AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening

PLoS Genet. 2016 Mar 9;12(3):e1005903. doi: 10.1371/journal.pgen.1005903. eCollection 2016 Mar.

Abstract

The involvement of ethylene in fruit ripening is well documented, though knowledge regarding the crosstalk between ethylene and other hormones in ripening is lacking. We discovered that AUXIN RESPONSE FACTOR 2A (ARF2A), a recognized auxin signaling component, functions in the control of ripening. ARF2A expression is ripening regulated and reduced in the rin, nor and nr ripening mutants. It is also responsive to exogenous application of ethylene, auxin and abscisic acid (ABA). Over-expressing ARF2A in tomato resulted in blotchy ripening in which certain fruit regions turn red and possess accelerated ripening. ARF2A over-expressing fruit displayed early ethylene emission and ethylene signaling inhibition delayed their ripening phenotype, suggesting ethylene dependency. Both green and red fruit regions showed the induction of ethylene signaling components and master regulators of ripening. Comprehensive hormone profiling revealed that altered ARF2A expression in fruit significantly modified abscisates, cytokinins and salicylic acid while gibberellic acid and auxin metabolites were unaffected. Silencing of ARF2A further validated these observations as reducing ARF2A expression let to retarded fruit ripening, parthenocarpy and a disturbed hormonal profile. Finally, we show that ARF2A both homodimerizes and interacts with the ABA STRESS RIPENING (ASR1) protein, suggesting that ASR1 might be linking ABA and ethylene-dependent ripening. These results revealed that ARF2A interconnects signals of ethylene and additional hormones to co-ordinate the capacity of fruit tissue to initiate the complex ripening process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Abscisic Acid / pharmacology
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • DNA-Binding Proteins / genetics*
  • Ethylenes / pharmacology
  • Fruit / genetics*
  • Fruit / growth & development
  • Gene Expression Regulation, Plant / drug effects
  • Indoleacetic Acids / pharmacology
  • Lycopersicon esculentum / genetics*
  • Lycopersicon esculentum / growth & development
  • Phenotype
  • Plant Growth Regulators / metabolism*
  • Plant Proteins / genetics*
  • Plant Proteins / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Signal Transduction / drug effects

Substances

  • ARF2 protein, Arabidopsis
  • Arabidopsis Proteins
  • Asr1 protein, Lycopersicon esculentum
  • DNA-Binding Proteins
  • Ethylenes
  • Indoleacetic Acids
  • Plant Growth Regulators
  • Plant Proteins
  • Repressor Proteins
  • Abscisic Acid
  • ethylene

Grant support

AA is supported by the Minerva Foundation (www.theminervafoundation.com) and the European Union Seventh Framework Program FP7/2007-2013 ‘SAMIT’ ERC grant #204575 (http://cordis.europa.eu/fp7/home_en.html). The work in the AA lab was supported by the Adelis Foundation, Leona M. and Harry B. Helmsley Charitable Trust, Jeanne and Joseph Nissim Foundation for Life Sciences, Tom and Sondra Rykoff Family Foundation Research and the Raymond Burton Plant Genome Research Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.