Metabolome and Transcriptome Analyses Unravels Molecular Mechanisms of Leaf Color Variation by Anthocyanidin Biosynthesis in Acer triflorum

Acer triflorum Komarov is an important ornamental tree, and its seasonal change in leaf color is the most striking feature. However, the quantifications of anthocyanin and the mechanisms of leaf color change in this species remain unknown. Here, the combined analysis of metabolome and transcriptome was performed on green, orange, and red leaves. In total, 27 anthocyanin metabolites were detected and cyanidin 3-O-arabinoside, pelargonidin 3-O-glucoside, and peonidin 3-O-gluside were significantly correlated with the color development. Several structural genes in the anthocyanin biosynthesis process, such as chalcone synthase (CHS), flavanone 3-hydroxylase (F3H), and dihydroflavonol 4-reductase (DFR), were highly expressed in red leaves compared to green leaves. Most regulators (MYB, bHLH, and other classes of transcription factors) were also upregulated in red and orange leaves. In addition, 14 AtrMYBs including AtrMYB68, AtrMYB74, and AtrMYB35 showed strong interactions with the genes involved in anthocyanin biosynthesis, and, thus, could be further considered the hub regulators. The findings will facilitate genetic modification or selection for further improvement in ornamental qualities of A. triflorum.

[1]  Yan Liu,et al.  Acer triflorum as a new nervonic acid-containing oilseed resource for the future: Fruit-and-seed weight, oil content and fatty acid composition , 2022, Industrial Crops and Products.

[2]  Jianlin Cheng,et al.  Isolation and functional diversification of dihydroflavonol 4-Reductase gene HvDFR from Hosta ventricosa indicate its role in driving anthocyanin accumulation , 2021, Plant signaling & behavior.

[3]  Yueyue Wang,et al.  Roles of the 2-Oxoglutarate-Dependent Dioxygenase Superfamily in the Flavonoid Pathway: A Review of the Functional Diversity of F3H, FNS I, FLS, and LDOX/ANS , 2021, Molecules.

[4]  Jingyuan Song,et al.  Integrative analysis of metabolome and transcriptome reveals the mechanism of color formation in white root (Salvia miltiorrhiza) , 2021 .

[5]  Qinsong Yang,et al.  Molecular and metabolic insights into anthocyanin biosynthesis during leaf coloration in autumn , 2021 .

[6]  Ying Xie,et al.  Combined transcriptome and metabolome integrated analysis of Acer mandshuricum to reveal candidate genes involved in anthocyanin accumulation , 2021, Scientific Reports.

[7]  A. S. Dubrovina,et al.  External dsRNA Downregulates Anthocyanin Biosynthesis-Related Genes and Affects Anthocyanin Accumulation in Arabidopsis thaliana , 2021, International journal of molecular sciences.

[8]  A. Allan,et al.  The interaction of MYB, bHLH and WD40 transcription factors in red pear (Pyrus pyrifolia) peel , 2021, Plant Molecular Biology.

[9]  Weiwei Zhang,et al.  Unraveling the Regulatory Mechanism of Color Diversity in Camellia japonica Petals by Integrative Transcriptome and Metabolome Analysis , 2021, Frontiers in Plant Science.

[10]  Xiaofeng Wang,et al.  Integrated metabolome and transcriptome analysis of the anthocyanin biosynthetic pathway in relation to color mutation in miniature roses , 2021, BMC Plant Biology.

[11]  Lifang Wu,et al.  The R2R3-MYB transcription factor SsMYB1 positively regulates anthocyanin biosynthesis and determines leaf color in Chinese tallow (Sapium sebiferum Roxb.) , 2021 .

[12]  Lu Xiaoyu,et al.  Systematic Analysis of MYB Genes Family in Acer rubrum and Functional Characterization of ArMYB89 Gene. , 2021, Journal of experimental botany.

