Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (1): 134-151.doi: 10.3864/j.issn.0578-1752.2022.01.012

• HORTICULTURE • Previous Articles     Next Articles

Transcriptome Analysis of Genes Involved in ABA-Induced Anthocyanin Accumulation in Grape

XU XianBin(),GENG XiaoYue,LI Hui,SUN LiJuan,ZHENG Huan,TAO JianMin()   

  1. College of Horticulture, Nanjing Agricultural University, Nanjing 210095
  • Received:2021-03-15 Accepted:2021-06-08 Online:2022-01-01 Published:2022-01-07
  • Contact: JianMin TAO E-mail:619262966@qq.com;taojianmin@njau.edu.cn

Abstract:

【Objective】 The aim of this study was to analyze the genes involved in the regulation of ABA induced grape coloring, and to explore the molecular mechanism of ABA induced anthocyanin accumulation in grape. 【Method】 In present study, Benibalado was used as the experimental material. In the early stage of veraison, the grape clusters were treated with 300 mg·L-1ABA, water treated as control. The grape phenotypes were observed and anthocyanins were determined by UPLC-MS. The mechanism of ABA promoting anthocyanin accumulation was analyzed by transcriptome sequencing. 【Result】 After 3 days of exogenous ABA treatment, the grape berries were obviously colored, and the variety and content of anthocyanins were also increased. Among them, Peonidin 3-O-glucoside and Malvidin 3-O-glucoside increased most significantly. By KEGG enrichment analysis, 11 DEGs related to ABA signaling and 52 DEGs that related to anthocyanin biosynthesis, and transportation were identified, all of which were up-regulated. After exogenous ABA treatment, the DEGs from RNA-seq were searched by using BLAST against the grape TF database, and 297 transcription factors were identified. Through the further analyzing of the expression patterns of identified TFs, 15 members of MYB, bHLH, bZIP, NAC, Dof, and HD-ZIP families were observed to regulate anthocyanin biosynthesis. The analyzing of cis-acting elements in promoters showed that ABREs were identified in most of the promoters. The accuracy of RNA-seq was validated by qRT-PCR analysis of some candidate genes. 【Conclusion】 Overall, ABA promoting anthocyanin accumulation in grape was a complex process, including 11 DEGs related to ABA signal transduction, 52 DEGs that related to anthocyanin biosynthesis, modification and transportation, 15 transcription factors. This study provided a basis for revealing the molecular mechanism of ABA promoting anthocyanin accumulation in grape fruits.

Key words: grape, anthocyanin, ABA, RNA-seq, promoter

Table 1

Primer sequences of real-time fluorescence quantitative PCR"

基因名称
Gene name
正向引物
Forward primer (5′→3′)
反向引物
Reverse primer (5′→3′)
NCBI登录号
Accession number
VvPAL GTGAGGGAAGAACTGGGAGC AATGAGCTTCCCTGCACACA LOC100233012
VvCHS CCGAGAAGTTACGCTCCACA CTTCCTCAGCCGACTTCCTC LOC100258106
VvC4H GCCCATTTCTCCCAATATAGCAC GTATGGAGAGAGGCCCTGGA LOC100267215
VvF3H CAAGGTGGCCTACAACGACT AGGCCTCCACGATTTTCCTG LOC100233079
VvUFGT GAGGTCCTAGCACATGAGGC CCTCCCATTGAGCCTTTGGT LOC100233099
VvFAOMT CAAAACTGAAGCCCTCACAAAGT TCGACAGGGACATTCATCAGG LOC100233134
VvGST TGGAGGTTGAATCCCAACAATATCA ACACATCCAGAACCTTACCCA LOC100242506
VvMATE AATTTTAATGGGTGGGAGGCCA GAGAGACTGAGAGACTGCGAC LOC 100250967
VvMYB4 ACAGCACTGGCGTCAAGAAT TCTGCGACTGCTGGGAAATC LOC100254518
VvNAC29 GCCCCGTATCCATTATCCCC GTAGCTCGGTTGGGTCTAGC LOC104879728
VvDof5.6 ATGCTCACTTGCTCCAGACC TACCTTGGCTGAGAGAGGCT LOC100265549
VvHD-ZIP CCTGCAAAGAGGATCACCAT GGTGCAATTCCCCGTAGTTA LOC100245524
VvActin TACAATTCCATCATGAAGTGTGATG TTAGAAGCACTTCCTGTGAACAATG LOC100246825

Fig. 1

Phenotypic trait of Benibalado grape treated with exogenous ABA for 3 days"

Table 2

Effects of exogenous ABA treatment on anthocyanin content and components of Benibalado grape skins"

