UDP-glycosyltransferase PpUGT74F2 is involved in fruit immunity via modulating salicylic acid metabolism

Dan Jiang , Siyin Lin , Linfeng Xie , Miaojing Chen , Yanna Shi , Kunsong Chen , Xian Li , Boping Wu , Bo Zhang

Horticulture Research ›› 2025, Vol. 12 ›› Issue (6) : 49

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Horticulture Research ›› 2025, Vol. 12 ›› Issue (6) :49 DOI: 10.1093/hr/uhaf049
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UDP-glycosyltransferase PpUGT74F2 is involved in fruit immunity via modulating salicylic acid metabolism

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Abstract

Flesh fruits are essential for human health, but pathogen infection poses a threat to fruit production and postharvest storage. The hormone salicylic acid (SA) and its metabolites, such as sugar conjugates and methyl salicylate (MeSA), play a crucial role in regulating plant immune responses. However, the UDP-glycosyltransferases (UGTs) responsible for modulating SA metabolism in fruit have yet to be identified, and further investigation is needed to elucidate its involvement in fruit immune response. Here, we identified PpUGT74F2 as an enzyme with the highest transcription level in peach fruit, responsible for catalyzing the biosynthesis of SA glucoside (SAG), but not for MeSAG formation in fruit. Furthermore, infection of peach fruit with Monilinia fructicola, which causes brown rot disease, led to reduced expression of PpUGT74F2, resulting in a significant decrease in SAG content and an increase in MeSA levels. Transgenic tomatoes expressing heterologous PpUGT74F2 increased susceptibility to gray mold. Interestingly, overexpressing PpUGT74F2 did not affect SA levels but dramatically reduced MeSA levels in response to pathogen infection, accompanied by significantly reduced expression of pathogen-related (PR) genes in transgenic tomatoes. This study highlights that PpUGT74F2 acts as a negative regulatory factor for fruit immunity through a distinct mechanism not previously reported in plants.

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Dan Jiang, Siyin Lin, Linfeng Xie, Miaojing Chen, Yanna Shi, Kunsong Chen, Xian Li, Boping Wu, Bo Zhang. UDP-glycosyltransferase PpUGT74F2 is involved in fruit immunity via modulating salicylic acid metabolism. Horticulture Research, 2025, 12(6): 49 DOI:10.1093/hr/uhaf049

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Acknowledgements

This work was supported by Zhejiang Provincial Natural Science Foundation (LD22C150001) and Ningbo Key Research and Development Program (2022Z179). We want to thank Zhongjing Zhou (Central Laboratory, State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Zhejiang Academy of Agricultural Sciences) for the technical support in UPLC-QqQ-MS/MS analysis.

Author contributions

B.Z., B.W., and D.J. designed the experiments. D.J. performed most of the experiments and data analysis. S.L. participated in the experiment of peach fruit treatment. L.X. and B.W. detected the enzyme activity of recombinant proteins. M.C. and Y.S. took care of plants and provided fruit for analysis, K.C. and X.L. provided experimental instruments. B.W., D.J., and B.Z. prepared the manuscript. All authors have read and approved the final manuscript.

Data availability

RNA-Seq raw data can be found in the NCBI with accession number PRJNA576753 for peach samples at different development and ripening stages.

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Cesarino I. Killing me softly: a pathogen accelerates fruit ripen-ing and softening to cause disease. Plant Physiol. 2023; 191:21-3

[2]

Spoel SH, Dong XN. Salicylic acid in plant immunity and beyond. Plant Cell. 2024; 36:1451-64

[3]

Thompson AMG, Iancu CV, Neet KE. et al. Differences in salicylic acid glucose conjugations by UGT74F1 and UGT74F 2 from Ara-bidopsis thaliana. Sci Rep. 2017; 7:46629

[4]

Vicente MRS, Plasencia J. Salicylic acid beyond defence: its role in plant growth and development. JExp Bo.t 2011; 62: 3321-38

[5]

Nawrath C, Métraux JP. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell. 1999; 11:1393-404

[6]

Breen S, Williams SJ, Outram M. et al. Emerging insights into the functions of pathogenesis-related protein 1. Trends Plant Sci. 2017; 22:871-9

