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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (4): 944-956.doi: 10.3724/SP.J.1006.2024.34141

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Transcriptome analysis of tobacco in response to cadmium stress

ZHANG Hui(), ZHANG Xin-Yu, YUAN Xu, CHEN Wei-Da, YANG Ting()   

  1. College of Life Sciences, Jianghan University / Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056, Hubei, China
  • Received:2023-08-15 Accepted:2023-10-23 Online:2024-04-12 Published:2023-11-15
  • Contact: * E-mail: yangtingYT2016@163.com
  • Supported by:
    Natural Science Foundation of Hubei Province of China(2022CFB909);Youth Fund Project of the National Natural Science Foundation of China(31900095);First-Class Discipline Construction and Special Program of Jianghan University(2023XKZ016)

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Abstract:

With the development of industrialization process in society, the problem of cadmium (Cd) pollution in soil is increasing. However, Nicotiana tabacum has a strong Cd enrichment capacity in leaves, which seriously affects its economic value. To investigate the mechanism by which tobacco responds to Cd stress, tobacco leaves were harvested from the culture solution with Cd concentrations of 0 μmol L-1 and 500 μmol L-1 for subsequent transcriptome sequencing. In this study, a total of 76.94 Gb clean data was obtained, with Q30 base percentage exceeding 95.43%. The results showed that 7735 differentially expressed genes (DEGs) were screened under Cd stress conditions, including 4833 up-regulated genes and 2902 down-regulated genes. The reliability of transcriptome data was verified by qRT-PCR analysis to detect the expression patterns of candidate gene. Gene ontology (GO) annotation as well as Kyoto encyclopedia of genes and genomes (KEGG) pathway analysis were performed on differentially expressed transcripts. GO functional enrichment revealed that the differentially expressed genes were mainly distributed in metabolic processes, response to stimulus, cellular anatomical entity, catalytic activity, and transcription regulator activity. Meanwhile, KEGG analysis showed that the up-regulated differentially expressed genes were mainly involved in biosynthesis of amino acids, carbon metabolism, oxidative phosphorylation, and citrate cycle. Down-regulated differentially expressed genes were primarily enriched in photosynthesis, biosynthesis of secondary metabolites, metabolic pathways, and plant hormone signal transduction. Further analysis of plant hormone signal transduction pathways revealed that there were eight plant hormone pathways involved in response to cadmium stress in tobacco, and the relative expression patterns of different hormone gene member were also different. Experimental results from plant hormone application on tobacco leaves demonstrated that the regulation of gibberellins, brassinosteroids, and jasmonic acid pathways played roles in tobacco’s response to cadmium stress. The experimental results of Arabidopsis hormone signal mutant showed that plants respond to cadmium stress by regulating ethylene, gibberellin, brassinosteroid, and jasmonic acid pathways. In conclusion, this study not only explores the regulatory network of tobacco resistance to Cd stress, but also lays a theoretical foundation for the genetic improvement of crop resistance.

Key words: Nicotiana tabacum, cadmium stress, transcriptome analysis, regulatory mechanism, plant hormone

Table 1

Primers used for qRT-PCR in this study"

基因编号
Gene ID		 正向引物序列
Forward sequences (5°-3')		 反向引物序列
Reverse sequences (5°-3')
NtEF1α GCTGTAACAAGATGGATGC AGATGGGGACAAAGGGGAT
Nitab4.5_0001799g0060 TGATCGAACGGACCATTAT AAGCCTTATTCCAACTCTG
Nitab4.5_0000137g0100 GATCTTCTGAGTACCCGTAT CAACTTGATTCCTCCTTC
Nitab4.5_0001834g0020 GTAGCTGCATTGGCCCTTAG CTGTTGCTGCCTTCATTTCC
Nitab4.5_0001603g0110 ATAGTCAACAACTCCCTC CCTTCCAGCAGAATTAGA
Nitab4.5_0002739g0090 GTTGTTGTCGGAACTATGT ACCAGGCTTCTGATAAACT
Nitab4.5_0000303g0130 TCTCAGTCTCCGTTCCTCTA CTTTAAGCCTCTGGGTGTAG
Nitab4.5_0000786g0090 TCAACCTTTCTCGCTTCTGC CTGACCTCCCAAATTGCCTA

Fig. 1

Cd inhibited the growth of tobacco A: phenotypic changes of tobacco under Cd stress conditions; B: measurements of physiological parameter. The error line represents the mean ± standard deviation; *: P < 0.05; **: P < 0.01. The unit of leaf length, leaf width, and root length is cm; The unit of fresh weight is g. CK: 0 μmol L-1 Cd; Cd: 500 μmol L-1 Cd."

Table 2

Quality assessment of sample sequencing output data"

样品
Sample		 原始读长
Raw reads		 有效读长
Clean reads		 有效碱基
Clean bases		 GC含量
GC content (%)		 Q30%
Cd-1 117,197,630 114,117,568 16.28 51.24 96.27
Cd-2 92,057,888 89,923,200 12.87 52.87 95.43
Cd-3 92,277,960 89,807,396 12.79 52.84 96.01
CK-1 80,695,074 79,549,980 11.55 52.49 95.62
CK-2 90,502,566 88,261,644 12.36 53.06 96.45
CK-3 78,412,514 77,125,276 11.09 52.56 96.25

Fig. 2

Sample correlation and differential gene analysis A: sample correlation analysis; B: volcano map of differentially expressed genes."

