The NAC transcription factor FaRIF controls fruit ripening in strawberry

Authors: MARTIN-PIZZARO, CARMEN - University Of Malaga; VILLARINO, JOSE - University Of Malaga; OSORIO, SONIA - University Of Malaga; MECO, VICTORIANO - University Of Malaga; URRITIA, MARIA - University Of Malaga; PILLET, JEREMY - University Of Malaga; CASANAL, ANA - University Of Malaga; MERCHANTE, CATHARINA - University Of Malaga; AMAYA, IRAIDA - University Of Malaga; WILLMITZER, LOTHAR - Max Planck Institute Of Molecular Plant Physiology; FERNIE, ALISDAIR - Max Planck Institute Of Molecular Plant Physiology; Giovannoni, James; BOTELLA, MIGUEL - University Of Malaga; VALPUESTA, VICTORIANO - University Of Malaga; POSE, DAVID - University Of Malaga

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/20/2021
Publication Date: 2/24/2021
Citation: Martin-Pizzaro, C., Villarino, J., Osorio, S., Meco, V., Urritia, M., Pillet, J., Casanal, A., Merchante, C., Amaya, I., Willmitzer, L., Fernie, A., Giovannoni, J.J., Botella, M., Valpuesta, V., Pose, D. 2021. The NAC transcription factor FaRIF controls fruit ripening in strawberry. The Plant Cell. 331574-1593. https://doi.org/10.1093/plcell/koab070.
DOI: https://doi.org/10.1093/plcell/koab070

Interpretive Summary: Strawberry is one of the most popular fruit crops thanks to the unique flavor and aroma of its berries, two critical quality parameters that are acquired during the ripening process. The strawberry fruit consists of a fleshy part (receptacle) that results from the development of the flower receptacle, in which the actual fruits (achenes) are embedded. Strawberry ripening is a genetically programmed and highly coordinated process that leads to structural and biochemical changes such as softening and increase in the contents of sugars, anthocyanins, volatile compounds, and vitamins. Strawberry fruit has been considered as a genuine example of non-climacteric fruit ripening, which, in contrast to that of climacteric fruits, does not require ethylene to initiate and/or maintain the ripening program. We identified and characterized a transcription factor, NAC FaRIF, that plays a central role in controlling strawberry fruit ripening. Its regulatory role is executed from the early stages of fruit development and its disruption results in inhibition of fruit ripening.

Technical Abstract: In contrast to climacteric fruits such as tomato, the knowledge on key regulatory genes controlling the ripening of straw- berry, a nonclimacteric fruit, is still limited. NAC transcription factors (TFs) mediate different developmental processes in plants. Here, we identified and characterized Ripening Inducing Factor (FaRIF), a NAC TF that is highly expressed and induced in strawberry receptacles during ripening. Functional analyses based on stable transgenic lines aimed at silencing FaRIF by RNA interference, either from a constitutive promoter or the ripe receptacle-specific EXP2 promoter, as well as over-expression lines showed that FaRIF controls critical ripening-related processes such as fruit softening and pigment and sugar accumulation. Physiological, metabolome, and transcriptome analyses of receptacles of FaRIF-silenced and overexpression lines point to FaRIF as a key regulator of strawberry fruit ripening from early developmental stages, controlling abscisic acid biosynthesis and signaling, cell-wall degradation, and modification, the phenylpropanoid pathway, volatiles production, and the balance of the aerobic/anaerobic metabolism. FaRIF is therefore a target to be modified/edited to control the quality of strawberry fruits.