Transcriptomic analysis uncovers the red leaf coloration mechanism in Euonymus sacrosancta Koidz

Xinyan Gao , Zhongjia Yuan , Haoda Liu , Yang Liu , Ying Wang , Lianfeng Xu , Huihui Zhang , Xuemei Liu

Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) : 74

PDF
Journal of Forestry Research ›› 2025, Vol. 36 ›› Issue (1) :74 DOI: 10.1007/s11676-025-01873-4
Original Paper
research-article

Transcriptomic analysis uncovers the red leaf coloration mechanism in Euonymus sacrosancta Koidz

Author information +
History +
PDF

Abstract

Two leaf color variants red-leaf (R-type) and common-leaf (G-type) of Euonymus sacrosancta Koidz., were employed as experimental materials to elucidate the molecular mechanisms underlying chromatic transition. Physiological profiling identified anthocyanins and flavonoids as the predominant pigments responsible for the red foliar phenotype, which exhibited reduced chlorophyll and carotenoid accumulation but elevated soluble sugars and proteins. Comparative transcriptomic analysis revealed that differentially expressed genes (DEGs) between R-type and G-type were significantly enriched in flavonoid biosynthesis and carotenoid metabolism pathways. The up-regulation of 22 key genes of anthocyanin synthesis (e.g., CHS, CHI, LAR, LDOX and UFGT) in R-type may lead to the phenotype of red leaves through the increase of anthocyanin accumulation. The downregulated expression of 13 carotenoid synthesis-related genes (e.g., PSY, PDS and VDE) and 6 carotenoid degradation genes (e.g., ABA2, CYP707A and NCED) may lead to lower carotenoid content in R-type compared to G-type. Combined with weighted gene co-expression network analysis (WGCNA), five candidate genes (EsLAR, EsLDOX, EsPDS, EsCYP707A and EsABA2) were screened from two modules highly correlated with anthocyanin content in E. sacrosancta leaves. These genes may play key regulatory roles in leaf coloration and could serve as candidate genetic resources for leaf color improvement in E. sacrosancta. Additionally, transcription factors such as C2H2s, C3Hs, and WRKYs were identified as potential regulators in the formation of R-type in E. sacrosancta. This study provides the first systematic elucidation of the transcriptional regulatory network governing red-leaf formation in E. sacrosancta, establishing a critical theoretical foundation for molecular breeding in ornamental plants.

Keywords

Euonymus sacrosancta / Transcriptome / Leaf coloration / Anthocyanin / Carotenoids

Cite this article

Download citation ▾
Xinyan Gao, Zhongjia Yuan, Haoda Liu, Yang Liu, Ying Wang, Lianfeng Xu, Huihui Zhang, Xuemei Liu. Transcriptomic analysis uncovers the red leaf coloration mechanism in Euonymus sacrosancta Koidz. Journal of Forestry Research, 2025, 36(1): 74 DOI:10.1007/s11676-025-01873-4

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Alappat B, Alappat J. Anthocyanin pigments: beyond aesthetics. Molecules, 2020, 25(23): 5500

[2]

Bai YX, Shi K, Shan DQ, Wang CY, Yan TC, Hu ZH, Zheng XD, Zhang T, Song HD, Li RX, Zhao YX, Deng Q, Dai CJ, Zhou ZY, Guo Y, Kong J. The WRKY17-WRKY50 complex modulates anthocyanin biosynthesis to improve drought tolerance in apple. Plant Sci, 2024, 340 111965

[3]

Cappellini F, Marinelli A, Toccaceli M, Tonelli C, Petroni K. Anthocyanins: from mechanisms of regulation in plants to health benefits in foods. Front Plant Sci, 2021, 12 748049

[4]

Cheng J, Liao L, Zhou H, Gu C, Wang L, Han YP. A small indel mutation in an anthocyanin transporter causes variegated colouration of peach flowers. J Exp Bot, 2015, 66(227227-7239

[5]

Chen JH, Liu YH, Zhao HB, Xu JM, Zheng P, Liu SQ, Sun BM. CsHY5 regulates light-induced anthocyanin accumulation in Camellia sinensis. Int J Mol Sci, 2025, 26(7): 3253

[6]

Chen X, Li MH, Ni J, Hou JY, Shu X, Zhao WW, Su PF, Wang DC, Afzal Shah F, Huang SW, Liu ZJ, Wu LF. The R2R3-MYB transcription factor SsMYB1 positively regulates anthocyanin biosynthesis and determines leaf color in Chinese tallow (Sapium sebiferum Roxb). Ind Crops Products, 2021, 164 113335

[7]

