EMS mutagenesis; SSR markers; plant hormone; premature leaf senescence; tobacco; Ecology, Evolution, Behavior and Systematics; Ecology; Plant Science
Abstract :
[en] As the last stage of plant development, leaf senescence has a great impact on plant's life cycle. Genetic manipulation of leaf senescence has been used as an efficient approach in improving the yield and quality of crop plants. Here we describe an ethyl methane sulfonate (EMS) mutagenesis induced premature leaf senescence mutant yellow leaf 1 (yl1) in common tobacco (Nicotiana tabacum L.). The yl1 plants displayed early leaf yellowing. Physiological parameters and marker genes expression indicated that the yl1 phenotype was caused by premature leaf senescence. Genetic analyses indicated that the yl1 phenotype was controlled by a single recessive gene that was subsequently mapped to a specific interval of tobacco linkage group 11 using simple sequence repeat (SSR) markers. Exogenous plant hormone treatments of leaves showed that the yl1 mutant was more sensitive to ethylene and jasmonic acid than the wild type. No similar tobacco premature leaf senescence mutants have been reported. This study laid a foundation for finding the gene controlling the mutation phenotype and revealing the molecular regulation mechanism of tobacco leaf senescence in the next stage.
Disciplines :
Agriculture & agronomy
Author, co-author :
Gao, Xiaoming ✱; Université de Liège - ULiège > TERRA Research Centre ; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Wu, Xinru ✱; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Liu, Guanshan; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Zhang, Zenglin; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Chao, Jiangtao; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Li, Zhiyuan ; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Guo, Yongfeng ; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
Sun, Yuhe; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, China
✱ These authors have contributed equally to this work.
Language :
English
Title :
Characterization and Mapping of a Novel Premature Leaf Senescence Mutant in Common Tobacco (Nicotiana tabacum L.).
NSCF - National Natural Science Foundation of China [CN]
Funding text :
This research was funded by the Science Foundation for Young Scholars of Tobacco Research Institute of Chinese Academy of Agricultural Sciences, grant number 2017B07; and the Agricultural Science and Technology Innovation Program, grant number ASTIP-TRIC02.Funding: This research was funded by the Science Foundation for Young Scholars of Tobacco Research Institute of Chinese Academy of Agricultural Sciences, grant number 2017B07; and the Agricultural Science and Technology Innovation Program, grant number ASTIP-TRIC02.
Masclaux, C.; Valadier, M.H.; Brugière, N.; Morot-Gaudry, J.F.; Hirel, B. Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 2000, 211, 510–518.
Edwards, K.D.; Bombarely, A.; Story, G.W.; Allen, F.; Mueller, L.A.; Coates, S.A.; Jones, L. TobEA: An atlas of tobacco gene expression from seed to senescence. BMC Genom. 2010, 11, 142.
Arntzen, C.J. Using tobacco to treat cancer. Science 2008, 321, 1052–1053.
Monreal-Escalante, E.; Ramos-Vega, A.A.; Salazar-Gonzalez, J.A.; Banuelos-Hernandez, B.; Angulo, C.; Rosales-Mendoza, S. Expression of the VP40 antigen from the Zaire ebolavirus in tobacco plants. Planta 2017, 246, 123–132.
Budzianowski, J. Tobacco against Ebola virus disease. Przegl. Lek. 2015, 72, 567–571.
Vanhercke, T.; El Tahchy, A.; Liu, Q.; Zhou, X.R.; Shrestha, P.; Divi, U.K.; Ral, J.P.; Mansour, M.P.; Nichols, P.D.; James, C.N. et al. Metabolic engineering of biomass for high energy density: Oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol. J. 2014, 12, 231–239.
Fuchs, J.; Neuberger, T.; Rolletschek, H.; Schiebold, S.; Nguyen, T.H.; Borisjuk, N.; Borner, A.; Melkus, G.; Jakob, P.; Borisjuk, L. A noninvasive platform for imaging and quantifying oil storage in submillimeter tobacco seed. Plant Physiol. 2013, 161, 583–593.
Andrianov, V.; Borisjuk, N.; Pogrebnyak, N.; Brinker, A.; Dixon, J.; Spitsin, S.; Flynn, J.; Matyszczuk, P.; Andryszak, K.; Laurelli, M. et al. Tobacco as a production platform for biofuel: Overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass. Plant Biotechnol. J. 2010, 8, 277–287.
Li, W.; Zhang, H.L.; Li, X.X.; Zhang, F.X.; Liu, C.; Du, Y.M.; Gao, X.M.; Zhang, Z.L.; Zhang, X.B.; Hou, Z.H. et al. Intergrative metabolomic and transcriptomic analyses unveil nutrient remobilization events in leaf senescence of tobacco. Sci. Rep. 2017, 7, 12126.
Zhao, J.Y.; Li, L.L.; Zhao, Y.N.; Zhao, C.X.; Chen, X.; Liu, P.P.; Zhou, H.N.; Zhang, J.J.; Hu, C.X.; Chen, A.G. et al. Metabolic changes in primary, secondary, and lipid metabolism in tobacco leaf in response to topping. Anal. Bioanal. Chem. 2018, 410, 839–851.
Zhao, Z.; Li, Y.F.; Zhao, S.C.; Zhang, J.W.; Zhang, H.; Fu, B.; He, F.; Zhao, M.Q.; Liu, P.F. Transcriptome Analysis of Gene Expression Patterns Potentially Associated with Premature Senescence in Nicotiana tabacum L. Molecules 2018, 23, 2856.
Li, L.L.; Zhao, J.Y.; Zhao, Y.N.; Lu, X.; Zhou, Z.H.; Zhao, C.X.; Xu, G.W. Comprehensive investigation of tobacco leaves during natural early senescence via multi-platform metabolomics analyses. Sci. Rep. 2016, 6, 37976.
Lim, P.O.; Kim, H.J.; Gil Nam, H. Leaf Senescence. Annu. Rev. Plant Biol. 2007, 58, 115–136.
Gan, S.S.; Amasino, R.M. Making Sense of Senescence (Molecular Genetic Regulation and Manipulation of Leaf Senescence). Plant Physiol. 1997, 113, 313–319.
Ali, A.; Gao, X.M.; Guo, Y.F. Initiation, Progression, and Genetic Manipulation of Leaf Senescence. Methods Mol. Biol. 2018, 1744, 9–31.
Guo, Y.; Cai, Z.; Gan, S. Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 2004, 27, 521–549.
Jibran, R.; Hunter, D.A.; Dijkwel, P.P. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Boil. 2013, 82, 547–561.
Yolcu, S.; Li, X.; Li, S.; Kim, Y.J. Beyond the genetic code in leaf senescence. J. Exp. Bot. 2018, 69, 801–810.
Wingler, A.; Masclaux-Daubresse, C.; Fischer, A.M. Sugars, senescence, and ageing in plants and heterotrophic organisms. J. Exp. Bot. 2009, 60, 1063–1066.
Guo, Y.F.; Gan, S.S. Translational researches on leaf senescence for enhancing plant productivity and quality. J. Exp. Bot. 2014, 65, 3901–3913.
Gregersen, P.L.; Culetic, A.; Boschian, L.; Krupinska, K. Plant senescence and crop productivity. Plant Mol. Biol. 2013, 82, 603–622.
Hortensteiner, S.; Krautler, B. Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 2011, 1807, 977–988.
Breeze, E.; Harrison, E.; McHattie, S.; Hughes, L.; Hickman, R.; Hill, C.; Kiddle, S.; Kim, Y.S.; Penfold, C.A.; Jenkins, D. et al. High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation. Plant. Cell 2011, 23, 873–894.
Noh, Y.S.; Amasino, R.M. Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol. Biol. 1999, 41, 181–194.
Jan, S.; Abbas, N.; Ashraf, M.; Ahmad, P. Roles of potential plant hormones and transcription factors in controlling leaf senescence and drought tolerance. Protoplasma 2019, 256, 313–329.
Khan, M.; Rozhon, W.; Poppenberger, B. The role of hormones in the aging of plants—A mini-review. Gerontology 2014, 60, 49–55.
Bindler, G.; Plieske, J.; Bakaher, N.; Gunduz, I.; Ivanov, N.; van der Hoeven, R.; Ganal, M.; Donini, P. A high density genetic map of tobacco (Nicotiana tabacum L.) obtained from large scale microsatellite marker development. Theor. Appl. Genet. 2011, 123, 219–230.
