Scientia Agricultura Sinica ›› 2019, Vol. 52 ›› Issue (22): 3987-4001.doi: 10.3864/j.issn.0578-1752.2019.22.005

• MOLECULAR GENETICS • Previous Articles     Next Articles

Transcriptome Analysis and Gene Mining of Salt Tolerance in Sorghum Seedlings (Sorghum bicolor L. Moench)

DONG Ming1,KUERBAN Zaituniguli2,Lü Peng1,DU RuiHeng1,YE Kai2,HOU ShengLin1(),LIU GuoQing1()   

  1. 1 Institute of Millet Crops, Hebei Academy of Agriculture & Forestry Sciences/The Key Minor Cereal Crops Laboratory of Hebei Province, Shijiazhuang 050035;
    2 Institute of Bioenergy, Xinjiang Academy of Agriculture Sciences, Urumqi 830091
  • Received:2019-06-17 Accepted:2019-09-24 Online:2019-11-16 Published:2019-11-16
  • Contact: ShengLin HOU,GuoQing LIU E-mail:shenglinhou@aliyun.com;guoqingliu@hotmail.com

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Abstract:

【Object】The primary aim of this study was to identify salt tolerance genes and explore the tolerance response mechanism under salt stress in sorghum, which may provide a theoretical basis for sorghum salt tolerance breeding. 【Method】Two sorghum varieties, L-Tian, salt-sensitive and Shihong 137, salt-tolerant were employed as plant materials. The sorghum seedlings were treated with 2% NaCl solution at three-leaf and one heart stage. Three treatments including 0 h (CK), 1 h and 24 h were conducted. The plant height, root length, dry matter weight, Na + content and relative content of chlorophyll (SPAD value) were determined, and the transcriptome sequencing was performed on Illumina HiSeq 2000 platform. The FPKM method was employed to calculate the gene expression level. Both the differential expression fold (Fold Change) ≥ 2 and FDR<0.001 were used as screening criteria to detect the differentially expressed genes. The Gene Ontology and KEGG Pathway databases were used to analyze the differentially expressed genes involved in salt stress at different time points. 【Result】Salt stress had no significant effect on plant height, root length and dry matter weight of sorghum, but had significant effect on Na + content and SPAD value. The plant height, root length, Na + content and SPAD value of Shihong 137 were higher than those of L-tian. Totally 26628 known genes and 866 new genes have been identified from RNA-seq, of which, the number of differentially expressed genes from Shihong 137 is higher than that from L-tian. 375, 4206 and 3750 differentially expressed genes in 0 h VS 1 h, 0 h VS 24 h and 1 h VS 24 h groups had been identified from Shihong 137 respectively. The number of differentially expressed genes of 0 h VS 1 h, 0 h VS 24 h, and 1 h VS 24 h of L-tian was 167, 2534 and 1612, respectively. GO and KEGG analysis revealed that plant hormones such as abscisic acid, auxin, cytokinin, gibberellin and ethylene were involved in the salt tolerance of sorghum at an early stage of salt stress (1h), while Lhca, Lhcb, phosphoenolpyruvate carboxylase, and ribulose phosphate kinase were involved in the salt tolerance at a late stage of salt stress (24 h). The difference in salt tolerance between Shihong 137 and L-tian was mainly caused by the flavonoid biosynthetic metabolic pathway. 【Conclusion】The sorghum response to salt stress is a complex biological process that relies on the balanced expression of multiple genes in complex networks. Under salt stress, sorghum response to environmental stimuli was controlled by both hormonal signal transduction and photosynthesis. The flavonoid biosynthesis pathway played an important role in salt-tolerant varieties.

Key words: sorghum (Sorghum bicolor L.), salt stress, transcriptome, gene mining

Table 1

Primers of qRT-PCR"

基因ID Gene ID 正向引物 Forward primer (5′-3′) 反向引物 Reverse primer(5′-3′)
Sobic.006G018400 CATCAATGGTTACCGTGTGC CGCTCAGTGATGGTGATCTC
Sobic.006G034300 AGGAAGCGAAGGGAGTTAAAG TCTGGAACATGGAAAGGCTC
Sobic.004G300300 ACGGCTACGGCTACGACTAC ATGCCACCGCGTTCCACTC
Sobic.004G227400 TCATGTTCCAGCCGTCGTCG AAGAGGCCGTGGGCGTTG
GADPH TCACTGCTACCCAAAAGACG AGACATCAACGGTAGGAACAC

Fig. 1

Na+ content (Left) and SPAD value (Right) of L tian and Shihong 137 Different lowercase letters indicate a significant difference at a 5% level between different treatments"

Table 2

Statistics of agronomic characters under salt stress"