[13]  Xujia Duan,et al.  The R2R3-MYB gene PsMYB58 positively regulates anthocyanin biosynthesis in tree peony flowers. , 2021, Plant physiology and biochemistry : PPB.

[14]  Xiaoyan Yu,et al.  Acer triflorum: A maple species that serves as a resource for nervonic acid and that has an ultralow erucic acid content , 2021, Food Science and Technology.

[15]  R. Sederoff,et al.  MYB-Mediated Regulation of Anthocyanin Biosynthesis , 2021, International journal of molecular sciences.

[16]  Yu Gao,et al.  De novo transcriptome sequencing and anthocyanin metabolite analysis reveals leaf color of Acer pseudosieboldianum in autumn , 2020, BMC genomics.

[17]  Chunyu Li,et al.  MaMYB4, an R2R3-MYB Repressor Transcription Factor, Negatively Regulates the Biosynthesis of Anthocyanin in Banana , 2021, Frontiers in Plant Science.

[18]  Jun Tang,et al.  IbERF71, with IbMYB340 and IbbHLH2, coregulates anthocyanin accumulation by binding to the IbANS1 promoter in purple-fleshed sweet potato (Ipomoea batatas L.) , 2020, Plant Cell Reports.

[19]  Zhi-gang Xu,et al.  Study of the Relationship between Leaf Color Formation and Anthocyanin Metabolism among Different Purple Pakchoi Lines , 2020, Molecules.

[20]  F. Jiao,et al.  Metabolome and transcriptome analyses of the molecular mechanisms of flower color mutation in tobacco , 2020, BMC genomics.

[21]  Caixiang Liu,et al.  Metabolic and transcriptomic analysis related to flavonoid biosynthesis during the color formation of Michelia crassipes tepal. , 2020, Plant physiology and biochemistry : PPB.

[22]  Margaret H. Frank,et al.  TBtools - an integrative toolkit developed for interactive analyses of big biological data. , 2020, Molecular plant.

[23]  Zhujie Xie,et al.  Transcriptomic profiling of purple broccoli reveals light-induced anthocyanin biosynthetic signaling and structural genes , 2020, PeerJ.

[24]  Yongqi Zheng,et al.  Complete chloroplast genome sequence of the three-flowered maple, Acer triflorum (Sapindaceae) , 2020 .

[25]  A. Salvador,et al.  MBW complexes impinge on anthocyanidin reductase gene regulation for proanthocyanidin biosynthesis in persimmon fruit , 2020, Scientific Reports.

[26]  F. Wang,et al.  Transcriptomic analyses of Pinus koraiensis under different cold stresses , 2020, BMC Genomics.

[27]  Chuanyou Li,et al.  A Transcriptional Network Promotes Anthocyanin Biosynthesis in Tomato Flesh. , 2020, Molecular plant.

[28]  Kongshu Ji,et al.  Comparative transcriptome analysis of genes involved in response to thermal stress and leaf colour change of Acer palmatum , 2019, Scientia Horticulturae.

[29]  Kezhong Zhang,et al.  Regulatory mechanisms of leaf color change in Acer mono. , 2019, Genome.

[30]  C. Peng,et al.  Accumulation of Anthocyanins: An Adaptation Strategy of Mikania micrantha to Low Temperature in Winter , 2019, Front. Plant Sci..

[31]  Yao-wu Yuan,et al.  Transcriptional Regulation of Carotenoid Biosynthesis in Plants: So Many Regulators, So Little Consensus , 2019, Front. Plant Sci..

[32]  Shucai Wang,et al.  A functional homologue of Arabidopsis TTG1 from Freesia interacts with bHLH proteins to regulate anthocyanin and proanthocyanidin biosynthesis in both Freesia hybrida and Arabidopsis thaliana. , 2019, Plant physiology and biochemistry : PPB.

[33]  Zhu Chen,et al.  Transcriptome analysis based on a combination of sequencing platforms provides insights into leaf pigmentation in Acer rubrum , 2019, BMC Plant Biology.

