Whole-genome DNA methylation patterns and complex associations with gene expression associated with anthocyanin biosynthesis in apple fruit skin

Li, Wenfang; Ning, Gai-Xing; Mao, Juan; Guo, Zhigang; Zhou, Qi; Chen, Baihong

doi:10.1007/s00425-019-03266-4

Cited by 59 publications

(32 citation statements)

References 48 publications

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“…Other factors, such as transport proteins, plant hormones, and vascular pH, are also affecting the coloration for anthocyanins [30][31][32][33]. And recently, epigenetic modification has been introduced to reveal genetic variation in the regulation of the anthocyanins biosynthetic pathway [34][35][36][37].…”

Section: Introductionmentioning

confidence: 99%

“…DNA methylation, one of the best-studied epigenetic modifications, plays a key role in regulating eukaryotic growth and development processes involving gene expression regulation [38][39][40], genetic imprinting [41], tissue differentiation [42,43], transposon silencing [44], genomic stability maintenance and environmental adaptation [45][46][47], and so forth. The modification also leads to morphological abnormalities variation in plants, such as hypomethylated promoters of A1, DFR-B, and OgCHS genes driving brick-red pelargonidin pigmentation of flower petals of Oncidium [35], and cytosine methylation enrichment in promoter regions of MYB10 and MdGST genes are closely associated with red-and green-skinned fruits of apple and pear cultivars [32,36,37,[48][49][50][51]. Herein, we discuss the molecular mechanism for chimeric flower petals and gene expression of P. mume cv.…”

Section: Introductionmentioning

confidence: 99%

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Whole-Genome DNA Methylation Associated With Differentially Expressed Genes Regulated Anthocyanin Biosynthesis Within Flower Color Chimera of Ornamental Tree Prunus mume

Jiang

Zhang

2020

Forests

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DNA methylation is one of the best-studied epigenetic modifications involved in many biological processes. However, little is known about the epigenetic mechanism for flower color chimera of Prunus mume (Japanese apricot, mei). Using bisulfate sequencing and RNA sequencing, we analyzed the white (FBW) and red (FBR) petals collected from an individual tree of Japanese apricot cv. ‘Fuban Tiaozhi’ mei to reveal the different changes in methylation patterns associated with gene expression leading to significant difference in anthocyanins accumulation of FBW (0.012 ± 0.005 mg/g) and FBR (0.078 ± 0.013 mg/g). It was found that gene expression levels were positively correlated with DNA methylation levels within gene-bodies of FBW and FBR genomes; however, negative correlations between gene expression and DNA methylation levels were detected within promoter domains. In general, the methylation level within methylome of FBW was higher; and in total, 4,618 differentially methylated regions (DMRs) and 1,212 differentially expressed genes (DEGs) were detected from FBW vs. FBR. We also identified 82 DMR-associated DEGs, and 13 of them, including PmBAHD, PmCYP450, and PmABC, were playing critical roles in phenylalanine metabolism pathway, glycosyltransferase activity, and ABC transporter. The evidence exhibited DNA methylation may regulate gene expression resulting in flower color chimera of Japanese apricot.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Whole-Genome DNA Methylation Associated With Differentially Expressed Genes Regulated Anthocyanin Biosynthesis Within Flower Color Chimera of Ornamental Tree Prunus mume

Jiang

Zhang

2020

Forests

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“…In comparison with the hypomethylated state of flavonoid biosynthetic genes increasing both their expression and anthocyanin accumulation in apple fruit skin [ 33 ], methylation of MIA genes may appear as limited. A recent study has reported an inverse correlation between a P450 encoding gene methylation level and its expression [ 67 ].…”

Section: Results and Discussionmentioning

confidence: 99%

“…Specialized metabolic pathways in plants are developmentally and environmentally regulated and an additional epigenetic control has been proposed. For example, apple skin color in some cultivars is due to the accumulation of anthocyanins whose biosynthesis involves enzymes encoded by genes which are differentially methylated at cytosine nucleotides [ 33 ]. In addition, hypomethylation of flavonoid related genes has been correlated with increased expression and accumulation of anthocyanins.…”

