Exploring large-scale gene coexpression networks in peach (Prunus persica L.): a new tool for predicting gene function

Felipe Pérez de los Cobos , Beatriz E. García-Gómez , Luis Orduña-Rubio , Ignasi Batlle , Pere Arús , José Tomás Matus , Iban Eduardo

Horticulture Research ›› 2024, Vol. 11 ›› Issue (2) : 294

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (2) :294 DOI: 10.1093/hr/uhad294
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Exploring large-scale gene coexpression networks in peach (Prunus persica L.): a new tool for predicting gene function
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Abstract

Peach is a model for Prunus genetics and genomics, however, identifying and validating genes associated to peach breeding traits is a complex task. A gene coexpression network (GCN) capable of capturing stable gene-gene relationships would help researchers overcome the intrinsic limitations of peach genetics and genomics approaches and outline future research opportunities. In this study, we created four GCNs from 604 Illumina RNA-Seq libraries. We evaluated the performance of every GCN in predicting functional annotations using an algorithm based on the ‘guilty-by-association’ principle. The GCN with the best performance was COO300, encompassing 21 956 genes. To validate its performance predicting gene function, we performed two case studies. In case study 1, we used two genes involved in fruit flesh softening: the endopolygalacturonases PpPG21 and PpPG22. Genes coexpressing with both genes were extracted and referred to as melting flesh (MF) network. Finally, we performed an enrichment analysis of MF network and compared the results with the current knowledge regarding peach fruit softening. The MF network mostly included genes involved in cell wall expansion and remodeling, and with expressions triggered by ripening-related phytohormones, such as ethylene, auxin, and methyl jasmonate. In case study 2, we explored potential targets of the anthocyanin regulator PpMYB10.1 by comparing its gene-centered coexpression network with that of its grapevine orthologues, identifying a common regulatory network. These results validated COO300 as a powerful tool for peach and Prunus research. This network, renamed as PeachGCN v1.0, and the scripts required to perform a function prediction analysis are available at https://github.com/felipecobos/PeachGCN.

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Felipe Pérez de los Cobos, Beatriz E. García-Gómez, Luis Orduña-Rubio, Ignasi Batlle, Pere Arús, José Tomás Matus, Iban Eduardo. Exploring large-scale gene coexpression networks in peach (Prunus persica L.): a new tool for predicting gene function. Horticulture Research, 2024, 11 (2) : 294 DOI:10.1093/hr/uhad294

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Acknowledgements

We acknowledge financial support through the Severo Ochoa Programme for Centers of Excellence in R&D (SEV-2015-0533 and CEX2019-000902-S). Also, this work was funded by the Spanish Ministry of Science and Innovation through the Estate Agency of Research: Project PID2020-118612RR-I00 (Better Almonds) and PID2019-110599RR-I00. Authors F.P. C., I. E., I. B. are grateful to CERCA Program from Generalitat of Catalonia for its support. F. P. C. wishes to acknowledge the receipt of a FPI doctoral fellowship from the Spanish Ministry of Science and Innovation. This work was also supported by grants PID2021-128865NB-I00 and RYC-2017-23645 awarded to J.T.M. and the PRE2019-088044 fellowship awarded to L.O. from the Ministerio de Ciencia, Innovación y Universidades (MCIU, Spain), Agencia Estatal de Investigación (AEI, Spain), and Fondo Europeo de Desarrollo Regional (FEDER, European Union).

Author Contributions

F.P.C. participated in the conceptualization, analysis, and writing the original draft. B.G.G. participated in the analysis and writing the original draft, reviewing, and editing. L.O.R. participated in the analysis, reviewing, and editing. I.B. participated in the supervision, reviewing, editing, project management, and seeking funding. P.A. participated in the supervision, reviewing, editing, and project management. J.T.M. participated in the conceptualization, supervision, reviewing, and editing. I.E. participated in the conceptualization, supervision, reviewing, editing, project management, and seeking funding.

Data Availability

The PeachGCN v1.0, and the scripts necessary to run a function prediction analysis using it, are available at https://github.com/felipecobos/PeachGCN.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Oliver S. Guilt-by-association goes global. Nat Cell Biol. 2000; 403: 601-2

[2]

Schaefer RJ, Michno JM, Myers CL. Unraveling gene function in agricultural species using gene co-expression networks. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms. 2017; 1860:53-63

[3]

Amrine KCH, Blanco-Ulate B, Cantu D. Discovery of Core biotic stress responsive genes in Arabidopsis by weighted gene co-expression network analysis. PLoS One. 2015; 10:e0118731.