Bindler, G.; van der Hoeven, R.; Gunduz, I.; Plieske, J.; Ganal, M.; Rossi, L.; Gadani, F.; Donini, P. A microsatellite marker based linkage map of tobacco. Theor. Appl. Genet. 2007, 114, 341–349.
Tong, Z.J.; Yang, Z.M.; Chen, X.J.; Jiao, F.C.; Li, X.Y.; Wu, X.F.; Gao, Y.L.; Xiao, B.G.; Wu, W.W. Large-scale development of microsatellite markers in nicotiana tabacum and construction of a genetic map of flue-cured tobacco. Plant Breed. 2012, 131, 674–680.
Lan, T.; Zheng, S.F.; Yang, L.; Wu, S.X.; Wang, B.; Zhang, S.J.; Tong, Z.J.; Chen, Y.Z.; Chen, S.H.; Duan, Y.L. et al. Mapping of quantitative trait loci conferring resistance to bacterial wilt in tobacco (Nicotiana tabacum L.). Plant Breed. 2014, 133, 672–677.
Sun, M.M.; Cheng, L.R.; Jiang, C.H.; Zhu, C.G.; Ren, M.; Zhang, Y.S.; Zhang, Y.; Liu, D.; Zhao, Q.; Geng, R.M. et al. Identification of a major QTL affecting resistance to brown spot in tobacco (Nicotiana tabacum L.) via linkage and association mapping methods. Euphytica 2018, 214, 195–208.
Tong, Z.J.; Jiao, T.L.; Wang, F.Q.; Li, M.Y.; Leng, X.D.; Gao, Y.L.; Li, Y.P.; Xiao, B.G.; Wu, W.R. Mapping of quantitative trait loci conferring resistance to brown spot in flue-cured tobacco (Nicotiana tabacum L.). Plant Breed. 2012, 131, 335–339.
Vontimitta, V.; Lewis, R.S. Mapping of quantitative trait loci affecting resistance to Phytophthora nicotianae in tobacco (Nicotiana tabacum L.) line Beinhart-1000. Mol. Breed. 2012, 29, 89–98.
Cheng, L.R.; Yang, A.G.; Jiang, C.H.; Ren, M.; Zhang, Y.; Feng, Q.F.; Wang, S.M.; Guan, Y.S.; Luo, C. Quantitative trait loci mapping for plant height in tobacco using linkage and association mapping methods. Crop. Sci. 2015, 55, 641–647.
Kalivas, A.; Ganopoulos, I.; Bosmali, I.; Tsaliki, E.; Osathanunkul, M.; Xanthopoulou, A.; Moysiadis, T.; Avramidou, E.; Grigoriadis, I.; Zambounis, A. et al. Genetic diversity and structure of tobacco in greece on the basis of morphological and microsatellite markers. Crop. Sci. 2016, 56, 2652–2662.
Tong, Z.J.; Xiao, B.G.; Chen, X.J.; Fang, D.H.; Zhang, Y.H.; Huang, C.J.; Li, Y.P. Construction of a genetic linkage map of cigar tobacco (Nicotiana tabacum L.) based on SSR markers and comparative studies. Czech. J. Genet. Plant Breed. 2018, 54, 115–122.
Leitch, I.J.; Hanson, L.; Lim, K.Y.; Kovarik, A.; Chase, M.W.; Clarkson, J.J.; Leitch, A.R. The ups and downs of genome size evolution in polyploid species of Nicotiana (Solanaceae). Ann. Bot. 2008, 101, 805–814.
Renny-Byfield, S.; Chester, M.; Kovarik, A.; Le Comber, S.C.; Grandbastien, M.A.; Deloger, M.; Nichols, R.A.; Macas, J.; Novak, P.; Chase, M.W. et al. Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol. Biol. Evol. 2011, 28, 2843–2854.
Wu, Q.Z.; Wu, X.R.; Zhang, X.F.; Jiang, C.H.; Xiao, B.G.; Zhang, Y.Y.; Wang, Y.Y.; Liu, G.S. Mapping of two white stem genes in tetraploid common tobacco (Nicotiana tabacum L.). Mol. Breed. 2014, 34, 1065–1074.
