Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

microRNA regulation of fruit growth

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

Subjects

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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).

Similar content being viewed by others

References

  1. Ferrándiz, C., Pelaz, S. & Yanofsky, M. F. Control of carpel and fruit development in Arabidopsis. Annu. Rev. Biochem. 68, 321–354 (1999).

    Article  PubMed  Google Scholar 

  2. Roeder, A. H. & Yanofsky, M. F. Fruit Development in Arabidopsis. Arabidopsis Book 4, e0075 (2006).

    Google Scholar 

  3. Martínez-Laborda, A., Vera, A. in Fruit Development and Seed Dispresal Annual Plant Reviews, Vol. 38 (ed. Ostergaard, L. ) 172–203 (Wiley-Blackwell, UK, 2009).

    Book  Google Scholar 

  4. Seymour, G. B., Ostergaard, L., Chapman, N. H., Knapp, S. & Martin, C. Fruit development and ripening. Annu. Rev. Plant Biol. 64, 219–241 (2013).

    Article  CAS  PubMed  Google Scholar 

  5. Li, C., Zhou, A. & Sang, T. Rice domestication by reducing shattering. Science 311, 1936–1939 (2006).

    Article  CAS  PubMed  Google Scholar 

  6. Konishi, S. et al. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392–1396 (2006).

    Article  CAS  PubMed  Google Scholar 

  7. Simons, K. J. et al. Molecular characterization of the major wheat domestication gene Q. Genetics 172, 547–555 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Gu, Q., Ferrándiz, C., Yanofsky, M. F. & Martienssen, R. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125, 1509–1517 (1998).

    CAS  PubMed  Google Scholar 

  9. Ferrándiz, C., Liljegren, S. J. & Yanofsky, M. F. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289, 436–438 (2000).

    Article  PubMed  Google Scholar 

  10. Ferrándiz, C. Regulation of fruit dehiscence in Arabidopsis. J. Exp. Bot. 53, 2031–2038 (2002).

    Article  PubMed  Google Scholar 

  11. Liljegren, S. J. et al. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116, 843–853 (2004).

    Article  CAS  PubMed  Google Scholar 

  12. Dinneny, J. R., Weigel, D. & Yanofsky, M. F. A genetic framework for fruit patterning in Arabidopsis thaliana. Development 132, 4687–4696 (2005).

    Article  CAS  PubMed  Google Scholar 

  13. Alonso-Cantabrana, H. et al. Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene. Development 134, 2663–2671 (2007).

    Article  CAS  PubMed  Google Scholar 

  14. Ripoll, J. J., Roeder, A. H., Ditta, G. S. & Yanofsky, M. F. A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development 138, 5167–5176 (2011).

    Article  CAS  PubMed  Google Scholar 

  15. Gonzalez-Reig, S., Ripoll, J. J., Vera, A., Yanofsky, M. F. & Martinez-Laborda, A. Antagonistic gene activities determine the formation of pattern elements along the mediolateral axis of the Arabidopsis fruit. PLoS Genet. 8, e1003020 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Romera-Branchat, M., Ripoll, J. J., Yanofsky, M. F. & Pelaz, S. The WOX13 homeobox gene promotes replum formation in the Arabidopsis thaliana fruit. Plant J. 73, 37–49 (2013).

    Article  CAS  PubMed  Google Scholar 

  17. Ferrándiz, C., Gu, Q., Martienssen, R. & Yanofsky, M. F. Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127, 725–734 (2000).

    PubMed  Google Scholar 

  18. Gillaspy, G., Ben-David, H. & Gruissem, W. Fruits: a developmental perspective. Plant Cell 5, 1439–1451 (1993).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Crane, J. Growth substances in fruit setting and development. Annu. Rev. Plant Physiol. 15, 303–326 (1964).

    Article  CAS  Google Scholar 

  20. Dorcey, E., Urbez, C., Blazquez, M. A., Carbonell, J. & Perez-Amador, M. A. Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant J. 58, 318–332 (2009).

    Article  CAS  PubMed  Google Scholar 

  21. Bateman, A. et al. The Pfam protein families database. Nucleic Acids Res. 32 (Database issue), D138–141 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res. 42 (Database issue), D222–230 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. Ballas, N., Wong, L. M. & Theologis, A. Identification of the auxin-responsive element, AuxRE, in the primary indoleacetic acid-inducible gene, PS-IAA4/5, of pea (Pisum sativum). J. Mol. Biol. 233, 580–596 (1993).

