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microRNA regulation of fruit growth

Nature Plants volume 1, Article number: 15036 (2015) Cite this article

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Abstract

Growth is a major factor in plant organ morphogenesis and is influenced by exogenous and endogenous signals including hormones. Although recent studies have identified regulatory pathways for the control of growth during vegetative development, there is little mechanistic understanding of how growth is controlled during the reproductive phase. Using Arabidopsis fruit morphogenesis as a platform for our studies, we show that the microRNA miR172 is critical for fruit growth, as the growth of fruit is blocked when miR172 activity is compromised. Furthermore, our data are consistent with the FRUITFULL (FUL) MADS-domain protein and Auxin Response Factors (ARFs) directly activating the expression of a miR172-encoding gene to promote fruit valve growth. We have also revealed that MADS-domain (such as FUL) and ARF proteins directly associate in planta. This study defines a novel and conserved microRNA-dependent regulatory module integrating developmental and hormone signalling pathways in the control of plant growth.

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Figure 1: Arabidopsis fruit anatomy, fruit developmental stages.
Figure 2: miR172 function is required for normal fruit growth.
Figure 3: FUL directly activates MIR172C and both belong to the same regulatory pathway controlling fruit valve growth.
Figure 4: ARF8 and ARF6 act upstream of MIR172C to regulate its expression in fruit valves.
Figure 5: FUL associates with ARF6 and ARF8 to regulate MIR172C for proper fruit valve growth.
Figure 6: Model for the regulation of fruit growth and morphogenesis by the miR172-dependent regulatory module (MADS/ARF–miR172–AP2).

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Acknowledgements

The authors would like to thank José L. Pruneda-Paz, Pablo Jenik, Brian C. Crawford Antonio Vera and Antonio Martínez-Laborda for critical reading of the manuscript and helpful discussions and suggestions; members of the Yanofsky and Estelle laboratories for helpful discussions; Xuemei Chen, Javier Paz-Ares, Detlef Weigel, John L. Bowman, Markus Schmid, Dolf Weijers and Richard Immink for sharing published materials; Nigel Crawford's laboratory (UCSD) for the use of their fluorescence microscope; Peizhu Guan (UCSD) for technical advice with the Transient expression assays in Nicotiana and A. Amorós and V. López for technical help with SEM work (UA, Spain). We also thank Aria Davani, Jessica Huang, Aidan Estelle, Agustín Almoril and Tammy Tran for technical assistance, and Elena Monfort for help in generating construct precursors. Lindsay J. Bailey, Quynh-Anh Mai, Scott L. Wu and Cindy T. Hon were BSc/MS students from the BISP 199 UCSD programme under J. J. Ripoll and M. F. Yanofsky supervision. This work was funded by the National Science Foundation (IOS-1121055 to M.F.Y), the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (GBMF 3038 to M.E.), and the Paul D. Saltman Endowed Chair in Science Education (to M.F.Y).

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Authors and Affiliations

  1. Division of Biological Sciences, Section of Cell and Developmental Biology, University of California at San Diego, La Jolla, 92093-0116, California, USA

    Juan José Ripoll, Lindsay J. Bailey, Quynh-Anh Mai, Scott L. Wu, Cindy T. Hon, Elisabeth J. Chapman, Gary S. Ditta, Mark Estelle & Martin F. Yanofsky

  2. Howard Hughes Medical Institute, University of California San Diego, La Jolla, 92093, California, USA

    Mark Estelle

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Contributions

J.J.R. and M.F.Y. were responsible for the conception, planning and organization of the experimental time line. J.J.R., L.J.B, Q.A.M, S.L.W., C.T.H., E.J.C and G.S.D. carried out experiments. J.J.R., M.E. and M.F.Y. supervised the development of the experimental plan. J.J.R. and M.F.Y. directly supervised the experimental work done by L.J.B., Q.A.M., S.L.W. and C.T.H. J.J.R., M.E. and M.F.Y. discussed the resulting data. The manuscript was written by J.J.R. and M.F.Y.

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Correspondence to Martin F. Yanofsky.

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José Ripoll, J., Bailey, L., Mai, QA. et al. microRNA regulation of fruit growth. Nature Plants 1, 15036 (2015). https://doi.org/10.1038/nplants.2015.36

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