? Identification of salinity-related genes in <em>ENO2</em> mutant (<em>eno2<sup>–</sup></em>) of <em>Arabidopsis thaliana</em>
Quick Search in JIA      Advanced Search  
    2018, Vol. 17 Issue (01): 94-110     DOI: 10.1016/S2095-3119(17)61720-9
Crop Science Current Issue | Next Issue | Archive | Adv Search Previous Articles  |  Next Articles  
Identification of salinity-related genes in ENO2 mutant (eno2) of Arabidopsis thaliana
ZHANG Yong-hua1, CHEN Chao2, SHI Zi-han1, CHENG Hui-mei1, BING Jie1, MA Xiao-feng1, ZHENG Chao-xing1, LI Hong-jie3, ZHANG Gen-fa1  
1 Beijing Key Laboratory of Gene Resource and Molecular Development/College of Life Sciences, Beijing Normal University, Beijing 100875, P.R.China
2 Beijing Normal University, Zhuhai 519087, P.R.China
3 National Key Facility for Crop Gene Resources and Genetic Improvement/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
 Download: PDF in ScienceDirect (0 KB)   HTML (1 KB)   Export: BibTeX | EndNote (RIS)      Supporting Info
Abstract Abiotic stress poses a great threat to plant growth and can lead to huge losses in yield.  Gene enolase2 (ENO2) is important in resistance to abiotic stress in various organisms.  ENO2 T-DNA insertion mutant (eno2) plants of Arabidopsis thaliana showed complete susceptibility to sodium chloride treatment when were analyzed either as whole plants or by measuring root growth during NaCl treatment.  Quantitative real-time RT-PCR (RT-qPCR) was performed to investigate the expression profile of ENO2 in response to NaCl stress in Arabidopsis.  The transcript level of ENO2 was rapidly elevated in 300 mmol L–1 NaCl treatment.  ENO2 also responded to 300 mmol L–1 NaCl treatment at the protein level.  To illuminate the mechanism underlying ENO2 resistance to salt at the transcriptional level, we studied the wild-type and eno2 Arabidopsis lines that were treated with 300 mmol L–1 NaCl for 18 h using 454 GS FLX, which resulted in an expressed sequence tag (EST) dataset.  A total of 961 up-regulated and 746 down-regulated differentially expressed genes (DEGs) were identified in the pairwise comparison WT-18 h:eno2-18 h.  The DEGs were identified and functionally annotated using the databases of Gene Ontology (GO) and the Kyoto encyclopedia of genes and genomes (KEGG).  The identified unigenes were subjected to GO analysis to determine biological, molecular, and cellular functions.  The biological process was enriched in a total of 20 GO terms, the cellular component was enriched in 13 GO terms, and the molecular function was enriched in 11 GO terms.  Using KEGG mapping, DEGs with pathway annotations contributed to 115 pathways.  The top 3 pathways based on a statistical analysis were biosynthesis of the secondary metabolites (KO01110), plant-pathogen interactions (KO04626), and plant hormone signal transduction (KO04075).  Based on these results, ENO2 contributes to increased resistance to abiotic stress.  In particular, ENO2 is involved in some of the metabolic stress response pathways in Arabidopsis.  Our work also demonstrates that this EST dataset will be a powerful resource for further studies of ENO2, such as functional analyses, investigations of biological roles, and molecular breeding.  Additionally, 3-phosphoglycerate kinase (PGK), 3-phosphoglycerate kinase 1 (PGK1), triosephosphate isomerase (TPI), and pyruvate kinase (PK) in glycolysis interactions with ENO2 were verified using the yeast two-hybrid experiment, and ENO2 may regulate the expression of PGK, PGK1, TPI, and PK.  Taken together, the results from this study reflects that ENO2 gene has an important role in the response to the high salt stress.
E-mail this article
Add to my bookshelf
Add to citation manager
E-mail Alert
Articles by authors
Key wordsENO2     NaCl tolerance     abiotic stress     454 GS FLX sequencing     GO     KEGG     
Received: 2016-12-06; Published: 2017-05-05

This study was funded by the National Natural Science Foundation of China (31470399 and 31270365).