    Article  CAS  PubMed  Google Scholar 

  24. Ulmasov, T., Liu, Z. B., Hagen, G. & Guilfoyle, T. J. Composite structure of auxin response elements. Plant Cell 7, 1611–1623 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Ulmasov, T., Hagen, G. & Guilfoyle, T. J. ARF1, a transcription factor that binds to auxin response elements. Science 276, 1865–1868 (1997).

    Article  CAS  PubMed  Google Scholar 

  26. Guilfoyle, T. J., Ulmasov, T. & Hagen, G. The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol. Life Sci. 54, 619–627 (1998).

    Article  CAS  PubMed  Google Scholar 

  27. Chapman, E. J. & Estelle, M. Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 43, 265–285 (2009).

    Article  CAS  PubMed  Google Scholar 

  28. Boer, D. R. et al. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156, 577–589 (2014).

    Article  CAS  PubMed  Google Scholar 

  29. Nanao, M. H. et al. Structural basis for oligomerization of auxin transcriptional regulators. Nature Commun. 5, 3617 (2014).

    Article  Google Scholar 

  30. Lee, R. C., Feinbaum, R. L. & Ambros, V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854 (1993).

    Article  CAS  PubMed  Google Scholar 

  31. Wightman, B., Ha, I. & Ruvkun, G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862 (1993).

    Article  CAS  PubMed  Google Scholar 

  32. Reinhart, B. J. et al. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Juarez, M. T., Kui, J. S., Thomas, J., Heller, B. A. & Timmermans, M. C. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428, 84–88 (2004).

    Article  CAS  PubMed  Google Scholar 

  34. Mallory, A. C. et al. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J. 23, 3356–3364 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Fujii, H., Chiou, T. J., Lin, S. I., Aung, K. & Zhu, J. K. A miRNA involved in phosphate-starvation response in Arabidopsis. Curr. Biol. 15, 2038–2043 (2005).

    Article  CAS  PubMed  Google Scholar 

  36. Rubio-Somoza, I. & Weigel, D. MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 16, 258–264 (2011).

    Article  CAS  PubMed  Google Scholar 

  37. Cubillos-Ruiz, J. R., Sempere, L. F. & Conejo-Garcia, J. R. Good things come in small packages: Therapeutic anti-tumor immunity induced by microRNA nanoparticles. Oncoimmunology 1, 968–970 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sempere, L. F. Recent advances in miRNA-based diagnostic applications. Expert Rev. Mol. Diagn. 12, 557–559 (2012).

    Article  CAS  PubMed  Google Scholar 

  39. Zhao, Y. et al. MicroRNA-mediated repression of nonsense mRNAs. eLife 3, e03032 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bowman, J. L. Smyth, D. R. & Meyerowitz, E. M. Genes directing flower development in Arabidopsis. Plant Cell 1, 37–52 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Yant, L. et al. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22, 2156–2170 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kagale, S. & Rozwadowski, K. EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6, 141–146 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Krogan, N. T., Hogan, K. & Long, J. A. APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139, 4180–4190 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Aukerman, M. J. & Sakai, H. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15, 2730–2741 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Jung, J. H., Lee, S., Yun, J., Lee, M. & Park, C. M. The miR172 target TOE3 represses AGAMOUS expression during Arabidopsis floral patterning. Plant Sci. 215–216, 29–38 (2014).

    Article  PubMed  Google Scholar 

  46. Chen, X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022–2025 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Schwab, R. et al. Specific effects of microRNAs on the plant transcriptome. Dev. Cell 8, 517–527 (2005).

    Article  CAS  PubMed  Google Scholar 

  48. Moore, I., Samalova, M. & Kurup, S. Transactivated and chemically inducible gene expression in plants. Plant J. 45, 651–683 (2006).

    Article  CAS  PubMed  Google Scholar 

  49. Todesco, M., Rubio-Somoza, I., Paz-Ares, J. & Weigel, D. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet. 6, e1001031 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Riechmann, J. L., Wang, M. & Meyerowitz, E. M. DNA-binding properties of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA and AGAMOUS. Nucleic Acids Res. 24, 3134–3141 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Nagpal, P. et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132, 4107–4118 (2005).

