MdCSN5-MdIAMT module promotes anthocyanin accumulation by regulating IAA homeostasis in apple

Jiahu Zhang , Chen Wang , Haibo Wang , Ping He , Yuansheng Chang , Sen Wang , Wenyan Zheng , Nan Wang , Yongxu Wang , Qi Zou , Linguang Li , Xuesen Chen , Xiaowen He

Horticulture Research ›› 2026, Vol. 13 ›› Issue (2) : 290

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Horticulture Research ›› 2026, Vol. 13 ›› Issue (2) :290 DOI: 10.1093/hr/uhaf290
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MdCSN5-MdIAMT module promotes anthocyanin accumulation by regulating IAA homeostasis in apple
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Abstract

The apple anthocyanin content is an important trait in apple breeding. Auxin, as an important plant hormone, plays significant roles in regulating the biosynthesis of anthocyanins. However, the molecular mechanism of how plants regulate auxin content and activity to affect anthocyanin accumulation remains unclear. In this study, through fruit anthocyanin content analysis and transcriptome sequencing of the hybrids derived from ‘Golden Delicious’ and ‘Fuji Nagafu No. 2’ crosses, a key gene for regulating apple anthocyanin accumulation, indole-3-acetic acid (IAA) methyltransferase (MdIAMT), was identified. Functional analyses showed that the apple calli and peel overexpressing MdIAMT accumulated more anthocyanin than that in Vec by regulating IAA homeostasis. Yeast two-hybrid assays, luciferase complementation imaging assays and co-immunoprecipitation assays revealed that MdCSN5, an important protein in light signal transduction, interacts with MdIAMT. More importantly, further research showed that the MdCSN5-MdIAMT module affected auxin signal transduction pathway by regulating IAA homeostasis, thus promoting anthocyanin accumulation. In summary, our findings elucidate a novel mechanism by which auxin-regulated anthocyanin accumulation via MdCSN5-MdIAMT module, deepening our knowledge of plant hormone signaling in anthocyanin biosynthesis.

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Jiahu Zhang, Chen Wang, Haibo Wang, Ping He, Yuansheng Chang, Sen Wang, Wenyan Zheng, Nan Wang, Yongxu Wang, Qi Zou, Linguang Li, Xuesen Chen, Xiaowen He. MdCSN5-MdIAMT module promotes anthocyanin accumulation by regulating IAA homeostasis in apple. Horticulture Research, 2026, 13(2): 290 DOI:10.1093/hr/uhaf290

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Acknowledgements

This work was financially supported by the Key Research and Development Program of Shandong Province (2023LZGCQY009), the Research and Innovation Program Youth Project of Shandong Institute of Pomology (2023GSKY02), the Shandong Provincial Postdoctoral Science Foundation (SDCX-ZG-202202030), and the Earmarked Fund for China Agriculture Research System (CARS-27).

Author Contributions

C.W. and X.H. designed the research. J.Z. and H.W. performed most of the research and acquired the data, with the assistance of P.H., Y.C., S.W., W.Z., N.W., Y.W., Q.Z., L.L., P.W., and X.C. C.W., X.H., and J.Z. analyzed the data and wrote the paper.

Data availability statement

The data underlying this article are available in the article and in its online supplementary material.

Conflicts of interest statement

The authors declare no competing interests.

Supplementary material

Supplementary material is available at Horticulture Research online.

References

[1]

Gao HN, Jiang H, Cui JY. et al. Review: the effects of hormones and environmental factors on anthocyanin biosynthesis in apple. Plant Sci. 2021; 312:111024

[2]

Liu WJ, Mei ZX, Yu L. et al. The ABA-induced NAC transcription factor MdNAC1 interacts with a bZIP-type transcription factor to promote anthocyanin synthesis in red-fleshed apples. Hor-tic Res. 2023;10:uhad049

[3]

Bai YX, Shi K, Shan DQ. et al. The WRKY17-WRKY50 complex modulates anthocyanin biosynthesis to improve drought tol-erance in apple. Plant Sci. 2024; 340:111965

[4]

