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Manipulation of DET1 expression in tomato results in photomorphogenic phenotypes caused by post‐transcriptional gene silencing
Summary
The tomato HIGH PIGMENT‐2 gene encodes an orthologue of the Arabidopsis nuclear protein DE‐ETIOLATED 1 (DET1). From genetic analyses it has been proposed that DET1 is a negative regulator of light signal transduction, and recent results indicate that it may control light‐regulated gene expression at the level of chromatin remodelling. To gain further understanding about the function of DET1 during plant development, we generated a range of overexpression constructs and introduced them into tomato. Unexpectedly, we only observed phenotypes characteristic of DET1 inactivation, i.e. hyper‐responsiveness to light. Molecular analysis indicated in all cases that these phenotypes were a result of suppression of endogenous DET1 expression, due to post‐transcriptional gene silencing. DET1 silencing was often lethal when it occurred at relatively early stages of plant development, whereas light hyper‐responsive phenotypes were obtained when silencing occurred later on. The appearance of phenotypes correlated with the generation of siRNAs but not DNA hypermethylation, and was most efficient when using constructs with mutations in the DET1 coding sequence or with constructs containing only the 3′‐terminal portion of the gene. These results indicate an important function for DET1 throughout plant development and demonstrate that silencing of DET1 in fruits results in increased carotenoids, which may have biotechnological potential.
Citing Literature
Number of times cited: 36
- Aisha Saleem Khan, Carotenoids, Flowering Plants, (189-212), (2017).
- Rajan Katoch, Sunil Kumar Singh and Neelam Thakur, Biotechnological Interventions for Improvement of Plant Nutritional Value: From Mechanisms to Applications, Phytonutritional Improvement of Crops, (83-111), (2017).
- Lihong Liu, Zhiyong Shao, Min Zhang, Tianyu Liu, Haoran Liu, Shuo Li, Yuanyuan Liu and Qiaomei Wang, Improvement of Carotenoid Accumulation in Tomato Fruit, Phytonutritional Improvement of Crops, (309-338), (2017).
- Xiaofeng Tang, Min Miao, Xiangli Niu, Danfeng Zhang, Xulv Cao, Xichen Jin, Yunye Zhu, Youhong Fan, Hongtao Wang, Ying Liu, Yuan Sui, Wenjie Wang, Anquan Wang, Fangming Xiao, Jim Giovannoni and Yongsheng Liu, Ubiquitin‐conjugated degradation of golden 2‐like transcription factor is mediated by CUL4‐DDB1‐based E3 ligase complex in tomato, New Phytologist, 209, 3, (1028-1039), (2015).
- L. Boureau, A. How-Kit, E. Teyssier, S. Drevensek, M. Rainieri, J. Joubès, L. Stammitti, A. Pribat, C. Bowler, Y. Hong and P. Gallusci, A CURLY LEAF homologue controls both vegetative and reproductive development of tomato plants, Plant Molecular Biology, 90, 4-5, (485), (2016).
- Lihong Liu, Zhiyong Shao, Min Zhang and Qiaomei Wang, Regulation of Carotenoid Metabolism in Tomato, Molecular Plant, 10.1016/j.molp.2014.11.006, 8, 1, (28-39), (2015).
- Emeline Teyssier, Lisa Boureauv, Weiwei Chen, Ruie Lui, Charlotte Degraeve-Guibault, Linda Stammitti, Yiguo Hong and Philippe Gallusci, Epigenetic regulation during fleshy fruit development and ripening, Applied Plant Genomics and Biotechnology, 10.1016/B978-0-08-100068-7.00008-2, (133-151), (2015).
- Nisha Gupta, V Babu Prasad and Sudip Chattopadhyay, LeMYC2 acts as a negative regulator of blue light mediated photomorphogenic growth, and promotes the growth of adult tomato plants, BMC Plant Biology, 14, 1, (38), (2014).
- Junli Huang, Feng Qin, Guangchao Zang, Zhenhui Kang, Hanyan Zou, Feng Hu, Caili Yue, Xianyong Li and Guixue Wang, Mutation of OsDET1 increases chlorophyll content in rice, Plant Science, 210, (241), (2013).