[7]

Pieterse CMJ, Van der Does D, Zamioudis C. et al. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012; 28: 489-521

[8]

Bauer S, Mekonnen DW, Hartmann M. et al. UGT76B1, a promis-cuous hub of small molecule-based immune signaling, gluco-sylates N-hydroxypipecolic acid, and balances plant immunity. Plant Cell. 2021; 33:714-34

[9]

Mohnike L, Rekhter D, Huang W. et al. The glycosyltransferase UGT76B1 modulates N-hydroxy-pipecolic acid homeostasis and plant immunity. Plant Cell. 2021; 33:735-49.

[10]

Ortega MA, Celoy RM, Chacon F. et al. Altering cold-regulated gene expression decouples the salicylic acid-growth trade-off in Arabidopsis. Plant Cell. 2024; 36:4293-308.

[11]

Liang BB, Bai YJ, Zang CQ. et al. Overexpression of the first peanut-susceptible gene, AhS5H1 or AhS5H2, enhanced susceptibility to Pst DC3000 in Arabidopsis. Int J Mol Sci. 2023; 24:14210

[12]

Huang JL, Gu M, Lai ZB. et al. Functional analysis of the Arabidop-sis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol. 2010; 153:1526-38

[13]

Lefevere H, Bauters L, Gheysen G. Salicylic acid biosynthesis in plants. Front Plant Sci. 2020; 11:338

[14]

Ding PT, Ding YL. Stories of salicylic acid: a plant defense hormone. Trends Plant Sci. 2020; 25:549-65.

[15]

Vaca E, Behrens C, Theccanat T. et al. Mechanistic differences in the uptake of salicylic acid glucose conjugates by vacuolar membrane-enriched vesicles isolated from Arabidopsis thaliana. Physiol Plant. 2017; 161:322-38

[16]

Dean JV, Delaney SP. Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol Plant. 2008; 132:417-25

[17]

Noutoshi Y, Okazaki M, Kida T. et al. Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic acid glucosyltransferases in Arabidop-sis. Plant Cell. 2012; 24:3795-804

[18]

Boachon B, Gamir J, Pastor V. et al. Role of two UDP-glycosyltransferases from the L group of arabidopsis in resis-tance against Pseudomonas syringae. Eur J Plant Pathol. 2014; 139: 707-20

[19]

Song JT, Koo YJ, Seo HS. et al. Overexpression of AtSGT1, an Arabidopsis salicylic acid glucosyltransferase, leads to increased susceptibility to Pseudomonas syringae. Phytochemistry. 2008; 69: 1128-34

[20]

Park HJ, Kwon CS, Woo J-Y. et al. Suppression of UDP-glycosyltransferase-coding Arabidopsis thaliana UGT74E2 gene expression leads to increased resistance to Psuedomonas syringae pv. Tomato DC3000 infection. Plant Pathol. 2011; 27: 170-82

[21]

Hu YQ, Zhang MT, Lu MQ. et al. Salicylic acid carboxyl gluco-syltransferase UGT87E7 regulates disease resistance in Camellia sinensis. Plant Physiol. 2022; 188:1507-20

[22]

Zubieta C, Ross JR, Koscheski P. et al. Structural basis for sub-strate recognition in the salicylic acid carboxyl methyltrans-ferase family. Plant Cell. 2003; 15:1704-16

[23]

Tieman D, Zeigler M, Schmelz E. et al. Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J. 2010; 62: 113-23

[24]

Park SW, Kaimoyo E, Kumar D. et al. Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science. 2007; 318:113-6.

[25]

Yi HS, Heil M, Adame-Alvarez RM. et al. Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol. 2009; 151:2152-61

[26]

Wenig M, Ghirardo A, Sales JH. et al. Systemic acquired resis-tance networks amplify airborne defense cues. Nat Commun. 2019; 10:3813

[27]

Gong Q, Wang YJ, He LF. et al. Molecular basis of methyl-salicylate-mediated plant airborne defence. Nature. 2023; 622: 139-48

[28]

Zhang XH, Min DD, Li FJ. et al. Synergistic effects of L-arginine and methyl salicylate on alleviating postharvest disease caused by Botrysis cinerea in tomato fruit. J Agric Food Chem. 2017; 65: 4890-6

[29]

Chen L, Wang WS, Wang T. et al. Methyl salicylate glucosylation regulates plant defense signaling and systemic acquired resis-tance. Plant Physiol. 2019; 180:2167-81.

