Evolutionary dynamics and functional divergence of the UDP-glycosyltransferases gene family revealed by a pangenome-wide analysis in tomato

Abstract

UDP-dependent glycosyltransferases (UGTs) play a critical role in producing glycosylated metabolites that mediate plant-environment interactions. Recent studies have examined the role of UGT genes across various plant genomes. However, the evolutionary history and functional divergence of the UGT pan-gene family in the genus Solanum have not yet been explored. This study integrated data from 61 tomatoes and 9 representative genomes, ranging from algae to angiosperms, to identify 12 073 genes. The phylogeny of the UGT gene family reveals a clear evolutionary trajectory from unicellular algae to ferns, mosses, gymnosperms, and angiosperms. The study identified a significant number of tomato-specific UGT genes and explored the expansions of UGT73 and UGT85 subfamilies. The entire UGT genes (10 769) in tomato were classified into 118 orthologous gene groups, including 58 core, 31 softcore, 10 dispensable, 19 private orthologous gene groups, and the core groups contained 7811 genes, representing 72.53% of the total UGT genes. Analysis of gene family expansion revealed that whole-genome triplication and tandem duplication events play significant roles in the expansion of the UGT gene family. Selection pressure analysis revealed that the UGT genes experienced purifying selection in the genus Solanum. Additionally, expression profiles of some UGT genes in different tissues demonstrated expression divergence of multicopy genes across different UGT subfamilies due to the increase in gene dosage. Subcellular localization prediction revealed that most genes are localized in the chloroplast. These findings provide critical insights into the evolution and function of the UGT genes in tomato, laying a foundation for further exploration in adaptive evolution.

Acknowledgments

This work was financially supported in part by grants from the Key Research and Development Program of Zhejiang (2024SSYS0099) and the Project of Xianghu Laboratory (2023C1S02001 and 2023C1S01002).

Author contributions

J.Y. and S.X. conceived this project. M.H. analyzed the data and prepared the initial manuscript. M.H., P.Z., N.L., Q.C., Y.L., X.T., and B.H. performed data collection and analysis. J.Y. and M.H. revised the manuscript. All authors read and approved the final manuscript.

Data availability

All the data were obtained from public databases, with detailed information provided in the Materials and methods.

Conflict of interest statement

None declared.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1] Roda F, Walter GM, Nipper R. et al. Genomic clustering of adap-tive loci during parallel evolution of an Australian wildflower. Mol Ecol. 2017; 26:3687-99

[2] Lamichhaney S, Fuentes-Pardo AP, Rafati N. et al. Parallel adap-tive evolution of geographically distant herring populations on both sides of the North Atlantic Ocean. Proc Natl Acad Sci U S A. 2017;114:E3452-61

[3] Herold S, Kuhn M, Bonin MV. et al. Donor cell leukemia: evidence for multiple preleukemic clones and parallel long term clonal evolution in donor and recipient. Leukemia. 2017; 31:1637-40

[4] Strasser R. Plant protein glycosylation. Glycobiology. 2016; 26: 926-39

[5] Mackenzie PI, Owens IS, Burchell B. et al. The UDP glycosyltrans-ferase gene superfamily: recommended nomenclature update based on evolutionary divergence. Pharmacogenetics. 1997; 7: 255-69

[6] Wilson AE, Tian L. Phylogenomic analysis of UDP-dependent gly-cosyltransferases provides insights into the evolutionary land-scape of glycosylation in plant metabolism. Plant J. 2019; 100: 1273-88

[7] Caputi L, Malnoy M, Goremykin V. et al. A genome-wide phy-logenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J. 2012; 69:1030-42

[8] He Y, Ahmad D, Zhang X. et al. Genome-wide analysis of family-1 UDP glycosyltransferases (UGT) and identification of UGT genes for FHB resistance in wheat (Triticum aestivum L.). BMC Plant Biol. 2018; 18:67

[9] Sun YG, Wang B, Jin SH. et al. Ectopic expression of Arabidopsis glycosyltransferase UGT85A5 enhances salt stress tolerance in tobacco. PLoS One. 2013; 8:e59924

[10] Langlois-Meurinne M, Gachon CM, Saindrenan P. Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiol. 2005; 139:1890-901

[11] Yonekura-Sakakibara K, Hanada K. An evolutionary view of functional diversity in family 1 glycosyltransferases. Plant J. 2011; 66:182-93

[12] Barvkar VT, Pardeshi VC, Kale SM. et al. Phylogenomic analysis of UDP glycosyltransferase 1 multigene family in Linum usitatis-simum identified genes with varied expression patterns. BMC Genomics. 2012; 13:175

[13] Chen Y, Fu M, Li H. et al. Genome-wide characterization of the UDP-glycosyltransferase gene family reveals their potential roles in leaf senescence in cotton. Int J Biol Macromol. 2022; 222: 2648-60

[14] Li Y, Li P, Wang Y. et al. Genome-wide identification and phylo-genetic analysis of Family-1 UDP glycosyltransferases in maize (Zea mays). Planta. 2014; 239:1265-79