Jiang H, Zhou LJ, Gao HN. et al. The transcription factor MdMYB2 influences cold tolerance and anthocyanin accumu-lation by activating SUMO E3 ligase MdSIZ1 in apple. Plant Physiol. 2022; 189:2044-60

[5]

Gonzalez A, Zhao MZ, Leavitt JM. et al. Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 2008; 53:814-27

[6]

Fang HC, Dong YH, Yue XX. et al. The B-box zinc finger protein MdBBX20 integrates anthocyanin accumulation in response to ultraviolet radiation and low temperature. Plant Cell Env-iron. 2019; 42:2090-104

[7]

Araguirang GE, Richter AS. Activation of anthocyanin biosyn-thesis in high light - what is the initial signal? New Phytol. 2022; 236:2037-43

[8]

Zhang LZ, Zhang JT, Wei B. et al. Transcription factor MdNAC33 is involved in ALA-induced anthocyanin accumula-tion in apples. Plant Sci. 2024; 339:111949

[9]

Han SN, Liu YX, Bao A. et al. OsCSN1 regulates the growth of rice seedlings through the GA signaling pathway in blue light. J Plant Physiol. 2023; 280:153904

[10]

Dohmann EMN, Kuhnle C, Schwechheimer C. Loss of the CON-STITUTIVE PHOTOMORPHOGENIC9 signalosome subunit 5 is sufficient to cause the cop/det/fus mutant phenotype in Ara-bidopsis. Plant Cell. 2005; 17:1967-78

[11]

Wei S, Li X, Gruber MY. et al. COP9 signalosome subunit 5A affects phenylpropanoid metabolism, trichome formation and transcription of key genes of a regulatory tri-protein com-plex in Arabidopsis. BMC Plant Biol. 2018; 18:134

[12]

Mo XH, Zhang MK, Zhang ZY. et al. Phosphate (Pi) starvation up-regulated GmCSN5A/B participates in anthocyanin syn-thesis in soybean (Glycine max) dependent on Pi availability. Int J Mol Sci. 2021; 22:12348

[13]

Lashley A, Miller R, Provenzano S. et al. Functional diversifi-cation and structural origins of plant natural product methyl-transferases. Molecules. 2022; 28:43

[14]

Zhuge XL, Du X, Xiu ZJ. et al. Discovery of specific catalytic activity toward IAA/FA by LaSABATHs based on genome-wide phylogenetic and enzymatic analysis of SABATH gene family from Larix kaempferi. Int J Biol Macromol. 2023; 225:1562-74

[15]

Ross JR, Nam KH, D’Auria JC. et al. S-Adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys. 1999; 367:9-16

[16]

Yang Y, Xu R, Ma CJ. et al. Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiol. 2008; 147:1034-45

[17]

Qin GJ, Gu HY, Zhao YD. et al. An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell. 2005; 17:2693-704

[18]

Zhao N, Boyle B, Duval I. et al. SABATH methyltrans-ferases from white spruce (Picea glauca): gene cloning, func-tional characterization and structural analysis. Tree Physiol. 2009; 29:947-57

[19]

Li BJ, Bao RX, Shi YN. et al. Auxin response factors: important keys for understanding regulatory mechanisms of fleshy fruit development and ripening. Hortic Res. 2024;11:uhae209

[20]

Li Z, Ahammed GJ. Hormonal regulation of anthocyanin biosynthesis for improved stress tolerance in plants. Plant Physiol Biochem. 2023; 201:107835

[21]

Wang YC, Wang N, Xu HF. et al. Auxin regulates anthocyanin biosynthesis through the Aux/IAA-ARF signaling pathway in apple. Hortic Res. 2018; 5:59

[22]

Wang S, Wang T, Li QQ. et al. Phosphorylation of MdERF17 by MdMPK4 promotes apple fruit peel degreening during light/-dark transitions. Plant Cell. 2022b; 34:1980-2000

[23]

Chen CJ, Wu Y, Li JW. et al. TBtools-II: a “one for all, all for one” bioinformatics platform for biological big-data mining. Mol Plant. 2023; 16:1733-42

[24]

D’Auria JC. Acyltransferases in plants: a good time to be BAHD. Curr Opin Plant Biol. 2006; 9:331-40