[4]

Furuya T, Saito M, Uchimura H. et al. Gene co-expression network analysis identifies BEH3 as a stabilizer of secondary vascular development in Arabidopsis. Plant Cell. 2021; 33:2618-36

[5]

Lv L, Zhang W, Sun L. et al. Gene co-expression network analysis to identify critical modules and candidate genes of drought-resistance in wheat. PLoS One. 2020; 15:e0236186

[6]

Mao L, Van Hemert JL, Dash S. et al. Arabidopsis gene co-expression network and its functional modules. Bioinformatics. 2009; 10:1-24

[7]

Huang J, Vendramin S, Shi L. et al. Construction and optimization of a large gene coexpression network in maize using RNA-seq data. Plant Physiol. 2017; 175:568-83

[8]

Ma S, Ding Z, Li P. Maize network analysis revealed gene modules involved in development, nutrients utilization, metabolism, and stress response. BMC Plant Biol. 2017; 17:131-17

[9]

Childs KL, Davidson RM, Buell CR. Gene Coexpression network analysis as a source of functional annotation for Rice genes. PLoS One. 2011; 6:e22196

[10]

Ficklin SP, Luo F, Feltus FA. The Association of Multiple Interacting Genes with specific phenotypes in Rice using gene Coexpression networks. Plant Physiol. 2010; 154:13-24

[11]

Orduña L, Li M, Navarro-Payá D. et al. Direct regulation of shikimate, early phenylpropanoid, and stilbenoid pathways by subgroup 2 R2R3-MYBs in grapevine. Plant J. 2022; 110: 529-47

[12]

Orduña-Rubio L, Santiago A, Navarro-Payá D. et al. Aggregated gene co-expression networks for predicting transcription factor regulatory landscapes in a non-model plant species. BioRxiv. 2023

[13]

Wong DCJ. Network aggregation improves gene function prediction of grapevine gene co-expression networks. Plant Mol Biol. 2020; 103:425-41

[14]

Wong DCJ, Schlechter R, Vannozzi A. et al. A systems-oriented analysis of the grapevine R2R3-MYB transcription factor family uncovers new insights into the regulation of stilbene accumulation. DNA Res. 2016; 23:451-66

[15]

Aranzana MJ, Decroocq V, Dirlewanger E. et al. Prunus genetics and applications after de novo genome sequencing: achievements and prospects. 2019; 6:58.

[16]

Limera C, Sabbadini S, Sweet JB. et al. New biotechnological tools for the genetic improvement of major Woody fruit species. Front Plant Sci. 2017; 8:1418

[17]

Ricci A, Sabbadini S, Prieto H. et al. Genetic transformation in peach (Prunus persica L.): challenges and ways forward. Plan Theory. 2020; 9:971

[18]

Dardick C, Callahan A, Horn R. et al. PpeTAC1 promotes the horizontal growth of branches in peach trees and is a member of a functionally conserved gene family found in diverse plants species. Plant J. 2013; 75:618-30

[19]

Guseman JM, Webb K, Srinivasan C. et al. DRO1 influences root system architecture in Arabidopsis and Prunus species. Plant J. 2017; 89:1093-105

[20]

García-Gómez BE, Ruiz D, Salazar JA. et al. Analysis of metabolites and gene expression changes relative to apricot (Prunus armeniaca L.) fruit quality during development and ripening. Front Plant Sci. 2020; 11:1269

[21]

Jiang X, Liu K, Peng H. et al. Comparative network analysis reveals the dynamics of organic acid diversity during fruit ripening in peach (Prunus persica L. Batsch). BMC Plant Biol. 2023; 23: 1-14

[22]

Wang Q, Cao K, Li Y. et al. Identification of co-expressed networks and key genes associated with organic acid in peach fruit. Sci Hortic. 2023; 307:111496

[23]

Wu X, Du A, Zhang S. et al. Regulation of growth in peach roots by exogenous hydrogen sulfide based on RNA-Seq. Plant Physiol Biochem. 2021; 159:179-92

[24]

Xi W, Feng J, Liu Y. et al. The R2R3-MYB transcription factor PaMYB10 is involved in anthocyanin biosynthesis in apricots and determines red blushed skin. BMC Plant Biol. 2019; 19:287

[25]

Zhang Q, Feng C, Li W. et al. Transcriptional regulatory networks controlling taste and aroma quality of apricot (Prunus armeniaca L.) fruit during ripening. BMC Genomics. 2019; 20:45

[26]

Verde I, Abbott AG, Scalabrin S. et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet. 2013; 45:487-94

[27]