[15] Wu B, Gao L, Gao J. et al. Genome-wide identification, expres-sion patterns, and functional analysis of UDP glycosyltrans-ferase family in peach (Prunus persica L. Batsch). Front Plant Sci. 2017; 8:389

[16] Marks RA, Hotaling S, Frandsen PB. et al. Representation and participation across 20 years of plant genome sequencing. Nat Plants. 2021; 7:1571-8

[17] Hu H, Wang J, Nie S. et al. Plant pangenomics, current practice and future direction. Agric Commun. 2024; 2:100039

[18] Swanson-Wagner RA, Eichten SR, Kumari S. et al. Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res. 2010; 20:1689-99

[19] He Q, Tang S, Zhi H. et al. A graph-based genome and pan-genome variation of the model plant Setaria. Nat Genet. 2023; 55: 1232-42

[20] Zhao X, Yu J, Chanda B. et al. Genomic and pangenomic anal-yses provide insights into the population history and genomic diversification of bottle gourd. New Phytol. 2024; 242:2285-300

[21] Tomato Genome Consortium x. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012; 485: 635-41

[22] Project AG, Albert VA, Barbazuk WB. et al. The Amborella genome and the evolution of flowering plants. Science. 2013; 342:1241089

[23] The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007; 449: 463-7

[24] Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000; 408:796-815

[25] Boris K, Ryzhova N, Kochieva E. Identification and characteri-zation of intraspecific variability of the sucrose synthase gene Sus4 of potato (Solanum tuberosum). Russ J Genet. 2011; 47:168-75

[26] Lin T, Zhu G, Zhang J. et al. Genomic analyses provide insights into the history of tomato breeding. Nat Genet. 2014; 46:1220-6

[27] Pesaresi P, Mizzotti C, Colombo M. et al. Genetic regulation and structural changes during tomato fruit development and ripening. Front Plant Sci. 2014; 5:124

[28] Blanca J, Cañizares J, Cordero L. et al. Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS One. 2012; 7:e48198

[29] Zuriaga E, Blanca J, Nuez F. Classification and phylogenetic relationships in Solanum section Lycopersicon based on AFLP and two nuclear gene sequences. Genet Resour Crop Evol. 2009; 56: 663-78

[30] Rick CM, Fobes JF. Allozyme variation in the cultivated tomato and closely related species. Bull Torrey Bot Club. 1975; 102:376-84

[31] Jenkins JA. The origin of the cultivated tomato. Econ Bot. 1948; 2: 379-92

[32] Ross J, Li Y, Lim E-K. et al. Higher plant glycosyltransferases. Genome Biol. 2001;2:REVIEWS3004

[33] Conant GC, Birchler JA, Pires JC. Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr Opin Plant Biol. 2014; 19: 91-8

[34] Salami M, Heidari B, Batley J. et al. Integration of genome-wide association studies, metabolomics, and transcriptomics reveals phenolic acid-and flavonoid-associated genes and their regu-latory elements under drought stress in rapeseed flowers. Front Plant Sci. 2024; 14:1249142

[35] Huo H, Li J, Tian L. et al. Multi-omics analysis reveals the role of UGT72 family genes in arbutin biosynthesis in Pyrus and evo-lution driven by whole genome duplication. Int J Biol Macromol. 2025; 291:139005

[36] MaY, ZhaoS, MaX. et al. A high temperature responsive UDP-glucosyltransferase gene OsUGT72F1 enhances heat tolerance in rice and Arabidopsis. Plant Cell Rep. 2025; 44:48

[37] Yin Q, Shen G, Chang Z. et al. Involvement of three putative glucosyltransferases from the UGT72 family in flavonol glu-coside/rhamnoside biosynthesis in Lotus japonicus seeds. JExp Bot. 2016;68:erw420-612

[38] Guan H, Zhang Y, Li J. et al. Analysis of the UDP-glucosyltransferase (UGT) gene family and its functional involvement in drought and salt stress tolerance in Phoebe bournei. Plants (Basel). 2024; 13:722

[39] Yu JY, Hu F, Dossa K. et al. Genome-wide analysis of UDP-glycosyltransferase super family in Brassica rapa and Brassica oleracea reveals its evolutionary history and functional charac-terization. BMC Genomics. 2017; 18:474

[40] Finn RD, Clements J, Eddy SR. HMMER web server: interac-tive sequence similarity searching. Nucleic Acids Res. 2011;39: W29-37

[41] Katoh K, Misawa K, Kuma K. et al. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30:3059-66

[42] Jones P, Binns D, Chang HY. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014; 30: 1236-40

[43] Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. TrimAl: a tool for automated alignment trimming in large-scale phyloge-netic analyses. Bioinformatics. 2009; 25:1972-3

[44] Lanfear R, von Haeseler A, Woodhams MD. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020; 37:1530-4

[45] Wang Y, Tang H, Debarry JD. et al. MCScanX: a toolkit for detec-tion and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40:e49

[46] Horton P, Park KJ, Obayashi T. et al. WoLF PSORT: protein local-ization predictor. Nucleic Acids Res. 2007;35:W585-7