Chen LH, Hu B, Qin YH, Hu GB, Zhao JY. Advance of the negative regulation of anthocyanin biosynthesis by MYB transcription factors. Plant Physiol Biochem, 2019, 136: 178-187

[8]

Chiou CY, Pan HA, Chuang YN, Yeh KW. Differential expression of carotenoid-related genes determines diversified carotenoid coloration in floral tissues of Oncidium cultivars. Planta, 2010, 232(4937-948

[9]

Dong NQ, Lin HX. Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol, 2021, 63(1): 180-209

[10]

Feng SQ, Chen XS, Zhang YM, Wang YL, Song Y, Chen XL, Li XG, Min L, Jin L, Wang QZ, Liu MY. Differential expression of proteins in red pear following fruit bagging treatment. Protein J, 2011, 30(3): 194-200

[11]

Ge W, Wang XX, Li JY, Zhu WP, Cui JT, Zhang KZ. Regulatory mechanisms of leaf color change in Acer pictum subsp. mono. Genome, 2019, 62(12): 793-805

[12]

Han YJ, Wang XH, Chen WC, Dong M, Yuan W, Liu X, Shang F. Differential expression of carotenoid-related genes determines diversified carotenoid coloration in flower petal of Osmanthus fragrans. Tree Genet Genom, 2014, 10(2): 329-338

[13]

Han Y, Vimolmangkang S, Soria-Guerra RE, Korban SS. Introduction of apple ANR genes into tobacco inhibits expression of both CHI and DFR genes in flowers, leading to loss of anthocyanin. J Exp Bot, 2012, 63(7): 2437-2447

[14]

Hara M, Oki K, Hoshino K, Kuboi T. Enhancement of anthocyanin biosynthesis by sugar in radish (Raphanus sativus) hypocotyl. Plant Sci, 2003, 164(2): 259-265

[15]

Heimler D, Vignolini P, Dini MG, Romani A. Rapid tests to assess the antioxidant activity of Phaseolus vulgaris L. dry beans. J Agric Food Chem, 2005, 53(8): 3053-3056

[16]

Huang J, Zhao X, Zhang Y, Chen Y, Zhang XM, Yi Y, Ju ZG, Sun W. Chalcone-synthase-encoding RdCHS1 is involved in flavonoid biosynthesis in Rhododendron delavayi. Molecules, 2024, 29(8): 1822

[17]

Hirschberg J. Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol, 2001, 4(3210-218

[18]

Li C, Wang CL, Cheng ZY, Li Y, Li WJ. Carotenoid biosynthesis genes LcLCYB, LcLCYE, and LcBCH from wolfberry confer increased carotenoid content and improved salt tolerance in tobacco. Sci Rep, 2024, 14(1): 10586

[19]

Li DD, Yang JL, Pak S, Zeng MZ, Sun JL, Yu S, He YT, Li CH. PuC3H35 confers drought tolerance by enhancing lignin and proanthocyanidin biosynthesis in the roots of Populus ussuriensis. New Phytol, 2022, 233(1390-408

[20]

Li H, Tian J, Yao YY, Zhang J, Song TT, Li KT, Yao YC. Identification of leucoanthocyanidin reductase and anthocyanidin reductase genes involved in proanthocyanidin biosynthesis in Malus crabapple plants. Plant Physiol Biochem, 2019, 139: 141-151

[21]

Li HR, Zhang Y, Li H, Yang YX, Dong Y, Sun CX, Zheng H, Tao JM. Comparative transcriptome analysis of leaf color in 'Shine Muscat' and 'ZhongShan-HongYu' hybrids. Sci Hortic, 2025, 339 113896

[22]

Li JW, Zhou P, Deng YJ, Hu ZH, Li XH, Chen X, Xiong AS, Zhuang J. Overexpressing CsPSY1 gene of tea plant, encoding a phytoene synthase, improves α-Carotene and β-Carotene contents in Carrot. Mol Biotechnol, 2024, 66(11): 3311-3322

[23]

Li PH, Dong Q, Ge SJ, He XZ, Verdier J, Li DQ, Zhao J. Metabolic engineering of proanthocyanidin production by repressing the isoflavone pathways and redirecting anthocyanidin precursor flux in legume. Plant Biotechnol J, 2016, 14(7): 1604-1618

[24]

Li SS, Li QZ, Tang L, Wen J. Pigment comparison and expression of chlorophyll metabolism genes in yellow and green Acerpalmatum Thunb. ex Murray leaves. Can J Plant Sci, 2017, 97(5): 1-9

[25]

Li YN (2014) A study on phylogeny and evolution of Euonymus L. (Celastraceae) in China. Dissertation, Beijing Forestry University (in Chinese)