    Article  Google Scholar 

  52. Guilfoyle, T. J. & Hagen, G. Auxin response factors. Curr. Opin. Plant Biol. 10, 453–460 (2007).

    Article  Google Scholar 

  53. Ru, P., Xu, L., Ma, H. & Huang, H. Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res. 16, 457–465 (2006).

    Article  Google Scholar 

  54. Wu, M. F., Tian, Q. & Reed, J. W. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133, 4211–4218 (2006).

    Article  Google Scholar 

  55. Goetz, M. et al. Expression of aberrant forms of AUXIN RESPONSE FACTOR8 stimulates parthenocarpy in Arabidopsis and tomato. Plant Physiol. 145, 351–366 (2007).

    Article  Google Scholar 

  56. de Folter, S. et al. Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17, 1424–1433 (2005).

    Article  Google Scholar 

  57. Melzer, R., Verelst, W. & Theissen, G. The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro. Nucleic Acids Res. 37, 144–157 (2009).

    Article  Google Scholar 

  58. O'Maoileidigh, D. S., Graciet, E. & Wellmer, F. Gene networks controlling Arabidopsis thaliana flower development. New Phytol. 201, 16–30 (2014).

    Article  Google Scholar 

  59. Espinosa-Soto, C., Immink, R. G., Angenent, G. C., Alvarez-Buylla, E. R. & de Folter, S. Tetramer formation in Arabidopsis MADS domain proteins: analysis of a protein-protein interaction network. BMC Syst. Biol. 8, 9 (2014).

    Article  Google Scholar 

  60. Sridhar, V. V., Surendrarao, A. & Liu, Z. APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133, 3159–3166 (2006).

    Article  Google Scholar 

  61. Smaczniak, C. et al. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc. Natl Acad. Sci. USA 109, 1560–1565 (2013).

    Article  Google Scholar 

  62. Kaushal, S., Schneider, J. W., Nadal-Ginard, B. & Mahdavi, V. Activation of the myogenic lineage by MEF2A, a factor that induces and cooperates with MyoD. Science 266, 1236–1240 (1994).

    Article  Google Scholar 

  63. Brambilla, V. et al. Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell 19, 2544–2556 (2007).

    Article  Google Scholar 

  64. Walter, M. et al. Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J. 40, 428–438 (2004).

    Article  Google Scholar 

  65. Kim, J., Harter, K. & Theologis, A. Protein-protein interactions among the Aux/IAA proteins. Proc. Natl Acad. Sci. USA 94, 11786–11791 (1997).

    Article  Google Scholar 

  66. Tiwari, S. B., Hagen, G. & Guilfoyle, T. J. Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16, 533–543 (2004).

    Article  Google Scholar 

  67. Szemenyei, H., Hannon, M. & Long, J. A. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319, 1384–1386 (2008).

    Article  Google Scholar 

  68. Causier, B., Ashworth, M., Guo, W. & Davies, B. The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol. 158, 423–438 (2012).

    Article  Google Scholar 

  69. Guilfoyle, T. J. & Hagen, G. Getting a grasp on domain III/IV responsible for Auxin Response Factor-IAA protein interactions. Plant Sci. 190, 82–88 (2012).

    Article  Google Scholar 

  70. Smyth, D. R., Bowman, J. L. & Meyerowitz, E. M. Early flower development in Arabidopsis. Plant Cell 2, 755–767 (1990).

    Article  Google Scholar 

  71. Wang, R. et al. Multiple regulatory elements in the Arabidopsis NIA1 promoter act synergistically to form a nitrate enhancer. Plant Physiol. 154, 423–432 (2010).

    Article  Google Scholar 

  72. Llave, C., Kasschau, K. D. & Carrington, J. C. Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc. Natl Acad. Sci. USA 97, 13401–13406 (2000).

    Article  Google Scholar 

  73. Voinnet, O., Rivas, S., Mestre, P. & Baulcombe, D. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33, 949–956 (2003).

    Article  Google Scholar 

  74. Grigorova, B. et al. LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138, 2451–2456 (2011).

    Article  Google Scholar 

  75. Dinh, T. T. et al. The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139, 1978–1986 (2012).

    Article  Google Scholar 

Download references

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).

Author information

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

Authors
  1. Juan José Ripoll
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lindsay J. Bailey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Quynh-Anh Mai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Scott L. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cindy T. Hon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elisabeth J. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gary S. Ditta
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mark Estelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Martin F. Yanofsky
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Martin F. Yanofsky.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2015.36

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing