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Acta Agronomica Sinica ›› 2021, Vol. 47 ›› Issue (12): 2407-2422.doi: 10.3724/SP.J.1006.2021.04231


Screening candidate genes related to aluminum toxicity stress at germination stage via RNA-seq and QTL mapping in Brassica napus L.

WANG Rui-Li1(), WANG Liu-Yan1, LEI Wei1,2, WU Jia-Yi1, SHI Hong-Song1, LI Chen-Yang1, TANG Zhang-Lin1,2, LI Jia-Na1,2, ZHOU Qing-Yuan1,2,*(), CUI Cui1,*()   

  1. 1College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, China
    2Chongqing Rape Engineering Technology Research Center, Chongqing 400715, China
  • Received:2020-10-27 Accepted:2021-05-17 Online:2021-12-12 Published:2021-06-09
  • Contact: ZHOU Qing-Yuan,CUI Cui E-mail:1525731297@qq.com;qingyuan@swu.edu.cn;cuicui@swu.edu.cn
  • Supported by:
    National Key Research and Development Program of China(2018YFD0100500);China Agriculture Research System(CARS-12);Technological Innovation, and the Application Development in Chongqing(cstc2019jscx-msxmX0383)


With the aggravation of soil acidification, aluminum toxicity has become one of the important stress factors affecting seed germination quality and crop yield. In order to study the molecular mechanism of the effect of aluminum toxicity on rapeseed seed germination, a total of 9344 significantly differentially expressed genes [log2 (fold change) ≥ 1 and FDR ≤ 0.05] were detected in the transcriptome analysis of aluminum-tolerant strain 18D300 and aluminum-sensitive strain 27011 by RNA-seq technology, among which 4406 DEGs (differentially expressed genes) were up-regulated and 4938 DEGs were down-regulated. GO enrichment showed that DEGs were mainly related to oxidation reaction, carbohydrate metabolism, and transporter activity. KEGG enrichment revealed that DEGs were mainly concentrated in phenylpropane biosynthesis, starch and sucrose metabolism, MAPK signal pathway-plant, plant-pathogen interaction, plant hormone signal transduction and so on. In addition, 44 DEGs (10 down-regulated and 34 up-regulated) were screened by integrating the results of RNA transcriptome sequencing and QTL mapping of root-related traits at germination stage under aluminum toxicity stress in rapeseed, which were mainly related to oxidative stress, osmotic regulation, cell wall modification, transporter, and hormone signal transduction.

Key words: Brassica napus L., aluminum poison, transcriptome sequencing, QTLs, differentially expressed genes

Table 1

Quality analysis of sequencing data"

Sample name
S0 R0 ST RT 总数
原始读数Raw reads 48,585,792 55,778,592 45,860,428 47,308,644 197,533,456
干净读数Clean reads 44,642,424 51,491,214 41,819,768 43,518,768 181,472,174
干净碱基Clean data (bp) 6,696,363,600 7,723,682,100 6,272,965,200 6,527,815,200 27,220,826,100
N (%) 0.001385 0.00138 0.001418 0.00137
Q20 (%) 97.57 97.59 97.72 97.43
Q30 (%) 94.14 94.22 94.43 93.74

Table 2

Primers of candidate differentially expressed genes used for qRT-PCR"

Gene name
Forward primer (5°-3°)
Reverse primer (5°-3°)

Fig. 1

Mean root length of different resistant materials 0 represents the control; T represents the treatments; S represents the sensitive strain to aluminum; R represents the resistant strain to aluminum. **: P < 0.01."

Fig. 2

Differentially expressed genes in four libraries Abbreviations of sample name are the same as those given in Table 1."

Fig. 3

Venn analysis of differentially expressed genes Abbreviations of sample name are the same as those given in Table 1."

Fig. 4

GO classification of differentially expressed genes in S0 vs R0 and S0 vs ST Abbreviations of sample name are the same as those given in Table 1."