Corresponding Authors: Correspondence ZHANG Gen-fa, Tel: +86-10-58809453, E-mail: gfzh@bnu.edu.cn; LI Hong-jie, Tel: +86-10-82105321, E-mail: lihongjie@caas.cn   
Cite this article:   
ZHANG Yong-hua, CHEN Chao, SHI Zi-han, CHENG Hui-mei, BING Jie, MA Xiao-feng, ZHENG Chao-xing, LI Hong-jie, ZHANG Gen-fa. Identification of salinity-related genes in ENO2 mutant (eno2) of Arabidopsis thaliana[J]. Journal of Integrative Agriculture, 2018, 17(01): 94-110.
http://www.chinaagrisci.com/Jwk_zgnykxen/EN/ 10.1016/S2095-3119(17)61720-9      or     http://www.chinaagrisci.com/Jwk_zgnykxen/EN/Y2018/V17/I01/94
[1] Ahmad P, Prasad M N. 2012. Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability. Springer-Verlag, New York.
[2] Ahmad P, Rasool S, Gul A, Sheikh S A, Akram N A, Ashraf M, Kazi A M, Gucel S. 2016. Jasmonates: Multifunctional roles in stress tolerance. Frontiers in Plant Science, 7, 813.
[3] Altschul S F. 1993. A protein alignment scoring system sensitive at all evolutionary distances. Journal of Molecular Evolution, 3, 290-300.
[4] Amtmann A, Troufflard S, Armengaud P. 2008. The effect of potassium nutrition on pest and disease resistance in plants. Plant Physiology, 4, 682-691.
[5] Andriotis V M, Kruger N J, Pike M J, Smith A M. 2010. Plastidial glycolysis in developing Arabidopsis embryos. New Phytologist, 3, 649-662.
[6] Atkinson N J, Urwin P E. 2012. The interaction of plant biotic and abiotic stresses: From genes to the field. Journal of Experimental Botany, 10, 3523-3543.
[7] Banerjee A, Roychoudhury A. 2015. WRKY proteins: Signaling and regulation of expression during abiotic stress responses. Scientific World Journal, 2015, 807560.
[8] Banks R D, Blake C C, Evans P R, Haser R, Rice D W, Hardy G W, Merrett M, Phillips A W. 1979. Sequence, structure and activity of phosphoglycerate kinase: A possible hinge-bending enzyme. Nature, 279, 773-777.
[9] Barkla B J, Vera-Estrella R, Hernández-Coronado M, Pantoja O. 2009. Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. The Plant Cell, 12, 4044-4058.
[10] Bent A F, Mackey D. 2007. Elicitors, effectors, and R genes: The new paradigm and a lifetime supply of questions. Annual Review of Phytopathology, 45, 399-436.
[11] Blakeley S D, Dekroon C, Cole K P, Kraml M, Dennis D T. 1994. Isolation of a full-length cDNA encoding cytosolic enolase from Ricinus communis. Plant Physiology, 1, 455-456.
[12] Blomberg A, Adler L. 1993. Tolerance of fungi to NaCl. In: Jennings D H, ed., Stress Tolerance of Fungi. Marcel Dekker, New York. pp. 209-232.
[13] Bray A. 1997. Plant responses to water deficit. Trends in Plant Science, 2, 48-54.
[14] Bray E A, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stresses. In: Gruissem W, Buchnnan B, Jones R, eds., Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD. pp. 1158-1249.
[15] Caruso G, Cavaliere C, Guarino C, Gubbiotti R, Foglia P, Laganà A. 2008. Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Analytical and Bioanalytical Chemistry, 1, 381-390.
[16] Conesa A, Götz S, García-Gómez J M, Terol J, Talón M, Robles M. 2005. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 18, 3674-3676.
[17] Eremina M, Rozhon W, Poppenberger B. 2016. Hormonal control of cold stress responses in plants. Cellular and Molecular Life Sciences, 4, 797-810.
[18] Eremina M, Rozhon W, Yang S, Poppenberger B. 2015. ENO2 activity is required for the development and reproductive success of plants, and is feedback-repressed by AtMBP-1. The Plant Journal, 6, 895-906.