[25]

Han YP, Vimolmangkang S, Soria-Guerra RE. et al. Ectopic expression of apple F3’H genes contributes to anthocyanin accumulation in the Arabidopsis tt7 mutant grown under nitrogen stress. Plant Physiol. 2010; 153:806-20

[26]

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

[27]

Muhammad N, Luo Z, Yang M. et al. The joint role of the late anthocyanin biosynthetic UFGT-encoding genes in the flowers and fruits coloration of horticultural plants. Sci Hortic. 2022; 301:111110

[28]

Liu HM, Liu ZJ, Wu Y. et al. Regulatory mechanisms of antho-cyanin biosynthesis in apple and pear. Int J Mol Sci. 2021; 22: 8441

[29]

Zhao L, Chen JC, Zhang ZH. et al. Deciphering the transcrip-tional regulatory network governing starch and storage pro-tein biosynthesis in wheat for breeding improvement. Adv Sci (Weinh). 2024; 11:2401383

[30]

Sun CM, Wu J, Zhou XY. et al. Homoeologous exchanges con-tribute to branch angle variations in rapeseed: insights from transcriptome, QTL-seq and gene functional analysis. Plant Biotechnol J. 2024; 22:1636-48

[31]

Ding TY, Zhang RP, Zhang HT. et al. Identification of gene co-expression networks and key genes regulating flavonoid accumulation in apple ( Malus × domestica) fruit skin. Plant Sci. 2021; 304:110747

[32]

Bu YF, Wang S, Li CZ. et al. Transcriptome analysis of apples in high-temperature treatments reveals a role of MdLBD37 in the inhibition of anthocyanin accumulation. Int J Mol Sci. 2022; 23:3766

[33]

An JP, Zhang XW, Liu YJ. et al. ABI5 regulates ABA-induced anthocyanin biosynthesis by modulating the MYB1-bHLH3 complex in apple. J Exp Bot. 2021; 72:1460-72

[34]

Ji XH, Wang YT, Zhang R. et al. Effect of auxin, cytokinin and nitrogen on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell Tissue Organ Cult. 2015; 120: 325-37

[35]

Moro L, Hassimotto NMA, Purgatto E. Postharvest auxin and methyl jasmonate effect on anthocyanin biosynthesis in red raspberry (Rubus idaeus L.). J Plant Growth Regul. 2017; 36:773-82

[36]

Li HL, Liu ZY, Wang XN. et al. E3 ubiquitin ligases SINA4 and SINA11 regulate anthocyanin biosynthesis by targeting the IAA29-ARF5-1-ERF3 module in apple. Plant Cell Environ. 2023; 46:3902-18

[37]

Takos AM, Jaffé FW, Jacob SR. et al. Light-induced expres-sion of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol. 2006; 142:1216-32

[38]

Yue YC, Zhang XH, Wang L. et al. Identification and charac-terization of jasmonic acid methyltransferase involved in the formation of floral methyl jasmonate in Hedychium coronar-ium. Plants (Basel). 2023; 13:8

[39]

Luo D, Xiong C, Lin AH. et al. SlBBX20 interacts with the COP9 signalosome subunit SlCSN5-2 to regulate anthocyanin biosynthesis by activating SlDFR expression in tomato. Hortic Res. 2021; 8:163

[40]

Ye LX, Bai FX, Zhang L. et al. Transcriptome and metabolome analyses of anthocyanin biosynthesis in post-harvest fruits of a full red-type kiwifruit (Actinidia arguta) ‘Jinhongguan’. Front Plant Sci. 2023; 14:1280970

[41]

Liao ZK, Liu XJ, Zheng J. et al. A multifunctional true caffeoyl coenzyme A O-methyltransferase enzyme participates in the biosynthesis of polymethoxylated flavones in citrus. Plant Physiol. 2023; 192:2049-66

[42]

Wang LJ, Guo DZ, Zhao GD. et al. Group IIc WRKY transcrip-tion factors regulate cotton resistance to Fusarium oxysporum by promoting GhMKK2-mediated flavonoid biosynthesis. New Phytol. 2022a; 236:249-65

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