Table 3

Differentially expressed genes in the transcriptome"

基因编号
Gene ID		 倍数变化
log2 (Fold Change)		 校正后P值
Padj -value		 显著性
Significant		 相关功能
Related functions
Nitab4.5_0001799g0060 6.01645779051992 5.58600524883223E-53 上调Up NADH氧化酶 NADHoxidase
Nitab4.5_0000137g0100 4.93283684860978 5.82620770685452E-36 上调Up 脂氧合酶 Lipoxygenase
Nitab4.5_0001834g0020 2.2757421379006 0.00106352851309622 上调Up AP2/ERF结构域 AP2/ERFdomain
Nitab4.5_0001603g0110 2.27445197002978 5.39888738311809E-07 上调Up WRKY转录因子 DNA-bindingWRKY
Nitab4.5_0002739g0090 -2.11819490857942 3.37346132804127E-19 下调Down 光系统天线蛋白Photosystemantennaprotein-like
Nitab4.5_0000303g0130 -1.68510291076442 2.83044174648409E-15 下调Down 核糖体蛋白L21 RibosomalproteinL21
Nitab4.5_0000786g0090 -2.10064535366169 1.06320970799878E-18 下调Down 植物抗坏血酸过氧化物酶Plantascorbateperoxidase

Fig. 3

Verification of the differentially expressed genes by qRT-PCR The error line represents the mean ± standard deviation; *: P < 0.05; **: P < 0.01."

Table 4

Differentially expressed genes related to cadmium transport pathway in tobacco leaves"

基因编号
Gene ID		 倍数变化
log2 (Fold Change)		 校正后P值
Padj -value		 显著性
Significant		 基因符号
Gene symbol
Nitab4.5_0001331g0110 2.29205916646639 0.0000160056470884177 上调Up ABCC10
Nitab4.5_0001898g0080 2.22733652858828 0.000386104024008464 上调Up ABCC15
Nitab4.5_0000106g0390 1.31870696593661 0.0212689692966056 上调Up ABCG3
Nitab4.5_0000496g0120 -2.59158544291489 1.60564591983942E-08 下调Down ABCG5
Nitab4.5_0006252g0030 1.31746228592749 0.0341152515360627 上调Up ABCG20
Nitab4.5_0000221g0040 2.28821296882979 0.00370517654747173 上调Up ABCG21
Nitab4.5_0002381g0060 10.210671343785 0.0000908617814568147 上调Up CAX18
Nitab4.5_0002478g0050 2.03423844364883 2.69008075629427E-06 上调Up HMA1
Nitab4.5_0003524g0040 2.10793204476971 0.0000026522303535919 上调Up HMA3
Nitab4.5_0000492g0070 2.09307506718162 0.000256620985201009 上调Up HMA5
Nitab4.5_0000267g0020 -1.05182186076751 0.0000603639575690097 下调Down HMA32
Nitab4.5_0000915g0200 1.48223660266316 0.0032272780694283 上调Up HMA39
Nitab4.5_0001119g0080 2.64624606789856 7.33048509501148E-08 上调Up NRAMP 3
Nitab4.5_0004147g0050 5.31130934808622 9.33236566781447E-10 上调Up NRAMP 6
Nitab4.5_0004048g0010 3.17293738846753 2.66390391106025E-12 上调Up PT2.11
Nitab4.5_0000081g0170 -1.37360555768205 7.90967873459083E-09 下调Down PT4.5
Nitab4.5_0000417g0150 2.1229862013314 0.00122100988376109 上调Up PT4.6
Nitab4.5_0003449g0030 1.30297458667808 0.011869363195499 上调Up PT6.4
Nitab4.5_0000166g0100 7.21539127135386 1.40896298333894E-45 上调Up PT7.3

Fig. 4

GO functional annotation of DEGs The left vertical axis in the figure represents the proportion of genes annotated to a certain GO term to the total number of genes annotated with GO, the right vertical axis represents the number of genes annotated to a certain GO term, and the horizontal axis represents each detailed classification of GO."

Fig. 5

KEGG enrichment scatter plot A: KEGG pathway up-regulated gene top 30 enrichment scatter plot; B: KEGG pathway down-regulated gene top 30 enrichment scatter plot. The Y-axis represents the enriched KEGG pathways, while the X-axis represents ratio of enriched DEGs in KEGG pathways to the total amount of DEGs."

Fig. 6

Schematic diagram of plant hormone signal transduction The colors in the figure represent differentially significant genes. Red shows genes that are significantly up-regulated. Yellow shows genes that are significantly down-regulated. Blue indicates that there are both significantly up-regulated and down-regulated genes."

Fig. 7

Regulation of hormones on plant response to Cd stress A: the effects of hormone on tobacco phenotype under Cd stress conditions; B: the quantitative analysis of shoot biomass; C: the phenotypes of Arabidopsis mutants and wild-type plants under Cd stress conditions; D: the determination of Arabidopsis root length; E: determination of Arabidopsis fresh weight. The error line represents the mean ± standard deviation; *: P < 0.05; **: P < 0.01. The unit of root length is cm; The fresh weight unit of Arabidopsis is mg, and the fresh weight unit of tobacco is g."

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