain largely unknown in crops. Here, we found that functional disruption of CsCLV3 peptide and its receptor CsCLV1 both resulted in flowers with extra organs and stumpy fruits in cucumber. A heterotrimeric G protein α-subunit (CsGPA1) was shown to interact with CsCLV1. Csgpa1 mutant plants derived from gene editing displayed significantly increased floral organ numbers and shorter and wider fruits, a phenotype resembling that of Csclv mutants in cucumber. Moreover, the SAM size was enlarged and the longitudinal cell size of fruit was decreased in Csgpa1 mutants. The expression of the classical stem cell regulator WUSCHEL (WUS) was elevated in the SAM, while the expression of the fruit length stimulator CRABS CLAW (CRC) was reduced in the fruit of Csgpa1 mutants. Therefore, the Gα-subunit CsGPA1 protein interacts with CsCLV1 to inhibit floral organ numbers but promote fruit elongation, via repressing CsWUS expression and activating CsCRC transcription in cucumber. Our findings identified a new player in the CLV signaling pathway during flower and fruit development in dicots, increasing the number of target genes for precise manipulation of fruit shape during crop breeding.

Acknowledgements

This work was supported by grants from the National Key Research and Development Program of China (2022YFD1200502), the National Natural Science Foundation of China (32025033 and 31930097), Hunan High-level Talents Gathering Project-innovative Talents (2021RC5006), Pinduoduo-China Agricultural University Research Fund (PC2023B01002), and the 111 Project (B17043).

Author contributions

X.Z., L.H., and Z.Z. designed the project. L.H. performed the experiments; L.H. and X.Z. wrote the paper; Y.H., C.L., D.T., and D.S. provided assistance in cucumber cultivation management and phenotype analysis; M.L., Z.W., J.C., L.L., S.W., W.S., L.W., C.G., T.W., and J.Z. provided experimental assistance; all the authors revised the manuscript.

Data availability

The datasets have been submitted to the NCBI-SRA database under the BioProject PRJNA1088621.

Conflict of interest

The authors declare no conflict of interest.

Supplementary data

Supplementary data are available at Horticulture Research online.

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