处理 Treatment 株高 Plant height (cm) 根长 Root length (cm) 干物重 Dry weight (g)
gCK 5.24 4.86 0.18
g1h 5.21 4.83 0.18
g24h 5.20 4.77 0.22
nCK 6.56 6.23 0.25
n1h 6.69 6.22 0.26
n24h 6.59 6.22 0.28

Fig. 2

Phenotype of sorghum in four-leaf stage A: 0 h salt stress of Shihong137 and L tian; B: Salt stress treatment and control treatment of Shihong137"

Table 3

Sequencing statistics of transcriptomes in sorghum leaves"

分类Classification 最大值Maximum 最小值Minimum 平均值Average
总序列标签Total reads 56174902 42082348 48578108
比对到基因组序列标签Mapped reads 44513494 33795753 37417638
比对到基因组序列标签比例Ratio of mapped reads (%) 79.74 76.27 78.33
GC含量GC content (%) 58.67 55.73 57.30
Q30碱基百分比Percentage of Q30 base (%) 93.29 92.40 92.89
已知转录本数Number of known gene 26628
新转录本数Number of novel gene 866

Table 4

Number of DEGs in salt treatments"

处理DEG Set 差异表达基因数DEG Number 上调表达基因数Up-regulated gene number 下调表达基因数Down-regulated gene number
nCK VS n1h 375 332 43
nCK VS n24h 4206 1947 2259
n1h VS n24h 3750 1711 2039
gCK VS g1h 167 149 18
gCK VS g24h 2534 1259 1275
g1h VS g24h 1612 715 897
gCK VS nCK 1240 576 664
g1h VS n1h 1184 540 644
g24h VS n24h 1910 783 1127

Fig. 3

Venn map of DEGs g: Salt sensitive variety L tian; n: Salt tolerant variety Shihong 137; gCK: L tian control; g1h: L tian salt stress for 1 h; g24h: L tian salt stress for 24 h; nCK: Shihong 137 control; n1h: Shihong 137 salt stress for 1 h; n24h: Shihong 137 salt stress for 24 h. The same as below"

Table 5

GO enrichment analysis of s DEGs in sorghum leaves"

处理
Treatments		 GO编号
GO ID		 GO分类
Term		 注释基因数Annotated 显著基因数Significant 期望值
Expected		 显著性
KS
nCK VS n1h GO:0060416 生长激素响应Response to growth hormone 48 1 0.68 1.80E-08
GO:0006749 谷胱甘肽代谢Glutathione metabolic process 88 1 1.25 2.20E-07
GO:0006569 色氨酸分解代谢Tryptophan catabolic process 129 2 1.83 5.00E-07
GO:0009684 吲哚乙酸生物合成Indoleacetic acid biosynthetic process 210 3 2.99 6.10E-07
GO:0080148 缺水反应负调节过程Negative regulation of response to water deprivation 56 1 0.80 8.20E-07
GO:0015824 脯氨酸转运Proline transport 164 3 2.33 2.10E-06
GO:0016036 磷缺失细胞响应过程 Cellular response to phosphate starvation 319 7 4.53 2.60E-06
GO:0051260 蛋白质同源寡聚化Protein homooligomerization 43 2 0.61 6.20E-06
GO:0033506 硫代葡萄糖苷生物合成过程
Glucosinolate biosynthetic process from homomethionine		 11 0 0.16 1.00E-05
GO:0071475 细胞高渗盐反应Cellular hyperosmotic salinity response 10 1 0.14 1.60E-05
nCK VS n24h GO:0010207 光系统II组装Photosystem II assembly 257 123 39.38 1.40E-25
GO:0006364 核糖体RNA加工rRNA processing 403 161 61.75 8.30E-24
GO:0010027 类囊体膜组织Thylakoid membrane organization 366 149 56.08 1.00E-21
GO:0009773 光系统I中的光合电子输运
Photosynthetic electron transport in photosystem I		 70 43 10.73 1.10E-17
GO:0000023 麦芽糖代谢过程Maltose metabolic process 217 93 33.25 2.50E-16
GO:0019252 淀粉合成过程Starch biosynthetic process 280 110 42.90 5.70E-16
GO:0010114 红光响应过程Response to red light 299 119 45.82 9.60E-15
GO:0019344 半胱氨酸生物合成Cysteine biosynthetic process 389 129 59.61 8.60E-13
GO:0080167 karrikin响应过程Response to karrikin 493 124 75.54 2.20E-12
GO:0006569 色氨酸分解代谢Tryptophan catabolic process 129 38 19.77 9.20E-11
gCK VS g1h GO:0060416 生长激素响应Response to growth hormone 48 0 0.28 9.70E-09
GO:0006749 谷胱甘肽代谢Glutathione metabolic process 88 1 0.52 4.10E-08
GO:0080148 缺水反应负调节过程Negative regulation of response to water deprivation 56 0 0.33 4.60E-07
GO:0009684 吲哚乙酸生物合成Indoleacetic acid biosynthetic process 210 1 1.23 4.70E-07
GO:0006569 色氨酸分解代谢Tryptophan catabolic process 129 1 0.76 5.80E-07
GO:0015824 脯氨酸转运Proline transport 164 2 0.96 8.10E-07
GO:0016036 磷缺失细胞响应过程Cellular response to phosphate starvation 319 1 1.87 2.10E-06
GO:0051260 蛋白质同源寡聚化Protein homooligomerization 43 0 0.25 4.70E-06
GO:0033506 硫代葡萄糖苷生物合成过程
Glucosinolate biosynthetic process from homomethionine		 11 0 0.06 8.10E-06
GO:0009704 去乙醇De-etiolation 86 0 0.51 1.20E-05
gCK VS g24h GO:0006098 戊糖磷酸支路Pentose-phosphate shunt 325 134 30.72 6.40E-30
GO:0019288 异戊烯二磷酸生物合成过程Isopentenyl diphosphate biosynthetic process.
甲基赤藓糖醇4-磷酸通路Methylerythritol 4-phosphate pathway		 392 123 37.06 3.80E-19
GO:0010207 光系统II组装Photosystem II assembly 257 89 24.29 2.30E-17
GO:0000023 麦芽糖代谢Maltose metabolic process 217 77 20.51 5.00E-14
GO:0019252 淀粉生物合成Starch biosynthetic process 280 89 26.47 1.80E-13
GO:0009773 光系统I中的光合电子输运
Photosynthetic electron transport in photosystem I		 70 38 6.62 4.00E-13
GO:0080167 karrikin响应过程Response to karrikin 493 94 46.6 1.30E-11
GO:0010114 红光反应系统Response to red light 299 90 28.26 3.20E-11
GO:0060416 生长激素响应Response to growth hormone 48 12 4.54 1.60E-10
GO:0010027 类囊体膜组织Thylakoid membrane organization 366 93 34.60 3.60E-10

