|
|
|
|
|
| EaIspF1, Essential Enzyme in Isoprenoid Biosynthesis from Eupatorium adenophorum, Reveals a Novel Role in Light Acclimation |
| ZHANG Sheng-rui, JIANG Xue, WANG Ping, WU Di, WANG Qing-hua , HOU Yu-xia |
| College of Science, China Agricultural University, Beijing 100193, P.R.China |
|
|
|
摘要 Isoprenoids are a functionally and structurally diverse class of natural organic chemicals. The universal precursors of all isoprenoids, isopentenyl diphosphate and dimethylallyl diphosphate are synthesized through the mevalonate and 2C-methyl- D-erythritol 4-phosphate (MEP) pathways, respectively. Many isoprenoids produced through the MEP pathway play an important role in plant acclimation to different light environments. Eupatorium adenophorum, an invasive weed in China, presents a remarkable capacity to acclimate to various light environments, which constitutes its solid foundation of being a successful invasive species. Thus we aimed at gaining a deeper insight into the regulation of MEP pathway in E. adenophorum to further understand the invasive mechanism. 2C-Methyl-D-erythritol 2,4-cyclodiphosphate synthase (IspF or MCS) is an essential enzyme in the MEP pathway. In this paper, a novel IspF gene was cloned and characterized from E. adenophorum. Tissue-specific expression assays revealed a higher expression of EaIspF1 in leaves than in stems and roots. The expression of EaIspF1 was responsive to different light conditions. Some up-regulation of EaIspF1 expression was also found after the treatments with signal compounds and after wounding stress. Interestingly, the over-expression of EaIspF1 in Arabidopsis led to increase carotenoids contents, resulting in an enhanced tolerance to high light. Taken together, these results indicate that the EaIspF1-derived enzyme participates in isoprenoid metabolism and among others, the expression of this gene in E. adenophorum is involved in the regulation of plastidial isoprenoids, which play an important role in acclimation to various light environments.
Abstract Isoprenoids are a functionally and structurally diverse class of natural organic chemicals. The universal precursors of all isoprenoids, isopentenyl diphosphate and dimethylallyl diphosphate are synthesized through the mevalonate and 2C-methyl- D-erythritol 4-phosphate (MEP) pathways, respectively. Many isoprenoids produced through the MEP pathway play an important role in plant acclimation to different light environments. Eupatorium adenophorum, an invasive weed in China, presents a remarkable capacity to acclimate to various light environments, which constitutes its solid foundation of being a successful invasive species. Thus we aimed at gaining a deeper insight into the regulation of MEP pathway in E. adenophorum to further understand the invasive mechanism. 2C-Methyl-D-erythritol 2,4-cyclodiphosphate synthase (IspF or MCS) is an essential enzyme in the MEP pathway. In this paper, a novel IspF gene was cloned and characterized from E. adenophorum. Tissue-specific expression assays revealed a higher expression of EaIspF1 in leaves than in stems and roots. The expression of EaIspF1 was responsive to different light conditions. Some up-regulation of EaIspF1 expression was also found after the treatments with signal compounds and after wounding stress. Interestingly, the over-expression of EaIspF1 in Arabidopsis led to increase carotenoids contents, resulting in an enhanced tolerance to high light. Taken together, these results indicate that the EaIspF1-derived enzyme participates in isoprenoid metabolism and among others, the expression of this gene in E. adenophorum is involved in the regulation of plastidial isoprenoids, which play an important role in acclimation to various light environments.
|
|
Received: 19 March 2013
Accepted:
|
| Fund: This work was supported by a Public-Agricultural Research Project, Ministry of Agriculture, China (201103027) and the Genetically Modified Organism Breeding Major Project, Ministry of Agriculture, China (2013ZX08005002). |
|
Corresponding Authors:
HOU Yu-xia, Tel/Fax: +86-10-62733824, E-mail: houyuxia@tsinghua.org.cn
E-mail: houyuxia@tsinghua.org.cn
|
| About author: ZHANG Sheng-rui, E-mail: Shengruizhang@cau.edu.cn |
Cite this article:
ZHANG Sheng-rui, JIANG Xue, WANG Ping, WU Di, WANG Qing-hua , HOU Yu-xia.
2014.
