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      Comparative physiological, metabolomic and transcriptomic analyses reveal the mechanisms of differences in pear fruit quality between distinct training systems

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          Abstract

          Background

          Canopy architecture is critical in determining the fruit-zone microclimate and, ultimately, in determining an orchard’s success in terms of the quality and quantity of the fruit produced. However, few studies have addressed how the canopy environment leads to metabolomic and transcriptomic alterations in fruits. Designing strategies for improving the quality of pear nutritional components relies on uncovering the related regulatory mechanisms.

          Results

          We performed an in-depth investigation of the impact of canopy architecture from physiological, metabolomic and transcriptomic perspectives by comparing pear fruits grown in a traditional freestanding system (SP) or a flat-type trellis system (DP). Physiological studies revealed relatively greater fruit sizes, soluble solid contents and titratable acidities in pear fruits from DP systems with open canopies. Nontargeted metabolite profiling was used to characterize fruits at the initial ripening stage. Significant differences in fruit metabolites, including carbohydrates, nucleic acids, alkaloids, glycerophospholipids, sterol lipids, and prenol lipids, were observed between the two groups. Transcriptomic analysis indicated that a series of organic substance catabolic processes (e.g., the glycerol-3-phosphate catabolic process, pectin catabolic process and glucan catabolic process) were overrepresented in fruits of the DP system. Moreover, integrative analysis of the metabolome and transcriptome at the pathway level showed that DP pear fruits may respond to the canopy microenvironment by upregulating phenylpropanoid biosynthesis pathway genes such as PpPOD. Transient assays revealed that the contents of malic acid and citric acid were lower in the pear flesh of PpPOD RNAi plants, which was associated with regulating the expression of organic acid metabolism-related genes.

          Conclusions

          Our results provide fundamental evidence that at the physiological and molecular levels, open-canopy architecture contributes to improving pear fruit quality and is correlated with increased levels of carbohydrates and lipid-like molecules. This study may lead to the development of rational culture practices for enhancing the nutritional traits of pear fruits.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12870-023-04716-8.

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          Most cited references64

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          KEGG: kyoto encyclopedia of genes and genomes.

          M Kanehisa (2000)
          KEGG (Kyoto Encyclopedia of Genes and Genomes) is a knowledge base for systematic analysis of gene functions, linking genomic information with higher order functional information. The genomic information is stored in the GENES database, which is a collection of gene catalogs for all the completely sequenced genomes and some partial genomes with up-to-date annotation of gene functions. The higher order functional information is stored in the PATHWAY database, which contains graphical representations of cellular processes, such as metabolism, membrane transport, signal transduction and cell cycle. The PATHWAY database is supplemented by a set of ortholog group tables for the information about conserved subpathways (pathway motifs), which are often encoded by positionally coupled genes on the chromosome and which are especially useful in predicting gene functions. A third database in KEGG is LIGAND for the information about chemical compounds, enzyme molecules and enzymatic reactions. KEGG provides Java graphics tools for browsing genome maps, comparing two genome maps and manipulating expression maps, as well as computational tools for sequence comparison, graph comparison and path computation. The KEGG databases are daily updated and made freely available (http://www. genome.ad.jp/kegg/).
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            Mapping and quantifying mammalian transcriptomes by RNA-Seq.

            We have mapped and quantified mouse transcriptomes by deeply sequencing them and recording how frequently each gene is represented in the sequence sample (RNA-Seq). This provides a digital measure of the presence and prevalence of transcripts from known and previously unknown genes. We report reference measurements composed of 41-52 million mapped 25-base-pair reads for poly(A)-selected RNA from adult mouse brain, liver and skeletal muscle tissues. We used RNA standards to quantify transcript prevalence and to test the linear range of transcript detection, which spanned five orders of magnitude. Although >90% of uniquely mapped reads fell within known exons, the remaining data suggest new and revised gene models, including changed or additional promoters, exons and 3' untranscribed regions, as well as new candidate microRNA precursors. RNA splice events, which are not readily measured by standard gene expression microarray or serial analysis of gene expression methods, were detected directly by mapping splice-crossing sequence reads. We observed 1.45 x 10(5) distinct splices, and alternative splices were prominent, with 3,500 different genes expressing one or more alternate internal splices.
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              Is Open Access

              VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R

              Background Visualization of orthogonal (disjoint) or overlapping datasets is a common task in bioinformatics. Few tools exist to automate the generation of extensively-customizable, high-resolution Venn and Euler diagrams in the R statistical environment. To fill this gap we introduce VennDiagram, an R package that enables the automated generation of highly-customizable, high-resolution Venn diagrams with up to four sets and Euler diagrams with up to three sets. Results The VennDiagram package offers the user the ability to customize essentially all aspects of the generated diagrams, including font sizes, label styles and locations, and the overall rotation of the diagram. We have implemented scaled Venn and Euler diagrams, which increase graphical accuracy and visual appeal. Diagrams are generated as high-definition TIFF files, simplifying the process of creating publication-quality figures and easing integration with established analysis pipelines. Conclusions The VennDiagram package allows the creation of high quality Venn and Euler diagrams in the R statistical environment.
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                Author and article information

                Contributors
                wutaoga556@163.com
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                4 January 2024
                4 January 2024
                2024
                : 24
                : 28
                Affiliations
                Hubei Key Laboratory of Germplasm Innovation and Utilization of Fruit Trees, Research Institute of Fruit and Tea, Hubei Academy of Agricultural Sciences, ( https://ror.org/04qg81z57) Wuhan, Hubei 430064 China
                Article
                4716
                10.1186/s12870-023-04716-8
                10765702
                38172675
                79a6f371-d791-4036-8520-2b0e7109dc52
                © The Author(s) 2024

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 16 June 2023
                : 29 December 2023
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100010203, Agriculture Research System of China;
                Award ID: CARS, CARS-28
                Funded by: Major Program of Hubei Agricultural Science and Technology Innovation Center
                Award ID: 2020-620-000-002-05
                Categories
                Research
                Custom metadata
                © BioMed Central Ltd., part of Springer Nature 2024

                Plant science & Botany
                pear fruits,training systems,canopy environment,metabolome,transcriptome,phenylpropanoid biosynthesis pathway

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