[26]

Liao HS, Yang CC, Hsieh MH. Nitrogen deficiency- and sucrose-induced anthocyanin biosynthesis is modulated by HISTONE DEACETYLASE15 in Arabidopsis. J Exp Bot, 2022, 73(11): 3726-3742

[27]

Lin JX, Lai GT, Guo AL, He LY, Yang FX, Huang YJ, Che JM, Lai CC. Overexpression of LAR1 suppresses anthocyanin biosynthesis by enhancing catechin competition leading to promotion of proanthocyanidin pathway in Spine Grape (Vitis davidii) Cells. Int J Mol Sci, 2024, 25(22): 12087

[28]

Liu JX, Chiou CY, Shen CH, Chen PJ, Liu YC, Jian CD, Shen XL, Shen FQ, Yeh KW. RNA interference-based gene silencing of phytoene synthase impairs growth, carotenoids, and plastid phenotype in Oncidium hybrid orchid. Springer plus, 2014, 3: 478

[29]

Liu Y, Tikunov Y, Schouten RE, Marcelis LFM, Visser RGF, Bovy A. Anthocyanin biosynthesis and degradation mechanisms in Solanaceous vegetables: a review. Front Chem, 2018, 6: 52

[30]

Liu Q, Li SJ, Li TJ, Wei Q, Zhang Y. The characterization of R2R3-MYB genes in water lily nymphaea colorata reveals the involvement of NcMYB25 in regulating anthocyanin synthesis. Plants (Basel), 2024, 13(212990

[31]

Lo Piccolo E, Landi M, Pellegrini E, Agati G, Giordano C, Giordani T, Lorenzini G, Malorgio F, Massai R, Nali C, Rallo G, Remorini D, Vernieri P, Guidi L. Multiple consequences induced by epidermally-located anthocyanins in young, mature and senescent leaves of Prunus. Front Plant Sci, 2018, 9: 917

[32]

Luo JR, Duan JJ, Huo D, Shi QQ, Niu LX, Zhang YL. Transcriptomic analysis reveals transcription factors related to leaf anthocyanin biosynthesis in Paeonia qiui. Molecules, 2017, 22(122186

[33]

Mackon E, Jeazet Dongho Epse Mackon GC, Ma Y, Haneef Kashif M, Ali N, Usman B, Liu PQ. Recent insights into anthocyanin pigmentation, synthesis, trafficking, and regulatory mechanisms in Rice (Oryzasativa L.) Caryopsis. Biomolecules, 2021, 11(3394

[34]

Mao WW, Han Y, Chen YT, Sun MZ, Feng QQ, Li L, Liu LP, Zhang KK, Wei LZ, Han ZH, Li BB. Low temperature inhibits anthocyanin accumulation in strawberry fruit by activating FvMAPK3-induced phosphorylation of FvMYB10 and degradation of Chalcone Synthase 1. Plant Cell, 2022, 34(41226-1249

[35]

Mei H, Zhang XT, Zhao FK, Ruan RX, Fu QJ. Integrated metabolome and transcriptome analysis provides insight into the leaf color change of Cymbidium ensifolium. Acta Physiol Plant, 2024, 46: 50

[36]

Nakatsuka T, Suzuki T, Harada K, Kobayashi Y, Dohra H, Ohno H. Floral organ- and temperature-dependent regulation of anthocyanin biosynthesis in Cymbidium hybrid flowers. Plant Sci, 2019, 287 110173

[37]

Neta-Sharir I, Shoseyov O, Weiss D. Sugars enhance the expression of gibberellin-induced genes in developing petunia flowers. Physiol Plant, 2000, 109(2196-202

[38]

Payyavula RS, Singh RK, Navarre DA. Transcription factors, sucrose, and sucrose metabolic genes interact to regulate potato phenylpropanoid metabolism. J Exp Bot, 2013, 64(165115-5131

[39]

Sahu A, Singh R, Verma PK. Plant BBR/BPC transcription factors: unlocking multilayered regulation in development, stress and immunity. Planta, 2023, 258(2): 31

[40]

Shah FA, Chen Z, Kamal KA, Zhao Y, Zhu ZY, Chen JH, Ren J. ArMYB89 and ArCOP1 interaction modulates anthocyanin biosynthesis in Acer rubrum leaves under low-temperature conditions. Plant J, 2024, 120(62584-2601

[41]

Shen JZ, Zou ZW, Zhang XZ, Zhou L, Wang YH, Fang WP, Zhu XJ. Metabolic analyses reveal different mechanisms of leaf color change in two purple-leaf tea plant (Camelliasinensis L.) cultivars. Hortic Res, 2018, 5: 7