Table 3

KEGG pathway significantly overrepresented in R0 vs RT and S0 vs ST"

KEGG term
Genes number
Ratio (%)
R0 vs RT
bna00940 苯丙烷生物合成Phenylpropanoid biosynthesis 55 21.32 3.81844E-21
bna00500 淀粉和蔗糖代谢Starch and sucrose metabolism 27 10.47 2.29236E-06
bna00910 氮素代谢Nitrogen metabolism 13 5.04 1.81952E-05
bna00270 半胱氨酸和蛋氨酸代谢CySteine and methionine metabolism 21 8.14 0.000110181
bna04016 MAPK信号通路-植物MAPK signaling pathway-plant 23 8.91 0.000143365
bna00010 糖酵解/糖异生Glycolysis/Gluconeogenesis 21 8.14 0.000268893
bna00130 泛醌和其他萜类醌生物合成
Ubiquinone and other terpenoid-quinone biosynthesis
11 4.26 0.001478368
bna00380 色氨酸代谢Tryptophan metabolism 12 4.65 0.003486812
bna00360 苯丙氨酸代谢Phenylalanine metabolism 10 3.88 0.006641539
KEGG term
Genes number
Ratio (%)
bna00460 氰基氨基酸代谢Cyanoamino acid metabolism 12 4.65 0.006641539
bna00350 酪氨酸代谢Tyrosine metabolism 9 3.49 0.007588613
bna04075 植物激素信号转导Plant hormone signal transduction 34 13.18 0.007588613
bna00052 半乳糖代谢Galactose metabolism 10 3.88 0.009316627
S0 vs ST
bna00940 苯丙烷生物合成Phenylpropanoid biosynthesis 97 31.80 5.89634E-43
bna04016 MAPK信号通路-植物MAPK signaling pathway-plant 38 12.46 9.09024E-08
bna00910 氮素代谢Nitrogen metabolism 16 5.25 2.123E-05
bna00460 氰基氨基酸代谢Cyanoamino acid metabolism 19 6.23 0.000428636
bna04075 植物激素信号转导Plant hormone signal transduction 52 17.05 0.001727744
bna00520 氨基糖和核苷酸糖代谢
Amino sugar and nucleotide sugar metabolism
27 8.85 0.004361711
bna04626 植物-病原体相互作用Plant-pathogen interaction 35 11.48 0.004455032
bna00040 戊糖和葡糖醛酸相互转化
Pentose and glucuronate interconversions
21 6.89 0.005458802

Fig. 5

GO classification of differentially expressed genes in S0 vs R0 and ST vs RT Abbreviations of sample name are the same as those given in Table 1."

Fig. 6

Enrichment factor scatter plot of the top 11 significant KEGG pathways in S0 vs R0 and ST vs RT The horizontal axis represents enrichment factors, and the vertical axis represents metabolic pathways. The location of bubbles represents the enrichment item, the size of bubbles represents the number of differential genes, and the color of bubbles represents the significant degree of enrichment. Abbreviations of sample name are the same as those given in Table 1."

Fig. 7

Heat map of candidate genes in R0 and RT Abbreviations of samples names are the same as those given in Table 1."

Fig. 8

Heat map of candidate genes in S0 and ST Abbreviations of samples names are the same as those given in Table 1."

Table 4

Candidate genes possibly involved in aluminum poison coercion using QTL and RNA-Seq techniques"

