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An Evolutionary Analysis of B-Box Transcription Factors in Strawberry Reveals the Role of FaBBx28c1 in the Regulation of Flowering Time.

ABSTRACT: Flowering connects vegetative and generative developmental phases and plays a significant role in strawberry production. The mechanisms that regulate strawberry flowering time are unclear. B-box transcription factors (BBXs) play important roles in the flowering time regulation of plants. Nevertheless, BBXs in octoploid cultivated strawberry (Fragaria ananassa) and their functions in flowering time regulation have not been identified. Here, we identified 51 FaBBXs from cultivated strawberry and 16 FvBBXs from diploid wild strawberry (Fragaria vesca), which were classified into five groups according to phylogenetic analysis. Further evolutionary analysis showed that whole-genome duplication or segmental duplication is a crucial factor that leads to the expansion of the BBX gene family in two strawberry species. Moreover, some loss and acquisition events of FaBBX genes were identified in the genome of cultivated strawberry that could have affected traits of agronomic interest, such as fruit quality. The promoters of FaBBX genes showed an enrichment in light-responsive, cis-regulatory elements, with 16 of these genes showing changes in their transcriptional activity in response to blue light treatment. On the other hand, FaBBX28c1, whose transcriptional activity is reduced in response to blue light, showed a delay in flowering time in Arabidopsis transgenic lines, suggesting its role in the regulation of flowering time in cultivated strawberry. Our results provide new evolutionary insight into the BBX gene family in cultivated strawberry and clues regarding their function in flowering time regulation in plants.

SUBMITTER: Ye Y

PROVIDER: S-EPMC8583817 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Eukaryotic cells use nonsense-mediated mRNA decay (NMD) to clear aberrant mRNAs from the cell, thus preventing the accumulation of truncated proteins. In Arabidopsis, two UP-Frameshift (UPF) proteins, UPF1 and UPF3, play a critical role in NMD. Although deficiency of UPF1 and UPF3 leads to various developmental defects, little is known about the mechanism underlying the regulation of flowering time by NMD. Here, we showed that the upf1-5 and upf3-1 mutants had a late-flowering phenotype under long-day conditions and the upf1-5 upf3-1 double mutants had an additive effect in delaying flowering time. RNA sequencing of the upf mutants revealed that UPF3 exerted a stronger effect than UPF1 in the UPF-mediated regulation of flowering time. Among genes known to regulate flowering time, FLOWERING LOCUS C (FLC) mRNA levels increased (up to 8-fold) in upf mutants, as confirmed by qPCR. The upf1-5, upf3-1, and upf1-5 upf3-1 mutants responded to vernalization, suggesting a role of FLC in delayed flowering of upf mutants. Consistent with the high FLC transcript levels and delayed flowering in upf mutants, levels of FLOWERING LOCUS T (FT) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) mRNAs were reduced in the upf mutants. However, RNA-seq did not identify an aberrant FLC transcript containing a premature termination codon (PTC), suggesting that FLC is not a direct target in the regulation of flowering time by NMD. Among flowering time regulators that act in an FLC-dependent manner, we found that MAF3, NF-YA2, NF-YA5, and TAF14 showed increased transcript levels in upf mutants. We also found that BBX19 and ATC, which act in an FLC-independent manner, showed increased transcript levels in upf mutants. An aberrant transcript containing a PTC was identified from MAF3 and BBX19 and the levels of the aberrant transcripts increased in upf mutants. Taking these results together, we propose that the late-flowering phenotype of upf mutants is mediated by at least two different pathways, namely, by MAF3 in an FLC-dependent manner and by BBX19 in an FLC-independent manner.

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An Evolutionary Analysis of B-Box Transcription Factors in Strawberry Reveals the Role of FaBBx28c1 in the Regulation of Flowering Time.

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