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Divergences of MPF2-like MADS-domain proteins have an association with the evolution of the inflated calyx syndrome within Solanaceae

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Abstract

The inflated calyx syndrome (ICS) is a post-floral novelty within Solanaceae. Previous work has shown that MPF2-like MADS-box genes have been recruited for the development and evolution of ICS through heterotopic expression from vegetative to floral organs. ICS seems to be a plesiomorphic trait in Physaleae, but it has been secondarily lost in some lineages during evolution. We hypothesized that molecular and functional divergences of MPF2-like proteins might play a role in the loss of ICS. In this study we analyzed the phylogeny, selection and various functions of MPF2-like proteins with respect to the evolution of ICS. Directional selection of MPF2-like orthologs toward evolution of ICS was detected. While auto-activation capacity between proteins varies in yeast, MPF2-like interaction with floral MADS-domain proteins is robustly detected, hence substantiating their integration into the floral developmental programs. Dimerization with A- (MPF3) and E-function (PFSEP1/3) proteins seems to be essential for ICS development within Solanaceae. Moreover, the occurrence of the enlarged sepals, reminiscent of ICS, and MPF2-like interactions with these specific partners were observed in transgenic Arabidopsis. The interaction spectrum relevant to ICS seems to be plesiomorphic, reinforcing the plesiomorphy of this trait. The inability of some MPF2-like to interact with either the A-function or any of the E-function partners characterized is correlated with the loss of ICS in the lineages that showed a MPF2-like expression in the calyx. Our findings suggest that, after recruitment of MPF2-like genes for floral development, diversification in their coding region due to directional selection leads to a modification of the MADS-domain protein interacting spectrum, which might serve as a constraint for the evolution of ICS within Solanaceae.

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Abbreviations

BiFC:

Bimolecular fluorescent complementation

YFP:

Yellow fluorescent protein

ICS:

Inflated calyx syndrome

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Acknowledgments

We thank Dr. T Münster and H Sommer for offering cDNA clones of ZMM19 and INCO, respectively. We thank Dr. T Sang and C–P Stelzer for their valuable suggestions to improve the manuscript. CYH is grateful to Dr. H. Saedler for his support and advice. This work was supported by the National Natural Science Foundation of China (30870175) and the Hundred Talents Project of the Chinese Academy of Sciences to CYH. RMK was supported by a Higher Education Commission, Pakistan, and Deutscher Akademischer Austausch Dienst fellowship, and SR was supported by a fellowship of the Max-Planck-Society.

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  1. Muhammad Ramzan Khan

    Present address: National Agricultural Research Centre, National Institute for Genomics and Advanced Biotechnology, Islamabad, Pakistan

  2. Simone Riss

    Present address: Institute for Limnology of the Austrian Academy of Sciences, Mondseestr. 9, 5310, Mondsee, Austria

Authors and Affiliations

  1. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, **angshan, Bei**g, 100093, China

    Jisi Zhang, Ying Tian, Zhichao Li & Chaoying He

  2. Graduate University, Chinese Academy of Sciences, Yuquan Road 19, Bei**g, 100049, China

    Jisi Zhang & Zhichao Li

  3. Department of Molecular Plant Genetics, Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany

    Muhammad Ramzan Khan & Simone Riss

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  1. Jisi Zhang
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Correspondence to Chaoying He.

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J. Zhang and M.R. Khan equally contributed to this work.

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Zhang, J., Khan, M.R., Tian, Y. et al. Divergences of MPF2-like MADS-domain proteins have an association with the evolution of the inflated calyx syndrome within Solanaceae. Planta 236, 1247–1260 (2012). https://doi.org/10.1007/s00425-012-1684-0

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