Genome-wide identification and transcriptome profiling reveal that E3 ubiquitin ligase genes relevant to ethylene, auxin and abscisic acid are differentially expressed in the fruits of melting flesh and stony hard peach varieties

- Results: In this study, genome-wide identification, classification and characterization of the E3 ligase genes within the genome of peach ( Prunus persica ) was carried out.
- In total, 765 E3 (PpE3) ligase genes were identified in the peach genome.
- The PpE3 ligase genes were divided into eight subfamilies according to the presence of known functional domains.
- The primary mode of gene duplication of the PpE3 ligase genes was dispersed gene duplication (DSD).
- Four subgroups of the BTB subfamily never characterized before were newly identified in peach, namely BTBAND, BTBBL, BTBP and BTBAN..
- The expression patterns of the identified E3 ligase genes in two peach varieties that display different types of fruit softening (melting flesh, MF, and stony hard, SH) were analyzed at 4 different stages of ripening using Illumina technology.
- Among the 765 PpE3 ligase genes were expressed (FPKM >.
- 1) in the fruit of either MF or SH during fruit ripening.
- Most DEGs were members of the BTB, F-box, U-box and RING subfamilies.
- 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0.
- Full list of author information is available at the end of the article.
- Conclusions: The results of this study provide useful information for further understanding the functional roles of the ubiquitin ligase genes in peach.
- The findings also provide the first clues that E3 ligase genes may function in the regulation of peach ripening..
- Members of the RING, HECT and U-box subfamilies can function as a single subunit, while SCF (SKP1, Cullin1 and F-box protein), CUL3-BTB and CUL4-DDB proteins function in multi- subunit protein complexes.
- Many of the subfamilies of the E3 proteins have been extensively studied, see the reviews [5–7]..
- The establishment of the plantsUPS (a database of plant proteins related to the ubiquitin proteasome sys- tem) enables the exploration and comparative analysis of E3 ligase genes in higher plants (http://bioinformatics..
- Previous studies have shown that endopolyga- lacturonase (endo-PG), the enzyme responsible for cleaving the polygalacturonan network (pectins) of the cell walls, is a candidate gene for controlling the MF/.
- The transcriptome profiles of the PpE3 ligase genes from both a MF (‘Zhongyoutao 13’) and a SH (‘Zhongyoutao 16’) cultivar were examined during fruit ripening.
- Identification and chromosomal distribution of E3 ubiquitin ligase genes in peach.
- The PpE3 ligase genes ac- count for almost 3.0% of the predicted proteins in the peach genome.
- The number of putative E3 ligase genes.
- Normally there are nine subfamilies in the E3 ligase gene family.
- The number of genes in the different subfamilies differed in peach.
- The largest number of genes, 338, was in the RING subfamily.
- The second largest was 267 in the F-box family.
- The RING and F-box subfamilies represented 79% of the predicted PpE3 ligase genes.
- For each of the PpE3 ligase genes, the exons, introns, additional domains and the length of each domain were analyzed (Additional file 1: Table S2).
- According to the number of introns, the PpE3 ligase genes were divided into 5 groups.
- Most of the PpE3 ligase genes, 408, contained between 1 and 5 introns.
- All 765 of the identified PpE3 ligase genes were mapped onto one of the eight peach chromosomes (Additional file 2: Fig.
- Members of the BTB, U-box, F-box and RING subfamilies could be found on every chromosome, while there was no Cullin gene on chromosomes 2, 6, or 7, no SKP gene on chro- mosomes 3, 5, or 6, no HECT gene on chromosomes 2, 3, or 5, and no DDB gene on chromosome or 8.
- To explain the expansion and evolution of the E3 ligase gene family in peach, the patterns of gene duplication were analyzed and compared across the peach genome (Table 2).
- However, the expansion of the PpE3 sub- families did not all follow the same patterns.
- The genomic distribution of the different types of gene duplications found in the PpE3 family was dissected (Fig.
- These results provide further in- sights into the expansion of the PpE3 family in peach..
- SMART and Pfam databases were used to detect the specific domains, shared domains, and other domains of the predicted PpE3 proteins in the eight subfamilies in peach.
- In all, 81 other types of domains were identified in five of the E3 subfamilies (BTB, F-box, U- box, RING and HECT), some of which appeared in more than one subfamily.
- The classification of the BTB, F-box and U-box genes was based on the subfamily-specific domains plus additional domains..
- The phylogenetic analysis results of the BTB sub- family are shown in Fig.
- Members of the FBO subgroup were scattered about the tree, possibly due to the non-uniform domains in the FBO subgroup (Additional file 2: Fig.
- The U-box proteins of peach were also divided into seven subgroups, according to the identity of the add- itional domain (Additional file 2: Figure S4.
- In the phylogenetic tree of the U-box proteins, mem- bers of the ARM, U-box, Pkinase and WD40 subgroups clustered together (Additional file 2: Figure S5.
- The phylogenetic analysis of the eight subgroups partially supports our classification based on SMART and Pfam domains analyses..
- According to the spacing between the amino acids that bind the metal ligands or substitutions at one or more of the metal ligand positions, the RING subfamily was clas- sified into six subgroups, including the RING-C2 (18), RING-G (3), RING-HC (198), RING-H2 (109), RING-S/.
- In the phylogenetic tree, members of most subgroups clustered together, with the exception of the proteins Prupe.1G303200 and Prupe.5G119800, two members of the RING-S/T sub- group that clustered with the RING-HC subgroup (Add- itional file 2: Fig.
- The C-terminal end of the HECT proteins from peach contained an approximately 350-amino acid HECT do- main (Additional file 1: Table S5).
