玉米种胚内质网胁迫相关基因对人工老化处理的响应

doi:10.3864/j.issn.0578-1752.2016.03.003

Abstract

Abstract: 【Objective】 Endoplasmic reticulum (ER) stress and unfolded protein response (UPR) are involved in plant responses to environmental stresses. However, the expression of ER stress-related genes during maize seed aging has not been reported. In this study, the expression of ER stress-related genes during maize seed aging was investigated by Digital Gene Expression Profile (DGE) to provide theoretical support for clarifying the molecular mechanism of seed deterioration.【Method】 Hybrid maize (Zea mays L.) cultivar Zhengdan 958 seeds were used as experimental material and treated by artificial aging treatment (45℃, 100% relative humidity). DGE analysis was carried out on the Illumina Hiseq 2000 platform using total RNA extracted from 3 d artificial aging treatment and the untreated embryos (CK) of maize seeds. The reads with adaptor and ambiguous sequences, and the low-quality reads were filtered out to obtain the high quality clean reads. Clean reads were mapped to the maize reference genome and genes database using SOAPaligner/SOAP2. The gene expression level was calculated by the RPKM (Reads Per kb per million reads) method. A combination of FDR ＜0.001 and the absolute value of |log₂ ratio (T/CK)|≥1 was used as the threshold to determine the significance of gene expression difference. All differentially expressed genes (DEGs) were assigned to the pathways in KEGG (Kyoto Encyclopedia of Genes and Genomes) database and searched for the differentially expressed genes related to ER stress. Quantitative real-time PCR was performed to analyze the expression patterns of ER stress-related genes in the different artificial aging times.【Result】 Analysis of the DGE revealed that 104 DEGs were relevant to the protein processing in ER during the process of artificial aging treatment. A total of 97 DEGs related to ER stress including 81 and 16 genes respectively up- and down-regulated were screened out. The expression levels of ER stress marker BiP gene, as well as ER chaperones, such as CRT, CNT, GRP94 genes were considered to be significantly up-regulated. In particular, 83 DEGs were involved in ER-associated degradation (ERAD) pathway, including 70 up-regulated and 13 down-regulated DEGs. Among them, gene encoding EDEM (ER degradation enhancing mannosidase I-like protein) which is a rate-limiting enzyme of ERAD pathway was down-regulated. Genes involved in protein ubiquitination were altered in expression, including E2 ubiquitin-conjugating enzyme UbcH5, E3 ubiquitin-ligases Hrd1 and Doa10. The results of qRT-PCR analysis validated the diversity and complexity of ER stress-related genes expression in different artificial aging times.【Conclusion】 Artificial aging treatment can cause endoplasmic reticulum stress in maize embryo. The cell can respond to ER stress by inducing up-regulation of ER chaperones genes and activation of the ERAD pathway. Inhibition of ERAD pathway resulted in the accumulation of misfolded proteins in the ER with these leading to further cell damage and subsequently accelerating the loss of seed vigor.

Key words: maize, seed aging, differential expressed genes, ER stress, ERAD

CAO Guang-can, LIN Yi-xin, XUE Mei-zhen, XING Lu-man, Lü Wei-zeng, YANG Wei-fei, CHEN Jun-ying . Responses of Endoplasmic Reticulum Stress-Related Genes in Maize Embryo to Artificial Aging Treatment[J].Scientia Agricultura Sinica, 2016, 49(3): 429-442.

0
/ / Recommend

Add to citation manager EndNote|Reference Manager|ProCite|BibTeX|RefWorks

URL: https://www.chinaagrisci.com/EN/10.3864/j.issn.0578-1752.2016.03.003

https://www.chinaagrisci.com/EN/Y2016/V49/I3/429

References

[1] Schröder M, Kaufman R J. ER stress and the unfolded protein response. Mutation Research, 2005, 569: 29-63.

