Effect of H2S on glucosinolate biosynthesis in Arabidopsis thaliana based on transcriptomics
QI Hong-xue1, WU Li-hua2, LI Li-hong1
1. Department of Chemistry and Chemical Engineering, Jinzhong University, Yuci 030619, China; 2. Department of Biology, Taiyuan Normal University, Yuci 030619, China
Abstract:Glucosinolates are a group of nitrogen-and sulfur-containing secondary metabolites in cruciferous plants, which are closely related to environmental factors. In this study, transcriptome sequencing of Arabidopsis treated with hydrogen sulfide (H2S) was performed, and the biological functions and metabolic pathways of differentially expressed genes were analyzed to explore the regulatory effect of H2S on glucosinolate biosynthesis in plants. The results showed that a total of 3160 genes were differentially expressed in Arabidopsis seedlings sprayed with 100μmol/L H2S for 3 days, including genes involved in metabolism, binding, catalysis, transcription regulation, transport and signal transduction. KEGG enrichment analysis showed that differentially expressed genes were significantly enriched in multiple primary and secondary metabolism. After exogenous H2S treatment, nine genes (8up-regulated and 1down-regulated) involved in aliphatic glucosinolates biosynthesis were identified to be differentially expressed, but genes associated with indole glucosinolates biosynthesis showed no obvious change. Meantime, several genes that participated in sulfur metabolism, cysteine and methionine metabolism, and glutathione metabolism were up-regulated, suggesting that exogenous H2S can enhance sulfur-related metabolic pathways, which would promote the aliphatic glucosinolates biosynthesis in plants. Transcription factor analysis showed that MYB29 was up-regulated, which could positively regulate the aliphatic glucosinolates biosynthesis. And MYB51, which would inhibit the aliphatic glucosinolates biosynthesis, was down-regulated. These results suggested that H2S could regulate the aliphatic glucosinolates biosynthesis in plants through MYB transcription factors. The qRT-PCR analysis of several genes involved in the glucosinolate biosynthesis verified the accuracy of transcriptomic sequencing, which further proved that H2S participated in the regulation of glucosinolate biosynthesis in plants.
祁红学, 吴丽华, 李利红. 基于转录组分析外源H2S对拟南芥芥子油苷生物合成的影响[J]. 中国环境科学, 2023, 43(2): 957-963.
QI Hong-xue, WU Li-hua, LI Li-hong. Effect of H2S on glucosinolate biosynthesis in Arabidopsis thaliana based on transcriptomics. CHINA ENVIRONMENTAL SCIENCECE, 2023, 43(2): 957-963.
尚玉婷,张妮娜,上官周平,等.硫化氢在植物中的生理功能及作用机制 [J]. 植物学报, 2018,53(4):565-574. Shang Y T, Zhang N N, Shangguan Z P, et al. Physiological function and mechanism of hydrogen sulfide in plants [J]. Bulletin of Botany, 2018,53(4):565-574.
[2]
Xuan L, Li J, Wang X, et al. Crosstalk between hydrogen sulfide and other signal molecules regulates plant growth and development [J]. Internaional Journal of Molecular Sciences, 2020,21:4593.
[3]
Zhang J, Zhou M, Zhou H, et al. Hydrogen sulfide, a signaling molecule in plant stress responses [J]. Journal of Integrative Plant Biology, 2021,63(1):146-160.
[4]
Müller M, De Kok L J, Weidner W, et al. Differential effects of H2S on cytoplasmic and nuclear thiol concentrations in different tissues of Brassica roots [J]. Plant Physiology and Biochemistry, 2002,40:585-589.
[5]
Chen J, Shang Y T, Wang W H, et al. Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings [J]. Frontiers in Plant Science, 2016,7:1173.
[6]
Shi H, Ye T, Han B, et al. Hydrogen sulfide regulates abiotic stress tolerance and biotic stress resistance in Arabidopsis [J]. Journal of Integrative Plant Biology, 2015,l57:628-640.
[7]
Thinh Nguyen V P, Stewart J, Lopez M, et al. Glucosinolates: natural occurrence, biosynthesis, accessibility, isolation, structures, and biological activities [J]. Molecules, 2020,25(19):4537.
[8]
Mitreiter S, Gigolashvili T. Regulation of glucosinolate biosynthesis [J]. Journal of Experimental Botany, 2021,72(1):70-91.
[9]
Harun S, Abdullah-Zawawi M R, Goh H H, et al. A comprehensive gene inventory for glucosinolate biosynthetic pathway in Arabidopsis thaliana [J]. Journal of Agricultural and Food Chemistry, 2020,68(28): 7281-7297.
[10]
Poveda J, Eugui D, Velasco P. Natural control of plant pathogens through glucosinolates: an effective strategy against fungi and oomycetes [J]. Phytochemistry Reviews, 2020,19(4):1045-1059.
[11]
Liu Z C, Wang H P, Xie J M, et al. The roles of cruciferae glucosinolates in disease and pest resistance [J]. Plants, 2021,10(6): 1097.
[12]
Mao P, Li Q, Li Y, et al. The beneficial functions of blue light supplementary on the biosynthesis of glucosinolates in pakchoi (Brassica rapa L. ssp. chinensis) under greenhouse conditions [J]. Environmental and Experimental Botany, 2022,197:104834.