EaIspF1, Essential Enzyme in Isoprenoid Biosynthesis from Eupatorium adenophorum, Reveals a Novel Role in Light Acclimation. Journal of Integrative Agriculture, 13(5): 1024-1035.
|
| Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: A web-based environment for protein structure homology modeling. Bioinformatics, 22, 195-201 Bouvier F, Rahier A, Camara B. 2005. Biogenesis, molecular regulation and function of plant isoprenoids. Progress in Lipid Research, 44, 357-429 Buetow L, Brown A C, Parish T, Hunter W N. 2007. The structure of Mycobacteria 2C-methyl-D-erythritol-2,4 cyclodiphosphate synthase, an essential enzyme, provides a platform for drug discovery BMC Structural Biology, 7, 68. Calisto B, Perez-Gil J, Bergua M, Querol-Audi J, Fita I, Imperial S. 2007. Biosynthesis of isoprenoids in plants: Structure of the 2C-methyl-D-erithrytol 2,4-cyclodiphosphate synthase from Arabidopsis thaliana. Comparison with the bacterial enzymes. Protein Science, 16, 2082-2088 Chaded K, Oudin A, Guivarc’h N, Hamdi S, Chénieux J C, Rideau M, Clastre M. 2000. 1-Deoxy-D-xylulose 5 phosphate synthase from periwinkle: cDNA identification and induced gene expression in terpenoid indole alkaloid producing cells. Plant Physiology and Biochemistry, 38, 559-566 Cheong Y H, Chang H, Cupta R, Wang X, Zhu T, Luan S. 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology, 129, 661-677 Cunningham F X. 2002. Regulation of carotenoid synthesis and accumulation in plants. Pure and Applied Chemistry, 74, 1409-1417 Cutler S R, Rodriguez P L, Finkelstein R R, Abrams S R. 2010. Abscisic acid: emergence of a core signaling network. Annual Reviews of Plant Biology, 61, 651-679 DellaPenna D, Pogson B J. 2006. Vitamin synthesis in plants: Tocopherols and carotenoids. Annual Review of Plant Biology, 57, 711-738 Demmig-Adams B, Adams III W W. 1996. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science, 1, 21-26 Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J. 2005. The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proceedings of the National Academy of Sciences of the United States of America, 102, 933-938 Estévez J M, Cantero A, Reindl A, Reichler S, León P. 2001. 1-Deoxy-D-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants Journal of Biological Chemistry, 276, 22901- 22909. Enfissi E M A, Fraser P D, Lois L M, Boronat A, Schuch W, Bramley P M. 2005. Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnology Journal, 3, 17-27 Frank A H, Cogdell R J. 1996. Carotenoids in photosynthesis. Photochemistry and Photobiology, 63, 257-264 Gao S, Lin J, Liu X, Deng Z, Li Y, Sun X, Tang K. 2006. Molecular cloning, characterization and functional analysis of a 2C-methyl-D-erythritol 2, 4-cyclodiphosphate synthase gene from Ginkgo biloba. Journal of Biochemistry and Molecular Biology, 39, 502-510 Guo H, Ecker J R. 2003. The ethylene signaling pathway: new insights. Current Opinion of Plant Biology, 7, 40-49 Gupta P, Agarwal A V, Akhtar N, Sangwan R S, Singh S P, Trivedi K P. 2013. Cloning and characterization of 2-C-methyl-D-erthritol-4-phosphate pathway genes for isoprenoid biosynthesis from Indian ginseng, Withania somnifera Protoplasma, 250, 285-295 Havaux M, Niyogi K K. 1999. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proceedings of the National Academy of Sciences of the United States of America, 96, 8762-8767 Havaux M, Tardy F. 1996. Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: Possible involvement of xanthophyll-cycle pigments. Planta, 198, 324-333 Havaux M. 1998. Carotenoids as membrane stabilizers in chloroplasts. Trends in Plant Science, 3, 147-151 Herz S, Wungsintaweekul J, Schuhr M A, Hecht S, Lüttgen H, Sagner S, Fellermeier M, Eisenreich W, Zenk M H, Bacher A, Rohdich F. 2000. Biosynthesis of terpenoids: YgbB protein converts 4-diphosphocytidyl-2C-methyl- D-erythritol 2-phosphate to 2C-methyl-D-erythritol 2,4-cyclodiphosphate Proceedings of the National Academy of Sciences of the United States of America, 97, 2486-2490 Hsieh M, Goodman H M. 2006. Functional evidence for the involvement of Arabidopsis IspF homolog in the nonmevalonate pathway of plastid isoprenoid biosynthesis. Planta, 223, 779-784 Hurry V, Anderson J M, Chow W S, Osmond C B. 1997. Accumulation of zeaxanthin in abscisic acid-deficient mutants of Arabidopsis does not affect chlorophyll fluorescence quenching or sensitivity to photoinhibition in vivo. Plant Physiology, 113, 639-648 Kemp L E, Bond C S, Hunter WN. 2002. Structure of 2C-methyl-D-erythritol 2,4-cyclodiphosphate synthase: An essential enzyme for isoprenoid biosynthesis and target for antimicrobial drug development. Proceedings of the National Academy of Sciences of the United States of America, 99, 6591-6596 Kiefer F, Arnold K, Künzli M, Bordoli L, Schwede T. 2009. The SWISS-MODEL repository and associated resources. Nucleic Acids Research, 37, D387-D392. Kim C, Meskauskiene R, Zhang S, Lee P, Ashok M L, Blajecka K, Herrfurth C, Feussner I, Apel K. 2012. Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. The Plant Cell, 24, 3026-3039 Kumar K, Singh K, Kumar S. 2012. 2C-Methyl-D-erythritol 2,4-cyclodiphosphate synthase from Stevia rebaudiana Bertoni is a functional gene. Molecular Biology Reports, 39, 10971-10978 Lehmann C, Lim K, Toedt J, Krajewski W, Howard A, Eisenstein E, Herzberg O. 2002. Structure of 2C-methyl- D-erythrol-2,4-cyclodiphosphate synthase from Haemophilus influenzae: Activation by conformational transition Proteins: Structure, Function, and Bioinformatics, 49, 135-138. Liu W, Chen M, Yang C, Yang Y, Lan X, Liao Z. 2009. A new 2-C-methyl-D-erythritol 2,4-cyclodiphosphate s y n t h a s e gene from Taxus media : cloning, characterization and functional complementation. Journal of Medicinal Plants Research, 3, 395-402 Martin D M, Gershenzon J, Bohlmann J. 2003. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiology, 132, 1586-1599 Pateraki I, Kanellis A K. 2010. Stress and developmental responses of terpenoid biosynthetic genes in Cistus creticus subsp. creticus. Plant Cell Reports, 29, 629-641 Peitsch M C. 1995. Protein modeling by E-mail. Nature Biotechnology, 13, 658-660 Phillips M A, León P, Boronat A, Rodríguez-Concepción M. 2008. The plastidial MEP pathway: Unified nomenclature and resources. Trends in Plant Science, 12, 619-623 Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat J L, Havaux M. 2012. Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiology, 158, 1267- 1278. Rodríguez-Concepción M, Boronat A. 2002. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiology, 130, 1079-1089 Rodríguez-Concepción M. 2006. Early steps in isoprenoid biosynthesis: Multilevel regulation of the supply of common precursors in plant cells. Phytochemstry Reviews, 5, 1-15 Rohdich F, Wungsintaweekul J, Fellermeier M, Sagner S, Herz S, Kis K, Eisenreich W, Bacher A, Zenk M H. 1999. Cytidine 5´-triphosphate-dependent biosynthesis of isoprenoids: YgbP protein of Escherichia coli catalyzes the formation of 4-diphosphocytidyl-2C-methylerythritol Proceedings of the National Academy of Sciences of the United States of America, 96, 11758- 11763. Smith J L, de Moraes C M, Mescher M C. 2009. Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Management Science, 65, 497-503 Steinbacher S, Kaiser J, Wungsintaweekul J, Hecht S, Eisenreich W, Gerhardt S, Bacher A, Rohdich F. 2002. Structure of 2C-methyl-D-erythrol-2,4-cyclodiphosphate synthase inolved in mevalonate-independent biosynthesis of isoprenoids Journal of Molecular Biology, 316, 79- 88. Sunker R, Bartels D, Kirch H H. 2003. Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. Plant Journal, 35, 452-464 Veau B, Courtois M, Oudin A, Chénieux J C, Rideau M, Clastre M. 2000. Cloning and expression of cDNAs encoding two enzymes of the MEP pathway in Catharanthus roseus. Biochimica et Biophysica Acta, 1517, 159-163 Vickers C E, Gershenzon J, Lerdau M T, Loreto F. 2009. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nature Chemical Biology, 5, 283- 291. Wang J, Feng Y, Liang H. 2004. Adaptation of Eupatorium adenophorum photosynthetic characteristics to light intensity. Chinese Journal of Applied Ecology, 15, 1373- 1377. (in Chinese) Wang Q, Li F, Zhang X, Zhang X, Hou Y X, Zhang S R, Wu Z. 2011. Purification and characterization of a CkTLP protein from Cynanchum komarovii seeds that confers antifungal activity. PloS ONE, 6, e16930. Wang Q, Zhang X, Li F, Hou Y, Liu X, Zhang X. 2011. Identification of a UDP-glucose pyrophosphorylase from cotton (Gossypium hirsutum L.) involved in cellulose biosynthesis in Arabidopsis thaliana. Plant Cell Reports, 30, 1303-1312 Wang R, Wang Y 2006 Invasion dynamics and potential spread of the invasive alien plant species Ageratina adenophora (Asteraceae) in China Diversity and Distributions, 12, 397-408 Zavala J A, Baldwin I T. 2006. Jasmonic acid signaling and herbivore resistance traits constrain regrowth after herbivore attack in Nicotiana attenuate. Plant Cell & Environment, 29, 1751-1760. |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