[19] Fones H, Davis C A, Rico A, Fang F, Smith J A, Preston G M. 2010. Metal hyperaccumulation armors plants against disease. PLoS Pathogens, 9, e1001093.
[20] Holland M J, Holland J P. 1978. Isolation and identification of yeast messenger ribonucleic acids coding for enolase, glyceraldehyde-3-phosphate dehydrogenase, and phosphoglycerate kinase. Biochemistry, 23, 4900-4907.
[21] Huang G T, Ma S L, Bai L P, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo Z F. 2012. Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 2, 969-987.
[22] Jiang Y, Yang B, Harris N S, Deyholos M K. 2007. Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. Journal of Experimental Botany, 13, 3591-3607.
[23] Joshi R, Karan R, Singla-Pareek S L, Pareek A. 2016. Ectopic expression of Pokkali phosphoglycerate kinase-2 (OsPGK2-P) improves yield in tobacco plants under salinity stress. Plant Cell Reports, 1, 27-41.
[24] Kang M, Abdelmageed H, Lee S, Reichert A, Mysore K S, Allen R D. 2013. AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. The Plant Journal, 3, 481-493.
[25] Khan M N, Sakata K, Komatsu S. 2015. Proteomic analysis of soybean hypocotyl during recovery after flooding stress. Journal of Proteomics, 121, 15-27.
[26] Kissoudis C, van de Wiel C, Visser R G, van der Linden G. 2014. Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk. Frontiers in Plant Science, 5, 207.
[27] Lal S K, Johnson S, Conway T, Kelley P M. 1991. Characterization of a maize cDNA that complements an enolase-deficient mutant of Escherichia coli. Plant Molecular Biology, 5, 787-795.
[28] Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu K. 2002. LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional ENOLASE. EMBO Journal, 11, 2692-2702.
[29] Li T, Hu Y, Du X, Tang H, Shen C, Wu J. 2014. Salicylic acid alleviates the adverse effects of salt stress in Torreya grandis cv. Merrillii seedlings by activating photosynthesis and enhancing antioxidant systems. PLOS ONE, 10, e109492.
[30] Li W, Zhang C, Lu Q, Wen X, Lu C. 2011. The combined effect of salt stress and heat shock on proteome pro?ling in Suaeda salsa. Journal of Plant Physiology, 15, 1743-1752.
[31] Lin J W, Ding M P, Hsu Y H, Tsai C H. 2007. Chloroplast phosphoglycerate kinase, a gluconeogenetic enzyme, is required for efficient accumulation of Bamboo mosaic virus. Nucleic Acids Research, 35, 424-432.
[32] Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He Z H. 2013. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 38, 15485-15490.
[33] McHarg J, Kelly S M, Price N C, Cooper A, Littlechild J A. 1999. Site-directed mutagenesis of proline 204 in the ‘hinge’ region of yeast phosphoglycerate kinase. European Journal of Biochemistry, 259, 939-945.
[34] Mickelbart M V, Hasegawa P M, Bailey-Serres J. 2015. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nature Reviews Genetics, 4, 237-251.
[35] Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends in Plant Science, 1, 15-19.
[36] Mittler R, Blumwald E. 2010. Genetic engineering for modern agriculture: Challenges and perspectives. Annual Review of Plant Biology, 61, 443-462.
[37] Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. 2012. NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta, 2, 97-103.
[38] Ndimba B K, Chivasa S, Simon W J, Slabas A R. 2005. Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics, 16, 4185-4196.
[39] Pieterse C M, van der Does D, Zamioudis C, Leon-Reyes A, van Wees S C. 2012. Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology, 28, 489-521.
[40] Pirbalouti A G, Mirbagheri H, Hamedi B, Rahimi E. 2014. Antibacterial activity of the essential oils of myrtle leaves against Erysipelothrix rhusiopathiae. Asian Pacific Journal of Tropical Biomedicine, 4, 505-509.
[41] Poschenrieder C, Tolrà R, Barceló J. 2006. Can metals defend plants against biotic stress? Trends in Plant Science, 6, 288-295.