Section: Introductionmentioning

confidence: 99%

Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation

Bernonville

Maury

Delaunay

et al. 2020

IJMS

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Catharanthus roseus produces a wide spectrum of monoterpene indole alkaloids (MIAs). MIA biosynthesis requires a tightly coordinated pathway involving more than 30 enzymatic steps that are spatio-temporally and environmentally regulated so that some MIAs specifically accumulate in restricted plant parts. The first regulatory layer involves a complex network of transcription factors from the basic Helix Loop Helix (bHLH) or AP2 families. In the present manuscript, we investigated whether an additional epigenetic layer could control the organ-, developmental- and environmental-specificity of MIA accumulation. We used Whole-Genome Bisulfite Sequencing (WGBS) together with RNA-seq to identify differentially methylated and expressed genes among nine samples reflecting different plant organs and experimental conditions. Tissue specific gene expression was associated with specific methylation signatures depending on cytosine contexts and gene parts. Some genes encoding key enzymatic steps from the MIA pathway were found to be simultaneously differentially expressed and methylated in agreement with the corresponding MIA accumulation. In addition, we found that transcription factors were strikingly concerned by DNA methylation variations. Altogether, our integrative analysis supports an epigenetic regulation of specialized metabolisms in plants and more likely targeting transcription factors which in turn may control the expression of enzyme-encoding genes.

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“…More recently, it was reported that the histone H3K9 demethylase gene JMJ25 in Populus directly affects the DNA methylation level of MYB182 , resulting in repression of anthocyanin accumulation (Fan et al, ). Li et al () measured whole‐genome DNA methylation and found that upstream hypomethylation of MdMYB10 led to anthocyanin biosynthesis in apple fruit skin. The DNA methyltransferase MET1 contributes to promoter CpG island hypermethylation, and it has been demonstrated in maize that the expression of ZmMET1 is associated with DNA replication and altered DNA methylation status in cold‐stressed quiescent cells (Steward et al, ).…”

Section: Introductionmentioning

confidence: 99%

MiR399d and epigenetic modification comodulate anthocyanin accumulation in Malus leaves suffering from phosphorus deficiency

Peng

Tian

Luo

et al. 2020

Plant Cell & Environment

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Inorganic phosphorus (Pi) deficiency induces anthocyanin accumulation in the leaves of some plant species; however, the molecular mechanisms underlying this phenomenon have not been well characterized. Here, we showed that microRNA399d (miR399d), high-affinity Pi transporter McPHT1;4, and McMYB10 are strongly induced in Malus leaves suffering from Pi deficiency. By culturing explants of transiently transformed plants in MS medium under conditions of Pi sufficiency and Pi deficiency, miR399d and McPHT1;4 were shown to play essential roles in the response to Pi deficiency and to play positive roles in the regulation of anthocyanin biosynthesis. Silencing of McHDA6 expression and treatment with the inhibitor trichostatin A suggested that the low expression of McHDA6 simultaneously reduced the transcription of McMET1 and decreased the methylation level of the McMYB10 promoter; however, the expression of McMYB10 and anthocyanin content were increased. Bimolecular fluorescence complementation and yeast two-hybrid assays revealed that McHDA6 binds directly to McMET1 through its BAH2 and DNMT1-RFD domains. Based on the results of our study, we propose a mechanism for the molecular regulation of anthocyanin biosynthesis, namely, the miR399d and epigenetic modification comodulation model, to explain the phenomenon in which leaves turn red under conditions of Pi deficiency. K E Y W O R D S anthocyanin accumulation, epigenetic modification, Malus crabapple, McMYB10, miR399d, phosphorus deficiency

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Whole-genome DNA methylation patterns and complex associations with gene expression associated with anthocyanin biosynthesis in apple fruit skin

Cited by 59 publications

References 48 publications

Whole-Genome DNA Methylation Associated With Differentially Expressed Genes Regulated Anthocyanin Biosynthesis Within Flower Color Chimera of Ornamental Tree Prunus mume

Whole-Genome DNA Methylation Associated With Differentially Expressed Genes Regulated Anthocyanin Biosynthesis Within Flower Color Chimera of Ornamental Tree Prunus mume

Developmental Methylome of the Medicinal Plant Catharanthus roseus Unravels the Tissue-Specific Control of the Monoterpene Indole Alkaloid Pathway by DNA Methylation

MiR399d and epigenetic modification comodulate anthocyanin accumulation in Malus leaves suffering from phosphorus deficiency

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