Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening

Abstract

Background E2 ubiquitin-conjugating (UBC) enzymes are an integral component of the ubiquitin proteasome system that play an important role in plant development, growth, and external stress responses. Several UBC genes have been identified in various plants. However, no studies exploring the functions of UBC genes in regulating fruit of strawberry have been reported. In the present study, a systematic analysis of the entire UBC family members were conducted in the genome of strawberry (Fragaria ×ananassa) based on bioinformatics method, and the gene functioning in strawberry ripening was explored. Results A total of 191 UBC genes were identified in the genome of cultivated strawberry. These genes were unevenly distributed across the 28 chromosomes from the 4 subgenomes of cultivated strawberry, ranging from 3 to 11 genes per chromosome. Moreover, the expansion of FaUBC genes in strawberry was mainly driven by WGD. All the FaUBC genes were clarified into 13 groups and most of them were included in the group VI. The gene structure analysis showed that the number of exons varied from 1 to 23, and the structure of genes had few differences within the same groups but a distinction in different groups. Identification of the cis-acting elements of the promoter revealed multiple regulatory elements that responded to plant growth and development, phytohormone responsive, and abiotic and biotic stress. Data from functional annotation indicated that FaUBC genes play a role in a variety of biological processes. The RNA-seq data showed that FaUBC genes displayed different expression pattern during the fruit ripening process and clarified into 6 clusters. In particular, cluster 3 exhibiting a sudden expression increase in the turning red stage were speculated to be involved in fruit ripening. Hence, two FaUBC genes (FaUBC76 and FaUBC78) were selected for gene function analysis by transient over-expression method. The results indicated that FaUBC76 has a positive effect on the fruit development and ripening in strawberry by up-regulating accumulation of anthocyanins. Moreover, expression of some maturity-related genes were also significantly increased, further supporting a role for FaUBC76 in the regulation of fruit ripening or softening. On the contrary, the overexpression of FaUBC78 significantly increased the firmness of strawberry fruit, indicating that FaUBC78 had a positive role in inhibiting the decrease of strawberry fruit firmness. Conclusion Our study not only provide comprehensive information on system evolution and function on UBC genes, but also give a new insight into explore the roles of FaUBC genes in the regulation of strawberry ripening.

Genome-Wide Analysis of the ERF Family and Identification of Potential Genes Involved in Fruit Ripening in Octoploid Strawberry

“…Gene duplication events such as tandem duplication, WGD, and segmental duplication occurring during genome evolution are the main sources that give rise to gene expansion, and they have remarkable roles in plant growth, development, and adaptability to various stresses. Our result showed that the expansion of FaERFs was mainly due to WGD/segmental duplication, which was consistent with our previous studies in MAPK [37], UBC [38], GMP [39], and GST [40] gene families of the cultivated strawberry. In addition, we found that the number of FaERFs in the B-3 group was significantly greater than other groups by gene duplication, implying that B-3 of FaERFs had significant expansion through the evolution of cultivated strawberries.…”

High-resolution genome-wide association study of a large Czech collection of sweet cherry (Prunus avium L.) on fruit maturity and quality traits

“…Two UBC enzymes are connected with ripening in strawberry fruit. One has a positive effect on fruit development, ripening, and softening by upregulating anthocyanin accumulation and significantly increasing expression of maturity-related genes, whereas the other increases fruit firmness [ 62 ].…”

Genome-wide identification and expression profiling reveal the regulatory role of U-box E3 ubiquitin ligase genes in strawberry fruit ripening and abiotic stresses resistance

“…Meanwhile, the expression levels of some ripening-related genes were significantly increased or decreased. Based on previous reports (Yu et al, 2020;Li et al, 2022), we speculated that FaU-box127 may regulate fruit ripening by affecting the ABA or sucrose pathways, but the mechanism is still unclear and it needs further study.…”

“…Studies on strawberry fruit development and ripening have focused on the regulatory roles of ABA ( Li et al., 2011 ), auxin ( Mezzetti et al., 2004 ), and sucrose ( Luo et al., 2020 ). Furthermore, we have previously found the E2 ubiquitin-conjugating enzyme genes play a vital role in strawberry ripening ( Li et al., 2022 ), whereas, whether and which U-box E3 ubiquitin ligase gene members in strawberry are related to stress responses and fruit ripening is still unknown. In this study, we carried out genome-wide characterization analysis of U-box genes in cultivated strawberry by concentrating on the gene location, gene structure, evolutionary analysis, functional and protein-protein interaction analysis.…”