- The phylogenetic tree of the HECT subfamily coincided with the classifi- cation results using the SMART and Pfam databases (Additional file 2: Figure S9.
- Expression of E3 ubiquitin ligase genes during fruit ripening in MF and SH peach.
- To reveal the expression patterns of PpE3 ligase genes in peach fruit, the transcriptome of fruit was analyzed.
- About 95.5% of the high-quality reads were mapped against the peach refer- ence genome (Additional file 1: Table S6)..
- 1 Genomic distribution and duplication of the PpE3 ligase genes across the 8 chromosomes of peach.
- The number of DEGs in the differ- ent subfamilies was different (Table 3).
- Twenty- two of the cluster I DEGs belonged to the RING subfam- ily.
- Prupe.1G020100, a member of the RING subfamily, showed the greatest fold change between the MF and SH peaches (7.2-fold) at stage S4I.
- 2 Predicted domains of BTB proteins representing each of the 14 subgroups.
- Members of the BTB subfamily with different domains are shown.
- It was notable that four of the five CUL- LIN DEGs were in this cluster, Prupe.1G138700, Pru- pe.5G063200, Prupe.5G063700 and Prupe.8G255500..
- 3 Phylogenetic analysis of the peach BTB subfamily.
- The tree was based on the alignment of the full-length BTB protein sequences.
- The expression of the BTB gene Prupe.8G240700 showed the second lowest fold change.
- The num- ber of putative E3 ligase genes in peach was greater than the.
- PpE3 ligase genes represented almost 3.0% of the predicted peach genes, higher than in rice, poplar, soybean, Medicago and maize (around 2.2.
- This indicated that the number of E3 ligase genes in a genome is not associated with the size of the genome..
- The largest and second largest subfamilies, 338 in the RING and 267 in the F-box sub- families, accounted for 79% of the peach E3 ligase genes..
- In peach, the expansion of the RING subfamily was mainly through DSD and WGD.
- Domains within these new of BTB subgroups were detected in previous studies but the combinations of the domains are novel.
- Among the PpE3 ligase genes, the NPH3 (Non-phototropic hypocotyl 3) domain was only observed in the BTB subfamily.
- In this study, the transcriptome profiles of the predicted PpE3 ligase genes in MF and SH pea- ches were compared during fruit ripening.
- Of the identi- fied 765 PpE3 ligase genes were expressed in fruit flesh, and were differentially expressed.
- In Arabi- dopsis, the five members of the BTBZ subgroup (AtBT1-AtBT5) showed functional redundancy and transcriptional compensation among the subgroup members and played vital roles in multiple responses and plant development [56–58].
- Some components of the ethylene-response machinery are used by auxin signal- ing to drive ripening .
- In this study, 765 putative E3 ubiquitin ligase genes were identified in the peach genome, which could be divided into eight subfamilies according to the characterization of known functional domains.
- The primary mode of gene dupli- cation of the PpE3 ligase genes was dispersed gene du- plication (DSD).
- Four new subgroups of the BTB family were first identified in this study.
- All of the DEGs showed a variety of expression patterns during fruit rip- ening.
- Trees of the two cultivars were planted in an or- chard at the Institute of Zhengzhou Fruit Research, Chinese Academy of Agriculture Science (Zhengzhou, China) and were 6-years-old at the time of harvest..
- Eight libraries were gen- erated from the samples of the two peach cultivars at the four stages (S3-S4III) using an Illumina kit and were sequenced by an Illumina HiSeq™2500 sequencer..
- The deduced protein sequences of the E3 ubiquitin lig- ase genes from Arabidopsis and grape were downloaded from the NCBI (http://www.ncbi.nlm.nih.gov).
- The heatmap of the expression patterns of PpE3 ligase genes was gener- ated by Cluster 3.0 software..
- The characteristics of E3 ligase genes in peach.
- Prevalence of duplication modes in the PpE3 subfamilies.
- Phylogenetic analysis of the peach F-box subfamily.
- Phylogenetic analysis of the peach U-box subfamily.
- Se- quence logo of the overrepresented motifs found in the RING-C2, RING-H2, RING-HC, RING-G, RING-v or RING-S/T domains of the RING proteins predicted from the peach genome.
- Phylogenetic analysis of the peach RING subfamily.
- Prehylogenetic analysis of the peach HECT subfamily.
- Snyder for critical reading and language editing of the manuscript..
- The funding bodies had no role in the design of the study, collection, analysis, or interpretation of data or in the writing of the manuscript..
- Ethylene and fruit softening in the stony hard mutation in peach.
- Insertion of a transposon-like sequence in the 5 ′ -flanking region of the YUCCA gene causes the stony hard phenotype.
- Proteomic analysis of the effects of ABA treatments on ripening vitis vinifera berries.
- Genome-wide identification and characterization of the apple ( Malus domestica ) HECT ubiquitin-protein ligase family and expression analysis of their responsiveness to abiotic stresses.
- Genome-wide analyses of the soybean F-box gene family in response to salt stress.
- Genome-wide identification and expression analysis of the BTB domain-containing protein gene family in tomato.
- Genome-wide classification, identification and expression profile of the C3HC4-type Ring finger gene family in poplar ( Populus trichocarpa.
- Genome-wide analysis of the Ring finger gene family in apple.
- Identification and expression profiling of the BTB domain-containing protein gene family in the silkworm, bombyx mori.
- The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis .
- The Arabidopsis Ring-type E3 ligase XBAT32 mediates the proteasomal degradation of the ethylene biosynthetic enzyme, 1-aminocyclopropane-1-carboxylate synthase 7.
- The ATL gene family from Arabidopsis thaliana and Oryza sativa comprises a large number of putative ubiquitin ligases of the Ring-H2 type

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