[34]  Lingfei Xu,et al.  Differences among the Anthocyanin Accumulation Patterns and Related Gene Expression Levels in Red Pears , 2019, Plants.

[35]  P. Das,et al.  Ethylene mediates repression of anthocyanin accumulation in black rice pericarps in the absence of light. , 2019, Journal of plant physiology.

[36]  Xiaojun Chang,et al.  De novo transcriptome combined with spectrophotometry and gas chromatography-mass spectrometer (GC-MS) reveals differentially expressed genes during accumulation of secondary metabolites in purple-leaf tea (Camellia sinensis cv Hongyafoshou) , 2018, The Journal of Horticultural Science and Biotechnology.

[37]  Hongxing Xiao,et al.  Development of 15 microsatellite markers in Acer triflorum (Aceraceae) and cross‐amplification in congeneric species , 2018, Applications in plant sciences.

[38]  Li Li,et al.  Carotenoid Metabolism in Plants: The Role of Plastids. , 2018, Molecular plant.

[39]  Qianqian Shi,et al.  Transcriptomic Analysis of Leaf in Tree Peony Reveals Differentially Expressed Pigments Genes , 2017, Molecules.

[40]  G. Chung,et al.  Identification and Molecular Analysis of Four New Alleles at the W1 Locus Associated with Flower Color in Soybean , 2016, PloS one.

[41]  Marie-Agnès Dillies,et al.  SARTools: A DESeq2- and EdgeR-Based R Pipeline for Comprehensive Differential Analysis of RNA-Seq Data , 2015, bioRxiv.

[42]  L. Lepiniec,et al.  Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. , 2015, Trends in plant science.

[43]  M. Blaber,et al.  Structural basis for acceptor‐substrate recognition of UDP‐glucose: anthocyanidin 3‐O‐glucosyltransferase from Clitoria ternatea , 2015, Protein science : a publication of the Protein Society.

[44]  L. Tang,et al.  Analysis of the transcriptome of green and mutant golden-yellow leaves of Acer palmatum Thunb. using high-throughput RNA sequencing , 2015 .

[45]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[46]  A. Oshlack,et al.  Corset: enabling differential gene expression analysis for de novo assembled transcriptomes , 2014, Genome Biology.

[47]  Shutian Li.  Transcriptional control of flavonoid biosynthesis , 2014, Plant signaling & behavior.

[48]  Shan-Ju Li,et al.  Molecular Characterization and Expression Analyses of an Anthocyanin Synthase Gene from Magnolia sprengeri Pamp. , 2014, Applied Biochemistry and Biotechnology.

[49]  S. Korban,et al.  Introduction of apple ANR genes into tobacco inhibits expression of both CHI and DFR genes in flowers, leading to loss of anthocyanin , 2012, Journal of experimental botany.

[50]  Chuan-Yun Li,et al.  KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases , 2011, Nucleic Acids Res..

[51]  S. Korban,et al.  Ectopic Expression of Apple F3′H Genes Contributes to Anthocyanin Accumulation in the Arabidopsis tt7 Mutant Grown Under Nitrogen Stress1[C][W][OA] , 2010, Plant Physiology.

[52]  Matthew D. Young,et al.  Gene ontology analysis for RNA-seq: accounting for selection bias , 2010, Genome Biology.

[53]  Yoshikazu Tanaka,et al.  Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. , 2008, Current opinion in biotechnology.

[54]  Yoshikazu Tanaka,et al.  cDNA cloning and characterization of UDP-glucose:anthocyanidin 3-O-glucosyltransferase in Iris hollandica , 2005 .

[55]  J. Harborne,et al.  Anthocyanins and other flavonoids. , 2001, Natural product reports.

[56]  O. Paredes-López,et al.  Natural Pigments: Carotenoids, Anthocyanins, and Betalains — Characteristics, Biosynthesis, Processing, and Stability , 2000, Critical reviews in food science and nutrition.