Deciphering the regulatory network of the NAC transcription factor FvRIF, a key regulator of strawberry (Fragaria vesca) fruit ripening

Abstract

The NAC transcription factor RIF (Ripening Inducing Factor) was previously reported to be necessary for the ripening of octoploid strawberry (Fragaria × ananassa) fruit, but the mechanistic basis of RIF-mediated transcriptional regulation and how RIF activity is modulated remains elusive. Here we show that FvRIF in diploid strawberry, Fragaria vesca, is a key regulator in the control of fruit ripening, and that knockout mutations of FvRIF result in a complete block of fruit ripening. DNA affinity purification sequencing coupled with transcriptome deep sequencing suggests that 2080 genes are direct targets of FvRIF-mediated regulation, including those related to various aspects of fruit ripening. We provide evidence that FvRIF modulates anthocyanin biosynthesis and fruit softening by directly regulating the related core genes. Moreover, we demonstrate that FvRIF interacts with and serves as a substrate of mitogen-activated protein kinase 6 (FvMAPK6), which regulates the transcriptional activation function of FvRIF by phosphorylating FvRIF at Thr-310. Our findings uncover the FvRIF-mediated transcriptional regulatory network in controlling strawberry fruit ripening and highlight the physiological significance of phosphorylation modification on FvRIF activity in ripening.

For a Colorful Life: Recent Advances in Anthocyanin Biosynthesis during Leaf Senescence

“…Other transcription factors including HY5, BBX, NAC, and WRKY have been reported to play key roles in anthocyanin accumulation by regulating the expression of MYBs (Figure 1). FvRIF, a NAC transcription factor, activates the transcription of FvMYB10 in the fruit of strawberry, establishing a clear connection between fruit development and anthocyanin accumulation [38]. Several BBX proteins in pears have been identified as promoters of anthocyanin accumulation.…”

Tandem transcription factors PpNAC56 and PpNAC72 synergistically activate the transcription of PpPGF to regulate softening during peach fruit ripening

“…Transgenic introduction of MdNAC18.1 into the tomato nor mutant complemented the ripening de ciency observed in the nor mutant (Migicovsky et al 2021). Furthermore, the NAC transcription factor RIPENING INDUCING FACTOR (RIF), which is an orthologue of NOR, plays a crucial role in the regulation of strawberry fruit ripening and knockout mutations of FvRIF result in a complete blockade of fruit ripening (Martin-Pizarro et al 2021; Li et al 2023). Moreover, FvRIF modulates anthocyanin biosynthesis and fruit softening by directly regulating the expression of related core genes (Li et al 2023).…”

“…Furthermore, the NAC transcription factor RIPENING INDUCING FACTOR (RIF), which is an orthologue of NOR, plays a crucial role in the regulation of strawberry fruit ripening and knockout mutations of FvRIF result in a complete blockade of fruit ripening (Martin-Pizarro et al 2021; Li et al 2023). Moreover, FvRIF modulates anthocyanin biosynthesis and fruit softening by directly regulating the expression of related core genes (Li et al 2023). Collectively, these studies demonstrate that NOR and its orthologue genes play vital roles in both climacteric and non-climacteric fruit ripening.…”

The regulatory landscape of RIF-mediated ripening control in strawberry

“…Recent work identified RIPENING INDUCING FACTOR ( FaRIF ), a NAC transcription factor that plays a role in controlling ripening-related processes in the octoploid strawberry Fragaria × ananassa , such as color, the accumulation of sugars and organic acids, and fruit softening ( Martin-Pizarro et al 2021 ). In this issue, Xiaojing Li and colleagues ( Li et al 2023 ) expand the regulatory landscape of RIF-mediated ripening control by identifying regulatory elements acting down- and upstream of RIF, highlighting its role as a key regulator of fruit ripening. Using genome editing, the authors generated rif knockout lines in the diploid strawberry Fragaria vesca .…”