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Multiple and integrated functions of floral C-class MADS-box genes in flower and fruit development of Physalis floridana

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Abstract

Key message

This work reveals potentially multiple and integrated roles in flower and fruit development of floral C-class MADS-box genes in Physalis.

Abstract

The Physalis fruit features a morphological novelty, the Chinese lantern. Floral C-class MADS-domain AGAMOUS-like (AG-like) proteins can interact with the identified regulators of this novel structure. However, the developmental role of the floral C-class genes is unknown in Physalis. Here, we characterized two AG-like genes from Physalis floridana, designated PFAG1 and PFAG2. The two paralogous genes shared around 61.0% of sequence identity and had similar expression domains, with different expression levels in the floral and berry development. However, the genes had distinct expression patterns in leaf and calyx development. Protein–protein interaction analyses revealed that PFAG1 and PFAG2 could commonly or specifically dimerize with certain floral MADS-domain proteins as well as non-MADS-domain proteins involved in various floral developmental processes. Gene downregulation analyses demonstrated that PFAG1 may repress PFAG2, but PFAG2 did not affect PFAG1. Downregulating PFAG1 led to incomplete floral homeotic variation in the stamens and carpels, and alteration of petal coloration pattern, while downregulating PFAG2 did not result in any floral homeotic variation. PFAG1 affected pollen maturation, while PFAG2 affected female fertility. However, simultaneously downregulating PFAG1 and PFAG2 caused loss of the complete C-function, indicating that the two PFAG genes interact to determine the identity and functionality of androecia and gynoecia organs. Their potential roles in regulating fruit size and the Chinese lantern are also discussed. Our results reveal functional divergence of floral C-class MADS-box genes in Physalis, demonstrating that they may play multiple and integrated roles in flower and fruit development.

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Data availability

All data are available in the manuscript or the supplementary materials. The sequences reported in this work have been deposited in the NCBI GenBank under the accession numbers: KC794937 (PFAG1), MZ147807 (PFAG2) and MZ147808 (PFMBP3).

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Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (31525003) and the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB27010106) to CYH, the Youth Innovation Promotion Association CAS (2019081) and the National Natural Science Foundation of China (31500190) to PCG.

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  1. Jing Zhao and Pichang Gong contributed equally to this work.

Authors and Affiliations

  1. Life Science College, Northwest Normal University, Lanzhou, 730070, Gansu, China

    Jing Zhao

  2. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Jing Zhao, Pichang Gong, Hongyan Liu, Mingshu Zhang & Chaoying He

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Jing Zhao, Hongyan Liu, Mingshu Zhang & Chaoying He

  4. The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, China

    Chaoying He

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Contributions

CYH designed and conceived the research work. JZ performed nearly all the experiments and obtained the results. PCG prepared plant materials used for cDNA library construction of P. floridana. HYL, MSZ and PCG performed the library screening and PPI networks analyses. JZ, PCG and CYH analyzed the data. CYH, PCG and JZ drafted the manuscript. All authors read and approved the manuscript.

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Correspondence to Chaoying He.

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Zhao, J., Gong, P., Liu, H. et al. Multiple and integrated functions of floral C-class MADS-box genes in flower and fruit development of Physalis floridana. Plant Mol Biol 107, 101–116 (2021). https://doi.org/10.1007/s11103-021-01182-4

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