[2] Zhao L H, Ackerman S L. Endoplasmic reticulum stress in health and disease. Current Opinion in Cell Biology, 2006, 18: 444-452.

[3] Xu C Y, Bailly-Maitre B, Reed J C. Endoplasmic reticulum stress: Cell life and death decisions. The Journal of Clinical Investigation, 2005, 115: 2656-2664.

[4] Davies M J. The oxidative environment and protein damage. Biochimica et Biophysica Acta, 2005, 1703: 93-109.

[5] Berlett B S, Stadtman E R. Protein oxidation in ageing, disease, and oxidative stress. The Journal of Biological Chemistry,1997, 272(33): 20313-20316.

[6] Rajjou L, Lovigny Y, Groot S P, Belghazi M, Job C, Job D. Proteome-wide characterization of seed aging in Arabidopsis: A comparison between artificial and natural aging protocols. Plant Physiology, 2008, 148: 620-641.

[7] Rabek J P, Boylston W H, Papaconstantinou J. Carbonylation of ER chaperone proteins in aged mouse liver. Biochemical and Biophysical Research Communications, 2003, 305: 566-572.

[8] Chen H, Osuna D, Colville L, Lorenzo O, Graeber K, Küster H, Leubner-Metzger G, Kranner I. Transcriptome-wide mapping of pea seed ageing reveals a pivotal role for genes related to oxidative stress and programmed cell death. PLoS ONE, 2013, 8(10): e78471.

[9] Schröder M, Kaufman R J. The mammalian unfolded protein response. Annual Review of Biochemistry, 2005, 74: 739-789.

[10] Yoshida H. ER stress and diseases. FEBS Journal, 2007, 274(3): 630-658.

[11] Rao R V, Ellerby H M, Bredesen D E. Coupling endoplasmic reticulum stress to the cell death program. Cell Death and Differentiation, 2004, 11: 372-380.

[12] Fujita M, Mizukado S, Fujita Y, Ichikawa T, Nakazawa M, Seki M, Matsui M, Yamaguchi-Shinozaki K, Shinozaki K. Identification of stress-tolerance-related transcription-factor genes via mini-scale full-length cDNA Over-expressor (FOX) gene hunting system.Biochemical and Biophysical Research Communication, 2007, 364: 250-257.

[13] Jia X Y, Xu C Y, Jing R L, Li R Z, Mao X G, Wang J P, Chang X P. Molecular cloning and characterization of wheat calreticulin (CRT) gene involved in drought-stressed responses. Journal of Experimental Botany, 2008, 59(4): 739-751.

[14] Ruggiano A, Foresti O, Carvalho P. ER-associated degradation: Protein quality control and beyond. The Journal of Cell Biology, 2014, 204(6): 869-879.

[15] Meusser B, Hirsch C, Jarosch E, Sommer T. ERAD: The long road to destruction. Nature Cell Biology, 2005, 7: 766-772.

[16] Hiraishi H, Mochizuki M, Takagi H. Enhancement of stress tolerance in Saccharomyces cerevisiae by overexpression of ubiquitin ligase Rsp5 and ubiquitin-conjugating enzymes. Bioscience Biotechnology and Biochemistry, 2006, 70(11): 2762-2765.

[17] Hong Z, Jin H, Fitchette A C, Xia Y, Monk A M, Faye L, Li J M. Mutations of an α1,6 mannosyl transferase inhibit endoplasmic reticulum-associated degradation of defective brassinosteroid receptors in Arabidopsis. The Plant Cell, 2009, 21: 3792-3802.

[18] Yamamoto M, Kawanabe M, Hayashi Y, Endo T, Nishikawa S. A vacuolar carboxypeptidase mutant of Arabidopsis thaliana is degraded by the ERAD pathway independently of its N-glycan. Biochemical and Biophysical Research Communications, 2010, 393: 384-389.

[19] Liu L, Cui F, Li Q, Yin B, Zhang H, Lin B, Wu Y, Xia R, Tang S, Xie Q. The endoplasmic reticulum-associated degradation is necessary for plant salt tolerance. Cell Research, 2011, 21: 957-969.