Verde I, Jenkins J, Dondini L. et al. The peach v2.0 release: high-resolution linkage mapping and deep resequencing improve chromosome-scale assembly and contiguity. BMC Genomics. 2017; 18:225

[28]

Sayers EW, Bolton EE, Brister JR. et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 2022; 50:D20-6

[29]

Cheng C, Liu J, Wang X. et al. PpERF/ABR1 functions as an activator to regulate PpPG expression resulting in fruit softening during storage in peach (Prunus persica). Postharvest Biol Technol. 2022; 189:111919

[30]

Gu C, Wang L, Wang W. et al. Copy number variation of a gene cluster encoding endopolygalacturonase mediates flesh texture and stone adhesion in peach. J Exp Bot. 2016; 67:1993-2005

[31]

Jiang L, Kang R, Feng L. et al. iTRAQ-based quantitative proteomic analysis of peach fruit (Prunus persica L.) at different ripening and postharvest storage stages. Postharvest Biol Technol. 2020; 164:111137

[32]

Nakano R, Kawai T, Fukamatsu Y. et al. Postharvest properties of ultra-late maturing peach cultivars and their attributions to melting flesh (M) locus: re-evaluation of M locus in association with flesh texture. Front Plant Sci. 2020; 11:1817

[33]

Qian M, Xu Z, Zhang Z. et al. The downregulation of PpPG21 and PpPG22 influences peach fruit texture and softening. Planta. 2021; 254:22-12

[34]

Zhu Y, Zeng W, Wang X. et al. Characterization and transcript profiling of PME and PMEI gene families during peach fruit maturation. J Am Soc Hortic Sci. 2017; 142:246-59

[35]

Bretó MP, Cantín CM, Iglesias I. et al. Mapping a major gene for red skin color suppression (highlighter) in peach. Euphytica. 2017; 213

[36]

Cao K, Ding T, Mao D. et al. Transcriptome analysis reveals novel genes involved in anthocyanin biosynthesis in the flesh of peach. Plant Physiol Biochem. 2018; 123:94-102

[37]

Cheng J, Wei G, Zhou H. et al. Unraveling the mechanism underlying the glycosylation and methylation of anthocyanins in peach. Plant Physiol. 2014; 166:1044-58

[38]

Liu X, Chen M, Wen B. et al. Transcriptome analysis of peach (Prunus persica) fruit skin and differential expression of related pigment genes. Sci Hortic. 2019a; 250:271-7

[39]

Rahim MA, Busatto N, Trainotti L. Regulation of anthocyanin biosynthesis in peach fruits. Planta. 2014; 240:913-29

[40]

Ravaglia D, Espley RV, Henry-Kirk RA. et al. Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC Plant Biol. 2013; 13:68

[41]

Tuan PA, Bai S, Yaegaki H. et al. The crucial role of PpMYB10.1 in anthocyanin accumulation in peach and relationships between its allelic type and skin color phenotype. BMC Plant Biol. 2015; 15:280

[42]

Zhao Y, Dong W, Zhu Y. et al. PpGST1, an anthocyanin-related glutathione S-transferase gene, is essential for fruit coloration in peach. Plant Biotechnol J. 2020; 18:1284-95

[43]

Zhou H, Lin-Wang K, Wang H. et al. Molecular genetics of blood-fleshed peach reveals activation of anthocyanin biosynthesis by NAC transcription factors. Plant J. 2015; 82:105-21

[44]

Trainotti L, Tadiello A, Casadoro G. The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot. 2007; 58:3299-308

[45]

Soto A, Ruiz KB, Ziosi V. et al. Ethylene and auxin biosynthesis and signaling are impaired by methyl jasmonate leading to a transient slowing down of ripening in peach fruit. J Plant Physiol. 2012; 169:1858-65

[46]

Wei J, Wen X, Tang L. Effect of methyl jasmonic acid on peach fruit ripening progress. Sci Hortic. 2017; 220:206-13

[47]

Tonutti P, Bonghi C, Ruperti B. et al. Ethylene evolution and 1-aminocyclopropane-1-carboxylate oxidase gene expression during early development and ripening of peach fruit. J Am Soc Hortic Sci. 1997; 122:642-7

[48]

Tatsuki M, Nakajima N, Fujii H. et al. Increased levels of IAA are required for system 2 ethylene synthesis causing fruit softening in peach (Prunus persica L. Batsch). J Exp Bot. 2013; 64:1049-59

[49]

Wang X, Ding Y, Wang Y. et al. Genes involved in ethylene signal transduction in peach (Prunus persica) and their expression profiles during fruit maturation. Sci Hortic. 2017; 224:306-16

[50]