成分
Component
保留时间
Retention time (min)
分子/碎片
Molecular/Fragmention (m/z)
对照
Control (mg∙kg-1)
ABA处理
ABA treatment (mg∙kg-1)
飞燕草素 3-O-(6''-p-香豆酰葡萄糖苷)
Delphinidin 3-O-(6''-p-coumaroyl-glucoside)
3.02 465.10/303.05 1.24±0.19 1.23±0.25
矮牵牛素 3-O-葡萄糖苷
Petunidin 3-O-glucoside
4.18 479.12/301.07 0.00 1.5±0.20**
芍药素 3-O-葡萄糖苷
Peonidin 3-O-glucoside
4.76 463.12/301.07 1.46±0.25 18.08±1.95**
锦葵色素 3-O-葡萄糖苷
Malvidin 3-O-glucoside
5.02 493.13/331.08 1.31±0.30 11.82±1.59**
天竺葵素 3-O-(6''-p-香豆酰葡萄糖苷)
Cyanidin 3-O-(6''-p-coumaroyl-glucoside)
8.97 595.15/287.05 0.00 1.31±0.13**
芍药素 3-O-(6''-p-香豆酰葡萄糖苷)
Peonidin 3-O-(6''-p-coumaroyl-glucoside)
9.94 639.17/317.06 0.00 3.72±0.25**
总花青苷 Total anthocyanins / / 4.23±0.28 37.5±2.36**

Fig. 2

Analysis of VvNCED1 gene expression pattern after ABA treatment * and ** indicate significant difference between treatment and control at 0.05 and 0.01 level, respectively. The same as below"

Fig. 3

Analysis of VvNCED1 gene expression pattern after ABA treatment"

Table 3

Statistic of evaluating the RNA-seq data"

样本
Sample
原始序列
Number of raw
reads
干净序列
Number of clean
reads
有效比例
Effective reads ratio
(%)
比对序列
Mapped reads (Mapping rate,%)
Q30值
Q30 (%)
ABA18h-rep1 46698448 45502062 97.44% 42661098 (93.76) 94.55
ABA 18h-rep2 42356456 41455998 97.87% 38818882 (93.64) 94.56
ABA 18h-rep3 47460348 46189130 97.32% 43310745 (93.77) 94.84
CK 18h-rep1 45626112 44517058 97.57% 41826560 (93.96) 94.73
CK 18h-rep2 46629670 44922268 96.34% 42176033 (93.89) 95.04
CK 18h-rep3 46173614 44415392 96.19% 41599095 (93.66) 94.91
ABA 3d-rep1 48528740 47335738 97.54% 44167501 (93.31) 95.09
ABA 3d-rep2 45802840 44487648 97.13% 41636081 (93.59) 95.33
ABA 3d-rep3 46843568 45789804 97.75% 42741325 (93.34) 94.74
CK 3d-rep1 41352252 40054402 96.86% 36726263 (91.69) 94.33
CK 3d-rep2 46588212 45041810 96.68% 41795220 (92.79) 94.3
CK 3d-rep3 46096744 44484560 96.50% 40918000 (91.98) 94.44

Fig. 4

Differentially expressed genes at different developmental stages"

Fig. 5

Bubble chart for KEGG enrichment analysis of different expression genes"

Fig. 6

Analysis of gene expression pattern of ABA signaling pathway The color represents the corresponding FPKM value, and the higher the value, the redder the color; from left to right, the samples are CK-18 h, ABA-18 h, CK-3 d, ABA-3 d. The same as below"

Fig. 7

Analysis of gene expression pattern of anthocyanin accumulation related genes"

Fig. 8

Analysis of transcription factors in differential genes"

Table 4

Summary of the number of ABREs in 2000 bp promoter sequences of DEGs"