[42] Rangan P, Subramani R, Kumar R, Singh A K, Singh R. 2014. Recent advances in polyamine metabolism and abiotic stress tolerance. Biomed Research International, 2014, 239621.
[43] Reed G H, Poyner R R, Larsen T M, Wedekind J E, Rayment I. 1996. Structural and mechanistic studies of enolase. Current Opinion in Structural Biology, 6, 736-743.
[44] Robert-Seilaniantz A, Grant M, Jones J D. 2011. Hormone crosstalk in plant disease and defense: More than just JASMONATE-SALICYLATE antagonism. Annual Review of Phytopathology, 49, 317-343.
[45] Rothberg J M, Leamon J H. 2008. The development and impact of 454 sequencing. Nature Biotechnology, 26, 1117-1124.
[46] Sachs M M, Freeling M, Okimoto R. 1980. The anaerobic proteins of maize. Cell, 3, 761-767.
[47] Schaller G E, Kieber J J, Shiu S H. 2008. Two-component signaling elements and histidyl-aspartyl phosphorelays. Arabidopsis Book, 6, e0112.
[48] Schaller M. 2011. The behavioral immune system and the psychology of human sociality. Philosophical Transactions of the Royal Society of London Series B (Biological Sciences), 1583, 3418-3426.
[49] Sharma S, Mustafiz A, Singla-Pareek S L, Srivastava P S, Sopory S K. 2012. Characterization of stress and methylglyoxal inducible triose phosphate isomerase (OscTPI) from rice. Plant Signaling & Behavior, 10, 1337-1345.
[50] Shao H, Wang H, Tang X. 2015. NAC transcription factors in plant multiple abiotic stress responses: Progress and prospects. Frontiers in Plant Science, 6, 902.
[51] Shi H, Ye T, Chen F, Cheng Z, Wang Y, Yang P, Zhang Y, Chan Z. 2013. Manipulation of arginase expression modulates abiotic stress tolerance in Arabidopsis: Effect on arginine metabolism and ROS accumulation. Journal of Experimental Botany, 5, 1367-1379.
[52] Shinozaki K, Yamaguchi-Shinozaki K, Seki M. 2003. Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology, 5, 410-417.
[53] Souman M F, Kostandi S F. 1998. Effect of saline environment on yield and smut disease severity of different corn genotypes (Zea mays L.). Journal of Phytopathology, 4, 185-189.
[54] van der Straeten D, Rodrigues-Pousada R A, Goodman H M, van Montagu M. 1991. Plant enolase: Gene structure, expression and evolution. The Plant Cell, 7, 719-735.
[55] Umeda M, Uchimiya H. 1994. Differential transcript levels of genes associated with glycolysis and alcohol fermentation in rice plants (Oryza sativa L.) under submergence stress. Plant Physiology, 3, 1015-1022.
[56] Voll L M, Hajirezaei M R, Czogalla-Peter C, Lein W, Stitt M, Sonnewald U, Börnke F. 2009. Antisense inhibition of enolase strongly limits the metabolism of aromatic amino acids, but has only minor effects on respiration in leaves of transgenic tobacco plants. New Phytologist, 3, 607-618.
[57] Wang H, Wang H, Shao H, Tang X. 2016. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Frontiers in Plant Science, 7, 67.
[58] Wei L J, Deng X G, Zhu T, Zheng T, Li P X, Wu J Q, Zhang D W, Lin H H. 2015. Ethylene is involved in Brassinosteroids induced alternative respiratory pathway in cucumber (Cucumis sativus L.) seedlings response to abiotic stress. Frontiers in Plant Science, 6, 982.
[59] Yan S P, Tang Z, Su W, Sun W. 2005. Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics, 1, 235-244.
No Similar of article
Copyright © 2015 ChinaAgriSci.com, All Rights Reserved
Chinese Academy of Agricultural Sciences (CAAS) No. 12 South Street, Zhongguancun, Beijing 100081, P. R. China
http://www.ChinaAgriSci.com   JIA E-mail: jia_journal@caas.cn