Fig. 4

Heatmap of plant hormone signal transduction"

Table 6

Genes involved in photosynthesis and salt stress"

基因名称
Gene name		 基因ID
Gene ID		 FPKM 值FPKM value
gCK g1h g24h nCK n1h n24h
Lhca1 Sobic.004G056900 6845.75 5277.53 549.64 7487.56 6519.72 268.80
Lhca2 Sobic.002G215000 1138.05 1161.23 68.34 1049.57 1109.62 20.12
Lhca2 Sobic.002G352100 4759.34 3627.86 260.80 4158.43 3828.06 73.90
Lhca3 Sobic.010G189300 4871.52 3711.42 392.95 5321.69 4030.16 151.76
Lhca4 Sobic.007G136900 4332.36 3332.85 194.35 5032.23 4230.89 67.37
Lhca5 Sobic.004G308700 728.38 595.98 75.06 842.51 805.12 35.45
Lhcb1 Sobic.002G288300 3292.48 3102.02 307.94 3037.17 2900.42 181.03
Lhcb1 Sobic.003G209900 6389.25 4984.08 49.64 3469.75 3574.07 4.02
Lhcb1 Sobic.009G234600 5809.76 5237.89 653.41 4791.33 4965.73 479.47
Lhcb2 Sobic.001G177000 8469.69 6247.14 446.28 13066.13 9860.12 175.30
Lhcb3 Sobic.002G339200 1714.88 1482.53 72.21 1275.63 1696.12 42.19
Lhcb4 Sobic.002G338000 3871.83 3342.85 250.40 3352.35 3419.74 74.70
Lhcb5 Sobic.005G087000 3613.05 3154.13 108.67 3800.17 3639.70 34.51
Lhcb6 Sobic.006G264200 2859.62 2414.96 84.85 1956.43 2112.88 67.85
PPC Sobic.002G167000 22.50 22.36 85.39 13.85 12.02 71.82
PPC Sobic.010G160700 5064.26 4230.24 932.75 4640.39 4269.74 262.15
PPC Sobic.004G106900 66.57 55.44 537.14 71.04 145.90 649.27
PPC Sobic.007G106500 29.54 15.39 23.77 15.24 16.67 71.67
PRK Sobic.004G272100 1162.80 1074.55 96.36 1050.45 1166.71 20.26
PRK Sobic.006G200800 35.80 25.69 4.21 32.01 26.04 3.00

Fig. 5

KEGG enrichment map A：gCK VS nCK;B：g1h VS n1h;C：g24h VS n24h"

Fig.6

FPKM values of ANR and FLS in L tian and Shihong 137"

Fig. 7

The results of qRT-PCR A：Sobic.006G18400;B：006G034300;C：004G300300"

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