Gene ID in B. napus
Gene accession
RT:fpkm ST:fpkm 基因注释
Gene annotations
相对发芽势RGV Up 19.6 0.87
BnaA01g31480D AT3G10720 Up 58.3 16.8 植物转化酶/果胶甲基酯酶抑制剂超家族
Plant invertase/Pectin methyl esterase inhibitor superfamily
BnaA01g30490D AT3G12580 Up 176 56.5 热激蛋白70heatshockprotein70,hsp70
BnaA01g28900D AT3G15450 Up 264 30 Al具有YGL和LRDR图案的铝诱导蛋白质
Al-induced protein with YGL and LRDR patterns
BnaA01g27670D AT3G16690 Up 11.7 0.47 结蛋白MtN3家族蛋白Nodin MtN3 family protein
qRGV-A03-1 BnaA03g50730D AT3G48000 Down 0.08 13.5 乙醛脱氢酶2B4Acetaldehyde dehydrogenase 2B4
BnaA03g50130D AT4G30420 Up 20.9 4.05 结蛋白MtN21 /EamA样转运蛋白家族蛋白
Nodin MtN21 /EamA-like transporter family protein
BnaA03g50050D AT4G30270 Up 36.2 9.65 木葡聚糖内葡聚糖酰化酶/水解酶 (XTH)
Xyloglucan endoglucanase/hydrolase (XTH)
BnaA03g47720D AT4G26010 Up 6.4 0.7 过氧化物酶超家族蛋白Peroxidase superfamily protein
BnaA03g47250D AT4G25260 Up 36.6 4.89 植物转化酶/果胶甲基酯酶抑制剂超家族
Plant invertase/Pectin methyl esterase inhibitor superfamily
BnaA03g46060D AT4G23590 Up 11 0.16 酪氨酸转氨酶家族蛋白Tyrosine transaminase family protein
BnaA03g45950D AT4G00430 Up 18.7 2.9 跨膜蛋白CTransmembrane protein c
BnaA03g44820D AT4G21680 Down 3.21 4.06 硝酸盐转运体Nitrate transporter
BnaA03g43140D AT4G17550 Up 10.3 0.05 主要促进因子超家族蛋白质Major promoter superfamily proteins
BnaA03g42860D AT4G16820 Up 6.25 0.62 α/β-水解酶超家族蛋白质α/β-hydrolase superfamily protein
BnaA03g42310D AT4G15960 Up 17.6 4.18 α/β-水解酶超家族蛋白质α/β-hydrolase superfamily protein
BnaA03g40990D AT3G50830 Down 0.31 17.7 冷调节413等离子体Cold conditioning 413 plasma
BnaA03g40380D AT5G61600 Up 173 31.6 乙烯响应因子104 (ERF104)
Ethylene response factor 104 (ERF104)
qRGV-A03-2 BnaA03g09460D AT5G59530 Down 1.94 14.8 2-氧代戊二酸和铁依赖性加氧酶超家族蛋白
2-oxoglutarate and iron-dependent oxygenase superfamily proteins
BnaA03g09400D AT5G59550 Up 42.4 10.6 锌指(C3HC4型无名指)家族蛋白
Zinc finger (C3HC4 ring finger) family protein
BnaA03g09290D AT5G59730 Up 27.3 5.38 外胚层亚单位exo70家族蛋白
Exoderm subunit exo70 family protein
BnaA03g08870D AT5G60530 Up 10.7 0.26 晚期胚胎发生丰富蛋白/ LEA蛋白
Late embryogenesis rich protein/LEA protein
BnaA03g08820D AT5G60660 Up 44.5 0.84 质膜内在蛋白2 Plasma membrane intrinsic protein 2
BnaA03g07790D AT5G19855 Down 3.53 6.86 伴侣蛋白RbcX Companion protein RbcX
BnaA03g07660D AT5G19600 Down 2.83 21.8 硫酸盐转运蛋白Sulfate transporter
BnaA03g03740D AT5G12020 Up 99.8 18.3 17.6 kD二类热激蛋白(HSP17.6II)
17.6 kD class ii heat shock protein (HSP17.6II)
qRGV-C03 BnaC03g08610D AT5G17820 Up 14.7 0.78 过氧化物酶超家族蛋白Peroxidase superfamily protein
相对发芽率RGR qRGR-C04 BnaC04g10740D AT2G34500 Up 55.9 12.3 细胞色素P450,家族710,亚家族A,多肽1 (CYP710)