[30]

Fanesi B, D’ortenzio ALD, Kuhalskaya A. et al. Identification of volatile organic compounds as markers to detect Monilinia fructicola infection in fresh peaches. Postharvest Biol Technol. 2023; 206:112581

[31]

Zhang C, Duan W, Chen K. et al. Transcriptome and methylome analysis reveals effects of ripening on and off the vine on flavor quality of tomato fruit. Postharvest Biol Technol. 2020; 162: 111096

[32]

Wang P, Wu T, Cheng Y. et al. The phytocytokine systemin enhances postharvest tomato fruit resistance to Botrytis cinerea. Postharvest Biol Technol. 2024; 210:112738

[33]

Wu BP, Gao LX, 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.

[34]

Wu BP, Cao XM, Liu HR. et al. UDP-glucosyltransferase PpUGT85A2 controls volatile glycosylation in peach. JExp Bot. 2019; 70:925-36

[35]

Liu SL, Wu J, Zhang P. et al. Response of phytohormones and correlation of SAR signal pathway genes to the different resis-tance levels of grapevine against Plasmopara viticola infection. Plant Physiol Biochem. 2016; 107:56-66

[36]

Vlot AC, Dempsey DA, Klessig DF. Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol. 2009; 47: 177-206

[37]

Sun YF, Ji K, Liang B. et al. Suppressing ABA uridine diphosphate glucosyltransferase (SlUGT75C1) alters fruit ripening and the stress response in tomato. Plant J. 2017; 91:574-89

[38]

Huang XX, Zhu GQ, Liu Q. et al. Modulation of plant salicylic acid-associated immune responses via glycosylation of dihy-droxybenzoic acids. Plant Physiol. 2018; 176:3103-19

[39]

Shulaev V, Silverman P, Raskin I. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature. 1997; 385: 718-21

[40]

Liu PP, Von Dahl CC, Klessig DF. The extent to which methyl salicylate is required for signaling systemic acquired resistance is dependent on exposure to light after infection. Plant Physiol. 2011; 157:2216-26

[41]

Dempsey DA, Klessig DF. SOS—too many signals for systemic acquired resistance? Trends Plant Sci. 2012; 17:538-45

[42]

Fu ZQ, Dong X. Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol. 2013; 64:839-63

[43]

Zeier J. Metabolic regulation of systemic acquired resistance. Curr Opin Plant Biol. 2021; 62:102050

[44]

Jiang D, Han QY, Su YK. et al. Glycoside hydrolase PpGH28BG1 modulates benzaldehyde metabolism and enhances fruit aroma and immune responses in peach. Plant Physiol. 2024; 196:1444-59

[45]

Zhang B, Chen KS, Bowen J. et al. Differential expression within the LOX gene family in ripening kiwifruit. JExp Bot. 2006; 57: 3825-36

[46]

Zhang B, Tieman DM, Jiao C. et al. Chilling-induced tomato flavor loss is associated with altered volatile synthesis and transient changes in DNA methylation. Proc Natl Acad Sci USA. 2016; 113: 12580-5.

[47]

Wei CY, Liu HR, Cao XM. et al. Synthesis of flavour-related linalool is regulated by PpbHLH1 and associated with changes in DNA methylation during peach fruit ripening. Plant Biotechnol J. 2021; 19:2082-96

[48]

Cao X, Li X, Su Y. et al. Transcription factor PpNAC1 and DNA demethylase PpDML1 synergistically regulate peach fruit ripen-ing. Plant Physiol. 2024; 194:2049-68

[49]

Yang C, Li ZH, Cao XM. et al. Genome-wide analysis of calmodulin binding transcription activator (CAMTA) gene family in peach (Prunus persica L. Batsch) and ectopic expression of PpCAMTA1 in Arabidopsis camta2,3 mutant restore plant development. Int J Mol Sci. 2022; 23:10500

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