Heterometric expression of an LBD gene via LBD-TCP assembly regulates floral organ size and fruit weight in Physalis

Abstract

Plant LATERAL ORGAN BOUNDARIES DOMAIN (LBD) family is crucial for defining organ boundaries and participates in various developmental processes, but its role in fruit weight has rarely been elucidated. Here, we characterized an LBD gene, Physalis organ size 3 (POS3), in Physalis floridana, designated as PfPOS3. This gene exhibited high expression levels in floral meristems, carpels, and developing seeds and fruits when compared to Solanum pimpinellifolium and Solanum lycopersicum. The floral organ size, seed weight, and mature fruit weight were significantly reduced in PfPOS3 knockdown and knockout plants. Consistent with overexpression analyses, PfPOS3 promoted cell size and inhibited cell division during berry development. Moreover, overexpression of PfPOS3 and SlPOS3 shared identical phenotypic variation in transgenic Physalis plants. Both PfPOS3 and SlPOS3 interacted with Teosinte branched1/Cycloidea/Proliferating cell factor 15 (TCP15) and TCP18, and the POS3-TCP modules directly regulated the expression of Cyclin D1;1 (CYCD1;1) and CYCB1;1. Overall, POS3 may have the capability to orchestrate cell number and cell size, thus regulating fruit weight variation within Solanaceae. However, a significant reduction in the expression of SlPOS3 may result in a pronounced weakening or complete loss of this function within Solanum. Our findings shed new light on the reproductive organ size control, the developmental evolution of fruit morphology, and the breeding of Physalis crops.

Acknowledgments

We appreciate Drs. Yan Wang and Xiuping Xu, respectively, for their technical assistances in plant cultivation and SEM. The assistances of Bin Yong in phylogenetic and syntenic analyses, Meifang Luo in mRNA in situ hybridizations, and Wei Gou, Jun Li, and Qianqian Liu in VIGS analyses are sincerely acknowledged. This work was supported by the grants from the National Natural Science Foundation of China (32221001, 31930007, and 31525003) and by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB27010106).

Author contributions

C.Y.H. designed the work. J.L. initiated the work. Q.R.L. succeeded to perform experiments. L.F.W. generated pfpos3 plants and involved in phenotypic analyses. J.L. generated RNAi transgenic plants of PfPOS3 and completed phenotypic analyses. Q.R.L. generated overexpression transgenic plants and involved in phenotypic analyses. L.F.W. and Q.H.C. completed organ size and cell variation during fruit development in all transgenic plants. P.C.G. involved in protoplast transformation and transient expression. L.W. involved in in situ hybridization analyses. N.X. participated in VIGS analyses. Q.R.L., L.F.W., and C.Y.H. analyzed the data, and wrote the manuscript. C.Y.H., Q.R.L., L.F.W., and Q.H.C. revised the manuscript. C.Y.H. finalized the manuscript. All authors have read and approved the manuscript.

Data availability

All data are available in the manuscript or the Supplementary data. All related sequences reported in this work have been deposited in the NCBI GenBank under the accession numbers of OQ248608-OQ248622 and OQ248636-OQ248641.

Conflict of interest statement

The authors declare no conflict of interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

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