[13]
Rangkadilok N, Nieolas M E, Bennett R N, et al. The effect of sulfur fertilizer on glucoraphanin levels in Broccoli (B. oleracea L. var. italica) at different growth stages [J]. Journal of Agricultural and Food Chemistry, 2004,52(9):2632-3639.
[14]
陈亚州,陈思学,阎秀峰.环境对植物芥子油苷代谢的影响 [J]. 生态学报, 2008,28(6):2828-2833. Chen Y Z, Chen S X, Yan X F. Effect of environment on glucosinolate metabolism in plant [J]. Acta Ecologica Sinica, 2008,28(6):2828-2833.
[15]
庞秋颖,陈思学,于涛,等.盐胁迫对拟南芥和盐芥莲座叶芥子油苷含量的影响 [J]. 生态学报, 2011,31(16):4534-4541. Pang Q Y, Chen S X, Yu T, et al. Effects of salt stress onglucosinolate contents in Arabidopsis thaliana and Thellungiella halophila rosette leaves [J]. Acta Ecologica Sinica, 2011,31(16):4534-4541.
[16]
Li G, Shah A A, Khan W U, et al. Hydrogen sulfide mitigates cadmium induced toxicity in Brassica rapa by modulating physiochemical attributes, osmolyte metabolism and antioxidative machinery [J]. Chemosphere, 2021,263:127999.
[17]
裴雁曦.植物中的气体信号分子硫化氢:无香而立,其臭如兰 [J]. 中国生物化学与分子生物学报, 2016,32(7):721-733. Pei Y X. Gasotransmitter hydrogen sulfide in plants: stinking to high heaven, but refreshing to fine life [J]. Chinese Journal of Biochemistry and Molecular Biology, 2016,32(7):721-733.
[18]
Amir R, Galili G, Cohen H. The metabolic roles of free amino acids during seed development [J]. Plant Science, 2018,275:11-18.
[19]
Miao H, Cai C, Wei J, et al. Glucose enhances indolic glucosinolate biosynthesis without reducing primary sulfur assimilation [J]. Scientific Reports, 2016,6:31854.
[20]
张琳,范晓明,林青,等.锥栗种仁转录组及淀粉和蔗糖代谢相关酶基因的表达分析 [J]. 植物遗传资源学报, 2015,16(3):603-611. Zhang L, Fan X M, Lin Q, et al. Transcriptome analysis for developing kernel and expression analysis of starch and sucrose metabolism-related genes in Castanea henryi [J]. Journal of Plant Genetic Resources, 2015,16(3):603-611.
[21]
Li-Beisson Y, Beisson F, Riekhof W. Metabolism of acyl-lipids in Chlamydomonas reinhardtii [J]. Plant Journal, 2015,82(3):504-522.
[22]
Kim S J, Matsuo T, Watanabe M, et al. Effect of nitrogen and sulphur application on the glucosinolate content in vegetable turnip rape (Brassica rapa L.) [J]. Soil Science and Plant Nutrition, 2002,48: 43-49.
[23]
Chen X J, Zhu Z J, Ni X L, et al. Effect of nitrogen and sulfur supply on glucosinolates in Brassica campestris ssp. Chinensis [J]. Agricultural Sciences in China, 2006,5(8):603-608.
[24]
Li L, Zhang H, Chai X, et al. Transcriptome and proteome conjoint analysis revealed that exogenous sulfur regulates glucosinolate synthesis in Cabbage [J]. Plants, 2021,10(10):2104.
[25]
Heikal Y M, El-Esawi M A, Galilah D A. Morpho-anatomical, biochemical and molecular genetic responses of canola (Brassica napus L.) to sulphur application [J]. Environmental and Experimental Botany, 2022,194:104739.
[26]
Birke H, De Kok L J, Wirtz M, et al. The role of compartment-specific cysteine synthesis for sulfur homeostasis during H2S exposure in Arabidopsis [J]. Plant and Cell Physiology, 2015,56:358-367.
[27]
李利红,郭宇茹,侯俊鑫,等.H2S信号在拟南芥响应SO2胁迫过程中的作用 [J]. 中国环境科学, 2022,42(6):2904-2910. Li L H, Guo Y R, Hou J X, et al. Functions of H2S signal in response to SO2 stress in Arabidopsis thaliana [J]. China Environmental Science, 2022,42(6):2904-2910.
[28]
Gigolashvili T, Berger B, Flügge U I. Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana [J]. Phytochemistry Reviews, 2009,8:3–13.
[29]
Pireyre M, Burow M. Regulation of MYB and bHLH transcription factors: A glance at the protein level [J]. Molecular Plant, 2015,8(3): 378-388.
[30]
Zuluaga D L, Graham N S, Klinder A, et al. Overexpression of the MYB29 transcription factor affects aliphatic glucosinolate synthesis in Brassica oleracea [J]. Plant Molecular Biology, 2019,101:65–79.
[31]
Frerigmann H, Gigolashvili T. MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana [J]. Molecular Plant, 2014,7(5):814-828.