Michel, V.; Julio, E.; Candresse, T.; Cotucheau, J.; Decorps, C.; Volpatti, R.; Moury, B.; Glais, L.; Dorlhac de Borne, F.; Decroocq, V. et al. NtTPN1: A RPP8-like R gene required for Potato virus Y-induced veinal necrosis in tobacco. Plant J. 2018, 95, 700–714.
Bao, Y.G.; Ding, N.; Qin, Q.L.; Wu, X.; Martinez, N.; Miller, R.; Zaitlin, D.; Li, D.D.; Yang, S.M. Genetic mapping of the Ph gene conferring disease resistance to black shank in tobacco. Mol. Breed. 2019, 39, 122–131.
Wang, X.W.; Yang, S.; Chen, Y.D.; Zhang, S.M.; Zhao, Q.S.; Li, M.; Gao, Y.L.; Yang, L.; Bennetzen, J.L. Comparative genome-wide characterization leading to simple sequence repeat marker development for Nicotiana. BMC Genom. 2018, 19, 500.
Xiao, B.G.; Tan, Y.T.; Long, N.; Chen, X.J.; Tong, Z.J.; Dong, Y.; Li, Y.P. SNP-based genetic linkage map of tobacco (Nicotiana tabacum L.) using next-generation RAD sequencing. J. Biol. Res. Thessalon. 2015, 22, 11.
Gong, D.P.; Huang, L.; Xu, X.H.; Wang, C.Y.; Ren, M.; Wang, C.K.; Chen, M.L. Construction of a high-density SNP genetic map in flue-cured tobacco based on SLAF-seq. Mol. Breed. 2016, 36, 100.
Thimmegowda, G.C.; Ramadoss, S.K.; Kaikala, V.; Rathinavelu, R. Whole genome resequencing of tobacco (Nicotiana tabacum L.) genotypes and high-throughput SNP discovery. Mol. Breed. 2018, 38, 121.
Cheng, L.R.; Chen, X.C.; Jiang, C.H.; Ma, B.; Ren, M.; Cheng, Y.Z.; Liu, D.; Geng, R.M.; Yang, A.G. High-density SNP genetic linkage map construction and quantitative trait locus mapping for resistance to cucumber mosaic virus in tobacco (Nicotiana tabacum L.). Crop. J. 2019, 7, 539–547.
Reinbothe, C.; Springer, A.; Samol, I.; Reinbothe, S. Plant oxylipins: Role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J. 2009, 276, 4666–4681.
Hu, Y.R.; Jiang, Y.J.; Han, X.; Wang, H.P.; Pan, J.J.; Yu, D.Q. Jasmonate regulates leaf senescence and tolerance to cold stress: Crosstalk with other phytohormones. J. Exp. Bot. 2017, 68, 1361–1369.
Jiang, Y.J.; Liang, G.; Yang, S.Z.; Yu, D.Q. Arabidopsis wrky57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 2014, 26, 230–245.
Xie, Y.; Huhn, K.; Brandt, R.; Potschin, M.; Bieker, S.; Straub, D.; Doll, J.; Drechsler, T.; Zentgraf, U.; Wenkel, S. REVOLUTA and WRKY53 connect early and late leaf development in Arabidopsis. Development 2014, 141, 4772–4783.
Wang, D.W.; Wang, S.M.; Chao, J.T.; Wu, X.R.; Sun, Y.H.; Li, F.X.; Lv, J.; Gao, X.M.; Liu, G.S.; Wang, Y.Y. Morphological phenotyping and genetic analyses of a new chemical-mutagenized population of tobacco (Nicotiana tabacum L.). Planta 2017, 246, 149–163.
He, Y.H.; Gan, S.S. A Gene Encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 2002, 14, 805–815.
Edwards, K.D.; Fernandez-Pozo, N.; Drake-Stowe, K.; Humphry, M.; Evans, A.D.; Bombarely, A.; Allen, F.; Hurst, R.; White, B.; Kernodle, S.P. et al. A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genom. 2017, 18, 448.
Bassam, B.J.; Caetano-Anolles, G.; Gresshoff, P.M. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal. Biochem. 1991, 196, 80–83.
Li, H.H.; Ribaut, J.M.; Li, Z.L.; Wang, J.K. Inclusive composite interval mapping (ICIM) for digenic epistasis of quantitative traits in biparental populations. Theor. Appl. Genet. 2008, 116, 243–260.