[20] Cui F, Liu L, Zhao Q, Zhang Z, Li Q, Lin B, Wu Y, Tang S, Xie Q. Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in Brassinosteroid-mediated salt stress tolerance. The Plant Cell, 2012, 24: 233-244.

[21] Delouche J C, Baskin C C. Accelerated ageing techniques for predicting the relative storability of seed lots. Seed Science and Technology, 1973, 1: 427-452.

[22] 董国军, 胡兴明, 曾大力, 藤本宽, 滕胜, 国广泰史, 郭龙彪, 钱前. 水稻种子人工老化和自然老化的比较研究. 浙江农业科学, 2004(1): 29-31.

Dong G J, Hu X M, Zeng D L, Fujimoto K, Teng S, Kunihiro Y, Guo L B, Qian Q. Comparison between artificial ageing and natural ageing in rice. Journal of Zhejiang Agricultural Sciences, 2004(1): 29-31. (in Chinese)

[23] 吕伟增, 曹广灿, 林一欣, 薛梅真, 陈军营. 玉米种子老化相关MAPK途径基因表达分析. 植物生理学报, 2015, 51(6): 869-881.

Lü W Z, Cao G C, Lin Y X, Xue M Z, Chen J Y. Analysis of MAPK pathway genes expression related to maize seed ageing. Plant Physiology Journal, 2015, 51(6): 869-881. (in Chinese)

[24] 张景龙, 杨伟飞, 吕伟增, 曹广灿, 陈军营. 基于cDNA-AFLP 技术的玉米种子劣变相关基因分析. 植物生理学报, 2014, 50(7): 973-982.

Zhang J L, Yang W F, Lü W Z, Cao G C, Chen J Y. Analysis of genes related to seed deterioration in maize (Zea mays) based on cDNA-AFLP approach. Plant Physiology Journal, 2014, 50(7): 973-982. (in Chinese)

[25] Basak O, Demir I, Mavi K, Matthews S. Controlled deterioration test for predicting seedling emergence and longevity of pepper (Capsicum annuum L.) seed lots.Seed Science and Technology, 2006, 34: 723-734.

[26] Jana S, Choudhur M A. Glycolate metabolism of three submersed aquatic angiosperms during ageing. Aquatic Botany, 1982, 12: 345-354.

[27] 李合生. 植物生理生化实验原理和技术. 北京: 高等教育出版社, 2000: 164-169, 260-261.

Li H S. Experimental Principles and Techniques of Plant Physiological Biochemical. Beijing: Higher Education Press, 2000: 164-169, 260-261. (in Chinese)

[28] 杨伟飞, 张景龙, 吕伟增, 曹广灿, 陈军营. 人工劣变处理对玉米种胚差异基因表达的影响. 中国农业科学, 2014, 47(10): 1878-1893.

Yang W F, Zhang J L, Lü W Z, Cao G C, Chen J Y. Study on the differential genes expression in maize embryo treated by a controlled deterioration treatment. Scientia Agricultura Sinica, 2014, 47(10): 1878-1893. (in Chinese)

[29] Bennett S. Solexa Ltd. Pharmacogenomics, 2004, 5(4): 433-438.

[30] Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y. KEGG and the environment for linking genomes to life. Nucleic Acids Research, 2008, 36: 480-484.

[31] Lee A S. The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods,2005, 35: 373-381.

[32] Kaneko M, Nomura Y. ER signaling in unfolded protein response. Life Sciences, 2003, 74: 199-205.

[33] Wang B, Heath-Engel H, Zhang D, Nguyen N, Thomas D Y, Hanrahan J W, Shore G C. BAP31 interacts with Sec61 translocons and promotes retrotranslocation of CFTR△F508 via the Derlin-1 Complex. Cell,2008, 133: 1080-1092.