[42]

Sun TH, Rao S, Zhou XS, Li L. Plant carotenoids: recent advances and future perspectives. Mol Hortic, 2022, 2(1): 3

[43]

Sun Q, He ZC, Wei RR, Zhang Y, Ye JL, Chai LJ, Xie ZZ, Guo WW, Xu J, Cheng YJ, Xu Q, Deng XX. The transcriptional regulatory module CsHB5-CsbZIP44 positively regulates abscisic acid-mediated carotenoid biosynthesis in citrus (Citrusspp.). Plant Biotechnol J, 2024, 22(3722-737

[44]

Sun SJ, Zhang Q, Yu YF, Feng JY, Liu CL, Yang JD. Leaf coloration in Acer palmatum is associated with a positive regulator ApMYB1 with potential for breeding color-Leafed Plants. Plants (Basel), 2022, 11(6759

[45]

Sun Y, Hu PL, Jiang YN, Wang ZZ, Chang JX, Zhou YW, Shao HJ. Comprehensive analysis of metabolomics and transcriptomics reveals varied tepal pigmentation across Gloriosa varieties. BMC Plant Biol, 2025, 25(166

[46]

Song P, Ding YF, Li H, Wang YN. Studies on the color mechanism of Euonymus myrianthus and Euonymus europaea. J Henan Agric Sci, 2019, 48(08122-128in chinese

[47]

Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. Sucrose-sspecific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol, 2006, 140(2): 637-646

[48]

Tang YH, Fang ZW, Liu M, Zhao DQ, Tao J. Color characteristics, pigment accumulation and biosynthetic analyses of leaf color variation in herbaceous peony (Paeonialactiflora Pall). 3 Biotech, 2020, 10(2): 76

[49]

Vangelisti A, Guidi L, Cavallini A, Natali L, Lo Piccolo E, Landi M, Lorenzini G, Malorgio F, Massai R, Nali C, Pellegrini E, Rallo G, Remorini D, Vernieri P, Giordani T. Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes. Sci Rep, 2020, 10(11959

[50]

Wang DR, Yang K, Wang X, Lin XL, Rui L, Liu HF, Liu DD, You CX. 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(31897

[51]

Wang JQ, Gu XY, Dong YL, Wang T, Sun QM, Fu SY, Yang Y, Huang JY, Liang CT, Xie XT, Jiang HJ, Zheng BS, Chen Y, He Y. Advances in the endogenous and exogenous regulation of anthocyanins-the key to color change in eudicots. Crit Rev Plant Sci, 2023, 42(4217-238

[52]

Wang L, Wang QG, Fu NN, Song MY, Han X, Yang Q, Zhang YT, Tong ZK, Zhang JH. Cyanidin-3-O-glucoside contributes to leaf color change by regulating two bHLH transcription factors in Phoebe bournei. Int J Mol Sci, 2023, 24(4): 3829

[53]

Wu XX, Li Y, Du T, Kang L, Pei BL, Zhuang WB, Tang F. Transcriptome sequencing and anthocyanin metabolite analysis involved in leaf red color formation of Cinnamomum camphora. Sci Rep, 2024, 14(131470

[54]

Xia Y, Chen WW, Xiang WB, Wang D, Xue BG, Liu XY, Xing LH, Wu D, Wang SM, Guo QG, Liang GL. Integrated metabolic profiling and transcriptome analysis of pigment accumulation in Lonicera japonica flower petals during colour-transition. BMC Plant Biol, 2021, 21(198

[55]

Xiao Z, Su JL, Liu XQ, Sun XB, He LS, Zhou HM, Li C. Overexpression of RmLCYB from Rhododendron molle increases carotenoid in Nicotiana tabacum. Acta Physiol Plant, 2022, 44: 71

[56]

Xie YR, Liu Y, Ma MD, Zhou Q, Zhao YP, Zhao BB, Wang BB, Wei HB, Wang HY. Arabidopsis FHY3 and FAR1 integrate light and strigolactone signaling to regulate branching. Nat Commun, 2020, 11(11955

[57]

Xie YT, Pei NC, Hao ZZ, Shi ZW, Chen L, Mai B, Liu QH, Luo JJ, Luo MD, Sun B. Juvenile leaf color changes and physiological characteristics of Acer tutcheri (Aceraceae) during the spring season. Forests, 2023, 14(2328

[58]

Xu ZZ, Yang XY, Wang Y, Du SH. Changes in pigment and coloration mechanism of leaves during the discoloration period of Pistacia chinensis. J Nanjing For Univ (Natural Sci Ed), 2024, 48(0297-104in chinese

