Abstract
Within the tomato MADS-box gene family, TOMATO AGAMOUS1 (TAG1) and ARLEQUIN/TOMATO AGAMOUS LIKE1 (hereafter referred to as TAGL1) are, respectively, members of the euAG and PLE lineages of the AGAMOUS clade. They perform crucial functions specifying stamen and carpel development in the flower and controlling late fruit development. To gain insight into the roles of TAG1 and TAGL1 genes and to better understand their functional redundancy and diversification, we characterized single and double RNAi silencing lines of these genes and analyzed expression profiles of regulatory genes involved in reproductive development. Double RNAi lines did show cell abnormalities in stamens and carpels and produced extremely small fruit-like organs displaying some sepaloid features. Expression analyses indicated that TAG1 and TAGL1 act together to repress fourth whorl sepal development, most likely through the MACROCALYX gene. Results also proved that TAG1 and TAGL1 have diversified their functions in fruit development: while TAG1 controls placenta and seed formation, TAGL1 participates in cuticle development and lignin biosynthesis inhibition. It is noteworthy that both TAG1 and double RNAi plants lacked seed development due to abnormalities in pollen formation. This seedless phenotype was not associated with changes in the expression of B-class stamen identity genes Tomato MADS-box 6 and Tomato PISTILLATA observed in silencing lines, suggesting that other regulatory factors should participate in pollen formation. Taken together, results here reported support the idea that both redundant and divergent functions of TAG1 and TAGL1 genes are needed to control tomato reproductive development.
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Acknowledgments
The authors also thank research facilities provided by the Campus de Excelencia Internacional CeiA3. We thank Dr. F. J. Yuste-Lisbona for critical reading of the manuscript.
Funding
This work was supported by the Spanish Ministry of Economy and Competitiveness (Grant Numbers AGL2012-40150-C03-01, AGL2012-40150-C03-02 and AGL2015-64991-C3-1-R); and the European Commission through the JAE-Doc Program of the Spanish National Research Council (CSIC) (Grant Number AGL2012-40150-C03-01 to B.P.).
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E. G. conducted the experiments, assisted in data interpretation and drafted the manuscript. L. C. collaborated in the experimental work. B. P. and V. M. generated transgenic plants and collaborated in genetic analyses. I. L. P. contributed to a critical review of the manuscript. T. A. assisted in data analysis and reviewed the manuscript. R. L. planned the research work, assisted in data interpretation, and edited the manuscript. All authors have read and approved the final manuscript.
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Gimenez, E., Castañeda, L., Pineda, B. et al. TOMATO AGAMOUS1 and ARLEQUIN/TOMATO AGAMOUS-LIKE1 MADS-box genes have redundant and divergent functions required for tomato reproductive development. Plant Mol Biol 91, 513–531 (2016). https://doi.org/10.1007/s11103-016-0485-4
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DOI: https://doi.org/10.1007/s11103-016-0485-4