[34] Medicherla B, Kostova Z, Schaefer A, Wolf D H. A genomic screen identifies Dsk2p and Rad23p as essential components of ER- associated degradation. EMBO Reports, 2004, 5: 692-697.

[35] Hendry G A F. Oxygen, free radical processes and seed longevity. Seed Science Research, 1993, 3: 141-153.

[36] Bailly C. Active oxygen species and antioxidants in seed biology. Seed Science Research, 2004, 14: 93-107.

[37] Bailly C, Kranner I. Analyses of reactive oxygen species and antioxidants in relation to seed longevity and germination. Methods in Molecular Biology, 2011, 773: 343-367.

[38] Halliwell B, Gutteridge J M. Oxygen free radicals and iron in relation to biology and medicine: Some problems and concepts. Archives of Biochemistry and Biophysics, 1986, 246: 501-514.

[39] Henzler T, Steudle E. Transport and metabolic degradation of hydrogen peroxide in Chara coralline: Model calculations and measurements with the pressure probe suggest transport of H₂O₂ across water channels. Journal of Experimental Botany, 2000, 51(353): 2053-2066.

[40] Goel A, Goel A K, Sheoran I S. Changes in oxidative stress enzymes during artificial ageing in cotton (Gossypium hirsutum L.) seeds. Journal of Plant Physiology, 2003, 160: 1093-1100.

[41] Kibinza S, Vinel D, Côme D, Bailly C, Corbinea F. Sunflower seed deterioration as related to moisture content during ageing, energy metabolism and active oxygen species scavenging. Physiologia Plantarum, 2006, 128: 496-506.

[42] Yao Z, Liu L, Gao F, Rampitsch C, Reinecke D M, Ozga J A, Ayele B T. Developmental and seed aging mediated regulation of antioxidative genes and differential expression of proteins during pre and post-germinative phases in pea. Journal of Plant Physiology, 2012, 169: 1477-1488.

[43] Lisa S, Domingo B, Martínez J, Gilch S, Llopis J F, Schätzl H M, Gasset M. Failure of prion protein oxidative folding guides the formation of toxic transmembrane forms.Journal of Biological Chemistry, 2012, 287: 36693-36701.

[44] Tu B P, Weissman J S. Oxidative protein folding in eukaryotes: Mechanisms and consequences. The Journal of Cell Biology, 2004, 164(3): 341-346.

[45] Tu B P, Weissman J S. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Molecular Cell, 2002, 10: 983-994.

[46] Higa A, Chevet E. Redox signaling loops in the unfolded protein response.Cellular Signalling, 2012, 24: 1548-1555.

[47] Malhotra J D, Kaufman R J. Endoplasmic reticulum stress and oxidative stress: A vicious cycle or a double-edged sword? Antioxidants and Redox Signaling, 2007, 9: 2277-2293.

[48] Bravo R, Vicencio J M, Parra V, Troncoso R, Munoz J P, Bui M, Quiroga C, Rodriguez A E, Verdejo H E, Ferreira J, Iglewski M, Chiong M, Simmen T, Zorzano A, Hill J A, Rothermel B A, Szabadkai G, Lavandero S. Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. Journal of Cell Science, 2011, 124: 2143-2152.

[49] Yoon H, Kim D S, Lee G H, Kim K W, Kim H R, Chae H J. Apoptosis induced by manganese on neuronal SK-N-MC cell line: Endoplasmic reticulum (ER) stress and mitochondria dysfunction. Environmental Health and Toxicology, 2011, 26: e2011017.

[50] Bays N W, Gardner R G, Seelig L P, Joazeiro C A, Hampton R Y. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nature Cell Biology, 2001, 3: 24-29.

[51] Loertscher J, Larson L L, Matson C K, Parrish M L, Felthauser A, Sturm A, Tachibana C, Bard M, Wright R. Endoplasmic reticulum- associated degradation is required for cold adaptation and regulation of sterol biosynthesis in the yeast. Eukaryotic Cell, 2006, 5: 712-722.