[59]

Yang XT, Cai JW, Ren XJ, Tang ZH, Zhang J. Physiological and metabolic stage-specific characteristics of coloration in the Autumn leaves of Acer mono Maxim. J Northeast For Univ, 2024, 52(1147-55in chinese

[60]

Yuan YD, Zhang JC, Liu X, Meng MJ, Wang JP, Lin J. Tissue-specific transcriptome for Dendrobium officinale reveals genes involved in flavonoid biosynthesis. Genomics, 2020, 112(2): 1781-1794

[61]

Zeng ZY, Liao YW, Wang JZ, Liang XQ, Duan LQ, Huang YK, Han ZW, Lin K, Hu H, Ye KQ, Xu ZF, Ni J. Combined transcriptomic, metabolomic and physiological analysis reveals the key role of nitrogen, but not phosphate and potassium in regulating anthocyanin biosynthesis induced by nutrient deficiency in Eucalyptus. Int J Biol Macromol, 2024, 283(Pt 1 137564

[62]

Zhou NZ, Yan YJ, Wen YF, Zhang MH, Huang Y. Integrated transcriptome and metabolome analysis unveils the mechanism of color-transition in Edgeworthia chrysantha tepals. BMC Plant Biol, 2023, 23(1): 567

[63]

Zhou YW, Xu YC, Zhu GF, Tan JJ, Lin JY, Huang LS, Ye YJ, Liu JM. Pigment diversity in leaves of Caladium × hortulanum Birdsey and transcriptomic and metabolic comparisons between red and white leaves. Int J Mol Sci, 2024, 25(1605

[64]

Zhao T, Li N, Kong JX, Li XH, Huang CB, Wang YJ, Zhang CH, Li Y. An activator-represssor complex of VvWRKYs regulate proanthocyanidins biosynthesis through co-targeting VvLAR in grape. Int J Biol Macromol, 2024, 281(Pt 4 136653

[65]

Zhang C, Fu JX, Wang YJ, Gao SL, Du DN, Wu F, Guo J, Dong L. Glucose supply improves petal coloration and anthocyanin biosynthesis in Paeonia suffruticosa ‘Luoyang Hong’ cut flowers. Postharvest Biol Technol, 2015, 101: 73-81

[66]

Zhang HR, Du C, Wang Y, Wang J, Zheng LL, Wang YC. The Reaumuria trigyna leucoanthocyanidin dioxygenase (RtLDOX) gene complements anthocyanidin synthesis and increases the salt tolerance potential of a transgenic Arabidopsis LDOX mutant. Plant Physiol Biochem, 2016, 106: 278-287

[67]

Zhang J, Han N, Zhao AG, Wang ZY, Wang DM. ZbMYB111 Expression positively regulates ZbUFGT-Mediated anthocyanin biosynthesis in Zanthoxylum bungeanum with the involvement of ZbbHLH2. J Agric Food Chem, 2024, 72(3016941-16954

[68]

Zhang JK, Wang YC, Mao ZL, Liu WN, Ding LC, Zhang XN, Yang YW, Wu SQ, Chen XS, Wang YL. Transcription factor McWRKY71 induced by ozone stress regulates anthocyanin and proanthocyanidin biosynthesis in Malus crabapple. Ecotoxicol Environ Saf, 2022, 232 113274

[69]

Zhang KM, Li Z, Li Y, Li YH, Kong DZ, Wu RH. Carbohydrate accumulation may be the proximate trigger of anthocyanin biosynthesis under autumn conditions in Begonia semperflorens. Plant Biol (Stuttg), 2013, 15(6): 991-1000

[70]

Zhang L, Tao RY, Wang SM, Gao YH, Wang L, Yang SL, Zhang X, Yu WJ, Wu XY, Li KF, Ni JB, Teng YW, Bai SL. 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: 1022034

[71]

Zhang SK, Zhan W, Sun AR, Xie Y, Han ZM, Qu XB, Wang JY, Zhang LF, Tian MS, Pang XH, Zhang JB, Zhao XY. Combined transciptome and metabolome integrated analysis of Acer mandshuricum to reveal candidate genes involved in anthocyanin accumulation. Sci Rep, 2021, 11(123148

[72]

Zheng YJ, Tian L, Liu HT, Pan QH, Zhan JC, Huang WD. Sugars induce anthocyanin accumulation and flavanone 3-hydroxylase expression in grape berries. Plant Growth Regul, 2009, 58: 251-260

RIGHTS & PERMISSIONS

The Author(s)

PDF

295

Accesses

0

Citation

Detail

Sections
Recommended

/