Pan L, Zeng W, Niu L. et al. PpYUC11, a strong candidate gene for the stony hard phenotype in peach (Prunus persica L. Batsch), participates in IAA biosynthesis during fruit ripening. J Exp Bot. 2015; 66:7031-44

[51]

Bonghi C, Manganaris GA. Systems biology approaches reveal new insights into the molecular mechanisms regulating flesh fruit quality. In: Omics Technologies: Tools for Food Science. Taylor Francis group, 2012,25

[52]

Tanaka Y, Sasaki N, Ohmiya A. Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008; 54:733-49

[53]

Ma Y, Ma X, Gao X. et al. Light induced regulation pathway of anthocyanin biosynthesis in plants. Molecular sciences. 2021; 22:11116

[54]

Santin M, Simoni S, Vangelisti A. et al. Transcriptomic analysis on the Peel of UV-B-exposed peach fruit reveals an Upregulation of phenolic- and UVR8-related pathways. Plan Theory. 2023; 12:1818

[55]

Zhou Y, Guo D, Li J. et al. Coordinated regulation of anthocyanin biosynthesis through photorespiration and temperature in peach (Prunus persica f. atropurpurea). Tree Genetics and Genomes. 2013; 9:265-78

[56]

Zhu YC, Zhang B, Allan AC. et al. DNA demethylation is involved in the regulation of temperature-dependent anthocyanin accumulation in peach. Plant J. 2020; 102:965-76

[57]

Liu W, Lin L, Zhang Z. et al. Gene co-expression network analysis identifies trait-related modules in Arabidopsis thaliana. Planta. 2019b; 249:1487-501

[58]

Lu Z, Cao H, Pan L. et al. Two loss-of-function alleles of the glutathione S-transferase (GST) gene cause anthocyanin deficiency in flower and fruit skin of peach (Prunus persica). Plant J. 2021; 107:1320-31

[59]

Zhao Y, Dong W, Wang K. et al. Differential sensitivity of fruit pigmentation to ultraviolet light between two peach cultivars. Front Plant Sci. 2017; 8

[60]

Wang DR, Yang K, Wang X. et al. Overexpression of MdZAT5, an C2H2-type zinc finger protein, regulates anthocyanin accumulation and salt stress response in apple Calli and Arabidopsis. Int J Mol Sci. 2022; 23

[61]

Zhang L, Tao R, Wang S. et al. PpZAT5 suppresses the expression of a B-box gene PpBBX18 to inhibit anthocyanin biosynthesis in the fruit peel of red pear. Front Plant Sci. 2022; 13:1-14

[62]

Dekker JP, Boekema EJ. Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta Bioenerg. 2005; 1706:12-39

[63]

Montané MH, Kloppstech K. The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene. 2000; 258:1-8

[64]

Leinonen R, Sugawara H, Shumway M. et al. The sequence read archive. Nucleic Acids Res. 2011; 39:D19-21

[65]

Jung S, Lee T, Cheng C-H. et al. 15 years of GDR: new data and functionality in the genome database for Rosaceae. Nucleic Acids Res. 2019; 47:D1137-45

[66]

Ashburner M, Ball CA, Blake JA. et al. Gene ontology: tool for the unification of biology. Nat Genet. 2000; 25:25-9

[67]

Carbon S, Douglass E, Good BM. et al. The gene ontology resource: enriching a GOld mine. Nucleic Acids Res. 2021; 49:D325-34

[68]

Mistry J, Chuguransky S, Williams L. et al. Pfam:the protein families database in 2021. Nucleic Acids Res. 2021; 49: D412-9

[69]

Durinck S, Spellman PT, Birney E. et al. Mapping identifiers for the integration of genomic datasets with the R/bioconductor package biomaRt. Nat Protoc. 2009; 4:1184-91

[70]

Kanehisa M, Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000; 28:27-30

[71]

Mi H, Ebert D, Muruganujan A. et al. PANTHER version 16: a revised family classification, tree-based classification tool, enhancer regions and extensive API. Nucleic Acids Res. 2021; 49:D394-403

[72]

Thimm O, Bläsing O, Gibon Y. et al. Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004; 37:914-39

[73]

Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12:357-60

[74]

Danecek P, Bonfield JK, Liddle J. et al. Twelve years of SAMtools and BCFtools. GigaScience. 2021; 10:1-4

[75]

Li H, Handsaker B, Wysoker A. et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25:2078-9

[76]

Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014; 30:923-30

[77]

Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009; 10:57-63

[78]

Ballouz S, Weber M, Pavlidis P. et al. EGAD: ultra-fast functional analysis of gene networks. Bioinformatics. 2017; 33:612-4

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