Cytochrome P450, family 710, subfamily A, polypeptide 1 (CYP710)
BnaC04g08480D AT2G36780 Down 0.9 23.3 UDP-糖基转移酶超家族蛋白
UDP-glycosyltransferase superfamily protein
BnaC04g07650D AT2G37820 Up 10.1 0.22 富含半胱氨酸/组氨酸结构域家族蛋白
Protein rich in cysteine/histidine domain family
BnaC04g06480D AT2G38940 Down 3.11 182 磷酸盐转运蛋白Phosphate transporter
BnaC04g06140D AT2G39430 Up 33.4 5.44 抗病反应(定向蛋白样)家族蛋白
Disease resistance response (directed protein-like) family protein
相对根长RRL qRRL-A03-2 BnaA03g53200D AT4G35180 Down 0.46 0.31 赖氨酸/组氨酸转运蛋白7 (LHT7)
Lysine/histidine transporter 7 (LHT7)
BnaA03g52830D AT4G34410 Up 17.2 2.6 氧化还原反应转录因子1 (RRTF1)
Redox transcription factor 1 (RRTF1)
qRRL-A09 BnaA09g02040D AT4G12550 Up 37.1 0 生长素诱导的根培养Root culture induced by auxin
BnaA09g02030D AT4G12550 Up 470 34.5 生长素诱导的根培养1Auxin-induced root culture 1
qRRL-C03 BnaC03g65590D AT4G35060 Down 4.57 6.67 重金属转运/解毒超家族蛋白
Heavy metal transport/detoxification superfamily protein
BnaC03g65200D AT4G23550 Up 13.6 1.28 WRKY29家族WRKY29 familyWRKY29 family wrky 29 family
BnaC03g62130D AT4G23700 Up 256 70.6 阳离子/氢离子交换器17 (CHX17)
Cation/hydrogen ion exchanger 17 (CHX17)
相对芽长RBL qRBL-C08 BnaC08g17880D AT1G18300 Up 115 28.1 nudix水解酶同源物(NUDT) Nudix hydrolase homologue (NUDT)
BnaC08g16940D AT1G16390 Up 1.89 0.05 有机阳离子/肉碱转运蛋白Organic cation/carnitine transporter
相对干重RDW qRDW-A09-1 BnaA09g30120D AT1G23090 Up 0.04 0.66 硫酸盐转运蛋白(AST) Sulfate transporter (AST)
BnaA09g29940D AT4G13390 Up 38.4 3.17 富含脯氨酸的伸展蛋白样家族蛋白
Proline-rich extension-like family proteins
qRDW-A10-2 BnaA10g25970D AT5G04250 Down 7.13 22.2 半胱氨酸蛋白酶超家族蛋白
Cysteine protease superfamily protein

Fig. 9

Heat map of candidate genes in RT and ST Abbreviations of samples names are the same as those given in Table 1."

Fig. 10

Correlation analysis between qRT-PCR and RNA-seq"

Table 5

Physiological index of rapeseed root system after aluminum poison coercion"

Physiological index
R系 R strain S系 S strain
R0 RT 增幅
Range of increase (%)
S0 ST 增幅
Range of increase (%)
丙二醛 MDA (nmol g-1) 4.26 4.44 0.04 5.63 6.16 0.10**
苯丙氨酸解氨酶 PAL (U g-1) 4.54 6.53 0.44 5.06 6.45 0.27
脯氨酸 Pro (µg g-1) 51.26 56.70 0.11** 52.39 57.20 0.09**
超氧化物歧化酶 SOD (U g-1) 54.89 86.50 0.58** 58.63 66.13 0.13**
过氧化氢酶 CAT (U g-1) 281.71 261.39 -0.07** 376.24 282.13 -0.25**
过氧化物酶 POD (U g-1) 14,521.79 10,566.33 -0.27 13,381.75 10,337.50 -0.23**
可溶性糖 SUG (mg g-1) 2.18 1.80 -0.17** 3.12 2.85 -0.09**
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