[52] Kamauchi S, Nakatani H, Nakano C, Urade R. Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. The FEBS Journal, 2005, 272: 3461-3476.

[53] Martínez I M, Chrispeels M J. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. The Plant Cell, 2003, 15: 561-576.

[54] Deng Y, Srivastava R, Howell S H. Endoplasmic reticulum (ER) stress response and its physiological roles in plants. International Journal of Molecular Sciences, 2013, 14: 8188-8212.

[55] Avezov E, Frenkel Z, Ehrlich M, Herscovics A, Lederkremer G Z. Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for N-glycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Molecular Biology of the Cell, 2008, 19: 216-225.

[56] Oda Y, Hosokawa N, Wada I, Nagata K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science, 2003, 299(5611): 1394-1397.

[57] Eriksson K K, Vago R, Calanca V, Galli C, Paganetti P, Molinari M. EDEM contributes to maintenance of protein folding efficiency and secretory capacity. The Journal of Cell Biology, 2004, 279(43): 44600-44605.

[58] Molinari M, Calanca V, Galli C, Lucca P, Paganetti P. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science, 2003, 299(5611): 1397-1400.

[59] Su W, Liu Y D, Xia Y, Hong Z, Li J M. Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(2): 870-875.

[60] Ye Y, Meyer H H, Rapoport T A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature, 2001, 414(6): 652-656.

[61] Hirsch C, Gauss R, Horn S C, Neuber O, Sommer T. The ubiquitylation machinery of the endoplasmic reticulum. Nature, 2009, 458(7237): 453-460.

Metrics

Viewed

Full text

Abstract

Cited

Shared

Discussed

Comments

Recommended 0

No Suggested Reading articles found!

Responses of Endoplasmic Reticulum Stress-Related Genes in Maize Embryo to Artificial Aging Treatment