NCBI登录号
Accession number
FPKM值 FPKM Value ABRE元件数量
The number of ABREs
基因注释
Gene annotation
ABA18 h CK18 h ABA3 d CK3 d
LOC100233012 22.86 2.99 146.17 11.75 2 PAL
LOC100241575 27.27 3.94 146.49 10.51 1 PAL
LOC100241377 15.24 5.23 13.39 7.70 4 PAL
LOC100854997 1.09 0.24 1.48 0.87 6 PAL
LOC100245997 0.94 0.48 1.43 0.35 6 PAL
LOC100253493 72.53 6.17 23.01 2.61 3 C4H
LOC100267215 247.58 1.83 32.27 1.09 1 C4H
LOC100254698 32.99 12.71 23.72 13.25 4 4CL
LOC100245991 25.27 12.93 82.87 30.48 4 4CL
LOC100253166 1.81 0.76 0.54 0.39 3 CHS
LOC100263437 3.02 0.16 3.19 0.91 3 CHS
LOC100258106 843.21 485.95 3031.14 577.81 4 CHS
LOC100262321 3.25 1.53 3.78 1.58 3 CHS
LOC100264844 3.21 1.77 5.39 2.38 1 CHS
LOC100232843 187.92 57.83 509.38 113.44 0 CHS
LOC100263443 19.00 5.73 54.48 10.52 5 CHS
LOC100241164 2.14 0.39 1.66 1.34 0 CHS
LOC100233078 410.22 213.33 646.48 305.87 4 CHI
LOC100255217 255.72 183.82 637.94 284.91 4 CHI
LOC100232999 87.38 67.10 165.37 80.38 0 F3'H
LOC100261319 5.14 0.55 15.12 2.11 4 F3'5'H
LOC109122765 2.03 0.43 3.94 0.30 2 F3'5'H
LOC100243414 1.36 0.11 3.70 0.32 4 F3'5'H
LOC104877273 1.45 0.28 4.23 0.52 4 F3'5'H
LOC100241335 3.21 0.40 4.88 0.60 2 F3'5'H
LOC100233079 174.69 30.14 459.98 62.82 4 F3H
LOC100253950 526.93 291.78 592.54 357.45 5 F3H
LOC100233141 245.66 67.49 320.10 94.11 3 DFR
LOC100233142 493.12 246.34 1503.28 488.51 5 LDOX
LOC100233099 410.21 94.82 699.90 221.37 1 UFGT
LOC100852631 11.36 5.04 5.14 1.38 3 UFGT
LOC100264341 10.81 3.90 3.13 1.01 0 UFGT
LOC100257268 31.65 18.50 4.13 2.95 3 UFGT
LOC100255538 10.79 7.27 4.29 1.60 4 UFGT
LOC100265929 1.54 0.62 0.88 0.30 2 UFGT
NCBI登录号
Accession number
FPKM值 FPKM Value ABRE元件数量
The number of ABREs
基因注释
Gene annotation
ABA18 h CK18 h ABA3 d CK3 d
LOC100854172 103.23 23.28 67.84 21.74 1 OMT
LOC100233134 70.74 7.07 203.04 22.29 5 FAOMT
LOC100232862 105.44 36.52 55.05 25.23 2 OMT
LOC100232921 10.99 3.31 16.53 4.91 2 OMT
LOC100251744 6.90 3.62 4.87 3.39 0 OMT
LOC100243978 418.54 100.61 705.85 203.97 6 OMT
LOC100242506 38.68 4.88 72.67 6.66 0 GST
LOC100264838 8.74 1.18 3.02 0.60 4 GST
LOC100245065 19.94 8.57 17.88 14.00 4 GST
LOC100232976 190.44 68.50 1357.36 115.94 0 GST4
LOC100233043 231.50 154.62 241.01 199.76 0 GST
LOC100852746 3.00 1.06 1.65 1.09 1 GST
LOC104878920 5.29 1.65 5.94 1.69 1 3AT
LOC100252075 9.37 6.63 5.60 4.10 1 ABC
LOC100268149 75.98 92.38 114.89 97.89 11 VvAM1
LOC100250967 162.57 41.82 545.35 96.32 3 MATE
LOC100255800 16.82 2.83 25.14 9.63 5 MATE1
LOC100250616 38.07 11.73 37.19 17.00 2 MATE2
LOC100233098 31.24 2.48 39.68 9.14 13 MYBA1
LOC100232838 93.45 8.01 132.29 18.05 6 MYBA2
LOC100853472 166.39 8.79 333.69 23.14 6 MYBA3
LOC100233136 100.72 69.01 108.09 99.71 2 MYBC2-L1
LOC100254518 79.92 36.44 120.88 62.90 1 MYB4
LOC100251098 46.68 29.43 47.02 37.98 1 MYC1
LOC100260656 5.43 1.27 3.16 1.26 6 MYB
LOC100250940 6.10 1.08 2.67 1.14 2 MYB
LOC100260647 3.70 0.34 4.18 0.97 3 MYB
LOC104879728 34.16 7.04 18.04 4.46 8 NAC
LOC100243434 61.74 40.82 53.52 33.84 2 ABF1
LOC100232889 29.63 18.76 36.56 22.09 6 ABF2
LOC100258873 108.20 55.20 113.90 72.46 2 bZIP
LOC100265549 37.85 17.70 25.76 15.81 5 Dof
LOC100245524 51.19 6.03 32.12 5.14 6 HD-ZIP

Fig. 9

qRT-PCR analysis of differentially expressed genes"

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