An atypical HLH transcriptional regulator plays a novel and important role in strawberry ripened receptacle

Abstract

BackgroundIn soft fruits, the differential expression of many genes during development and ripening is responsible for changing their organoleptic properties. In strawberry fruit, although some genes involved in the metabolic regulation of the ripening process have been functionally characterized, some of the most studied genes correspond to transcription factors. High throughput transcriptomics analyses performed in strawberry red receptacle (Fragaria x ananassa) allowed us to identify a ripening-related gene that codes an atypical HLH (FaPRE1) with high sequence homology with the PACLOBUTRAZOL RESISTANCE (PRE) genes. PRE genes are atypical bHLH proteins characterized by the lack of a DNA-binding domain and whose function has been linked to the regulation of cell elongation processes.ResultsFaPRE1 sequence analysis indicates that this gene belongs to the subfamily of atypical bHLHs that also includes ILI-1 from rice, SlPRE2 from tomato and AtPRE1 from Arabidopsis, which are involved in transcriptional regulatory processes as repressors, through the blockage by heterodimerization of bHLH transcription factors. FaPRE1 presented a transcriptional model characteristic of a ripening-related gene with receptacle-specific expression, being repressed by auxins and activated by abscisic acid (ABA). However, its expression was not affected by gibberellic acid (GA3). On the other hand, the transitory silencing of FaPRE1 transcription by agroinfiltration in receptacle produced the down-regulation of a group of genes related to the ripening process while inducing the transcription of genes involved in receptacle growth and development.ConclusionsIn summary, this work presents for the first time experimental data that support an important novel function for the atypical HLH FaPRE1 during the strawberry fruit ripening. We hypothesize that FaPRE1 modulates antagonistically the transcription of genes related to both receptacle growth and ripening. Thus, FaPRE1 would repress the expression of receptacle growth promoting genes in the ripened receptacle, while it would activate the expression of those genes related to the receptacle ripening process.

Comparative transcriptome and metabolome analyses of two strawberry cultivars with different storability

“…Transcriptome and degradome analyses showed TFs belonging to WRKY and heat shock factor families and several miRNAs may play roles in regulation of the ripening [30]. An atypical HLH (FaPRE1) belonging to the basic helix-loop-helix/helix-loop-helix (bHLH/HLH) family was identified as a ripening-related TF in strawberry fruit [31,32]. Moreover, FvTCP9 (TEOSINTE BRANCHED 1, CYCLOIDEA, and PROLIFERATING4 CELL and the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry [IPET, grant number 617068-05-1-WT111, http:// www.ipet.re.kr/index.asp, EJL] through the Export Promotion Technology Development Program, funded by the Ministry of Agricultural, Food and Rural Affairs (MAFRA), Republic of Korea.…”

“…Transcriptome and degradome analyses showed TFs belonging to WRKY and heat shock factor families and several miRNAs may play roles in regulation of the ripening [ 30 ]. An atypical HLH ( FaPRE1 ) belonging to the basic helix-loop-helix/helix-loop-helix (bHLH/HLH) family was identified as a ripening-related TF in strawberry fruit [ 31 , 32 ]. Moreover, FvTCP9 (TEOSINTE BRANCHED 1, CYCLOIDEA, and PROLIFERATING4 CELL FACTORS) was revealed as the TF related to fruit ripening via regulation of biosynthesis of ABA and anthocyanin in woodland strawberry ( Fragaria vesca ) fruit [ 33 ].…”

Azacytidine arrests ripening in cultivated strawberry (Fragaria × ananassa) by repressing key genes and altering hormone contents

“…The TFs FaGAMYB ( FvH4_7g04470 ) [ 30 ] and FaASR ( FvH4_2g13410 ) [ 31 ], silencing of which also delays ripening, were also expressed at low levels. The list of TFs that are usually induced during ripening but downregulated in AZA treated tissues includes FaMADS9 ( FvH4_6g46420 ), which is responsible for the deposition of sugars and waxes during ripening [ 32 ], and FaPRE1 ( FvH4_3g04310) , silencing of which leads to repression of ripening related genes [ 33 ] (Additional file 2 ). Interestingly, AZA induced expression of FaMYB9 ( FvH4_2g31130 ) and FaMYB11 ( FvH4_6g34650 ) (Additional file 2 ), two TFs involved in the biosynthesis of proanthocyanins that are mainly accumulated in immature and green receptacles [ 34 ].…”

Insights into transcription factors controlling strawberry fruit development and ripening

“…Furthermore, other ripening-related TFs have been found to regulate FaQR expression. Thus, FaQR is downregulated when FaMADS9, FaSHP, FaPRE1 and FvTCP9 are silenced, supporting a positive role of these regulators on the biosynthesis of furaneol (Seymour et al, 2011;Daminato et al, 2013;Medina-Puche et al, 2019;Xie et al, 2020).…”