PDF

Abstract

Cite this article

share this article

References

Related Articles 15

Metrics

Comments

Recommended 0

[1]	ZHAO ZhengXin,WANG XiaoYun,TIAN YaJie,WANG Rui,PENG Qing,CAI HuanJie. Effects of Straw Returning and Nitrogen Fertilizer Types on Summer Maize Yield and Soil Ammonia Volatilization Under Future Climate Change [J]. Scientia Agricultura Sinica, 2023, 56(1): 104-117.
[2]	CHAI HaiYan,JIA Jiao,BAI Xue,MENG LingMin,ZHANG Wei,JIN Rong,WU HongBin,SU QianFu. Identification of Pathogenic Fusarium spp. Causing Maize Ear Rot and Susceptibility of Some Strains to Fungicides in Jilin Province [J]. Scientia Agricultura Sinica, 2023, 56(1): 64-78.
[3]	LI ZhouShuai,DONG Yuan,LI Ting,FENG ZhiQian,DUAN YingXin,YANG MingXian,XU ShuTu,ZHANG XingHua,XUE JiQuan. Genome-Wide Association Analysis of Yield and Combining Ability Based on Maize Hybrid Population [J]. Scientia Agricultura Sinica, 2022, 55(9): 1695-1709.
[4]	XIONG WeiYi,XU KaiWei,LIU MingPeng,XIAO Hua,PEI LiZhen,PENG DanDan,CHEN YuanXue. Effects of Different Nitrogen Application Levels on Photosynthetic Characteristics, Nitrogen Use Efficiency and Yield of Spring Maize in Sichuan Province [J]. Scientia Agricultura Sinica, 2022, 55(9): 1735-1748.
[5]	LI YiLing,PENG XiHong,CHEN Ping,DU Qing,REN JunBo,YANG XueLi,LEI Lu,YONG TaiWen,YANG WenYu. Effects of Reducing Nitrogen Application on Leaf Stay-Green, Photosynthetic Characteristics and System Yield in Maize-Soybean Relay Strip Intercropping [J]. Scientia Agricultura Sinica, 2022, 55(9): 1749-1762.
[6]	MA XiaoYan,YANG Yu,HUANG DongLin,WANG ZhaoHui,GAO YaJun,LI YongGang,LÜ Hui. Annual Nutrients Balance and Economic Return Analysis of Wheat with Fertilizers Reduction and Different Rotations [J]. Scientia Agricultura Sinica, 2022, 55(8): 1589-1603.
[7]	LI Qian,QIN YuBo,YIN CaiXia,KONG LiLi,WANG Meng,HOU YunPeng,SUN Bo,ZHAO YinKai,XU Chen,LIU ZhiQuan. Effect of Drip Fertigation Mode on Maize Yield, Nutrient Uptake and Economic Benefit [J]. Scientia Agricultura Sinica, 2022, 55(8): 1604-1616.
[8]	ZHANG JiaHua,YANG HengShan,ZHANG YuQin,LI CongFeng,ZHANG RuiFu,TAI JiCheng,ZHOU YangChen. Effects of Different Drip Irrigation Modes on Starch Accumulation and Activities of Starch Synthesis-Related Enzyme of Spring Maize Grain in Northeast China [J]. Scientia Agricultura Sinica, 2022, 55(7): 1332-1345.
[9]	TAN XianMing,ZHANG JiaWei,WANG ZhongLin,CHEN JunXu,YANG Feng,YANG WenYu. Prediction of Maize Yield in Relay Strip Intercropping Under Different Water and Nitrogen Conditions Based on PLS [J]. Scientia Agricultura Sinica, 2022, 55(6): 1127-1138.
[10]	LIU Miao,LIU PengZhao,SHI ZuJiao,WANG XiaoLi,WANG Rui,LI Jun. Critical Nitrogen Dilution Curve and Nitrogen Nutrition Diagnosis of Summer Maize Under Different Nitrogen and Phosphorus Application Rates [J]. Scientia Agricultura Sinica, 2022, 55(5): 932-947.
[11]	QIAO Yuan,YANG Huan,LUO JinLin,WANG SiXian,LIANG LanYue,CHEN XinPing,ZHANG WuShuai. Inputs and Ecological Environment Risks Assessment of Maize Production in Northwest China [J]. Scientia Agricultura Sinica, 2022, 55(5): 962-976.
[12]	HUANG ZhaoFu, LI LuLu, HOU LiangYu, GAO Shang, MING Bo, XIE RuiZhi, HOU Peng, WANG KeRu, XUE Jun, LI ShaoKun. Accumulated Temperature Requirement for Field Stalk Dehydration After Maize Physiological Maturity in Different Planting Regions [J]. Scientia Agricultura Sinica, 2022, 55(4): 680-691.
[13]	FANG MengYing,LU Lin,WANG QingYan,DONG XueRui,YAN Peng,DONG ZhiQiang. Effects of Ethylene-Chlormequat-Potassium on Root Morphological Construction and Yield of Summer Maize with Different Nitrogen Application Rates [J]. Scientia Agricultura Sinica, 2022, 55(24): 4808-4822.
[14]	DU WenTing,LEI XiaoXiao,LU HuiYu,WANG YunFeng,XU JiaXing,LUO CaiXia,ZHANG ShuLan. Effects of Reducing Nitrogen Application Rate on the Yields of Three Major Cereals in China [J]. Scientia Agricultura Sinica, 2022, 55(24): 4863-4878.
[15]	YI YingJie,HAN Kun,ZHAO Bin,LIU GuoLi,LIN DianXu,CHEN GuoQiang,REN Hao,ZHANG JiWang,REN BaiZhao,LIU Peng. The Comparison of Ammonia Volatilization Loss in Winter Wheat- Summer Maize Rotation System with Long-Term Different Fertilization Measures [J]. Scientia Agricultura Sinica, 2022, 55(23): 4600-4613.