- Peter M. Bramley, Carotenoid Biosynthesis and Chlorophyll Degradation, The Molecular Biology and Biochemistry of Fruit Ripening, (75-116), (2013).
- Xiaofeng Tang, Zizhi Tang, Shengxiong Huang, Jikai Liu, Jia Liu, Wei Shi, Xuefen Tian, Yuxiang Li, Danfeng Zhang, Jian Yang, Yongfeng Gao, Deer Zeng, Pei Hou, Xiangli Niu, Ying Cao, Guangwei Li, Xiao Li, Fangming Xiao and Yongsheng Liu, Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development, Planta, 238, 5, (923), (2013).
- Maria Florencia Cocaliadis, Rafael Fernández-Muñoz, Clara Pons, Diego Orzaez and Antonio Granell, Increasing tomato fruit quality by enhancing fruit chloroplast function. A double-edged sword?, Journal of Experimental Botany, 65, 16, (4589), (2013).
- Matthew O. Jones, Florence Piron-Prunier, Fabien Marcel, Elodie Piednoir-Barbeau, Abdullah A. Alsadon, Mahmoud A. Wahb-Allah, Abdullah A. Al-Doss, Chris Bowler, Peter M. Bramley, Paul D. Fraser and Abdelhafid Bendahmane, Characterisation of alleles of tomato light signalling genes generated by TILLING, Phytochemistry, 79, (78), (2012).
- Mohammad Alimohammadi, Kanishka de Silva, Clarisse Ballu, Nawab Ali and Mariya V. Khodakovskaya, Reduction of inositol (1,4,5)–trisphosphate affects the overall phosphoinositol pathway and leads to modifications in light signalling and secondary metabolism in tomato plants, Journal of Experimental Botany, 63, 2, (825), (2012).
- Avtar K. Handa, Martín-Ernesto Tiznado-Hernández and Autar K. Mattoo, Fruit development and ripening, Plant Biotechnology and Agriculture, 10.1016/B978-0-12-381466-1.00026-2, (405-424), (2012).
- Fei Guo, Wenjing Zhou, Jiancheng Zhang, Qiang Xu, Xiuxin Deng and Randall P. Niedz, Effect of the Citrus Lycopene β-Cyclase Transgene on Carotenoid Metabolism in Transgenic Tomato Fruits, PLoS ONE, 7, 2, (e32221), (2012).
- Mireia González, Meihong Xu, Cristina Esteras, Cristina Roig, Antonio J Monforte, Christelle Troadec, Marta Pujol, Fernando Nuez, Abdelhafid Bendahmane, Jordi Garcia-Mas and Belén Picó, Towards a TILLING platform for functional genomics in Piel de Sapo melons, BMC Research Notes, 4, 1, (289), (2011).
- E. B. Rukavtsova, V. V. Alekseeva and Ya. I. Buryanov, The use of RNA interference for the metabolic engineering of plants (Review), Russian Journal of Bioorganic Chemistry, 36, 2, (146), (2010).
- Raviv Azari, Yaakov Tadmor, Ayala Meir, Moshe Reuveni, Dalia Evenor, Sahadia Nahon, Haviva Shlomo, Lea Chen and Ilan Levin, Light signaling genes and their manipulation towards modulation of phytonutrient content in tomato fruits, Biotechnology Advances, 28, 1, (108), (2010).
- Gemma Farré, Georgina Sanahuja, Shaista Naqvi, Chao Bai, Teresa Capell, Changfu Zhu and Paul Christou, Travel advice on the road to carotenoids in plants, Plant Science, 179, 1-2, (28), (2010).
- R. Azari, M. Reuveni, D. Evenor, S. Nahon, H. Shlomo, L. Chen and I. Levin, Overexpression of UV-DAMAGED DNA BINDING PROTEIN 1 links plant development and phytonutrient accumulation in high pigment-1 tomato, Journal of Experimental Botany, 61, 13, (3627), (2010).
- Leandro Hueso Estornell, Diego Orzáez, Lucas López‐Peña, Benito Pineda, María Teresa Antón, Vicente Moreno and Antonio Granell, A multisite gateway‐based toolkit for targeted gene expression and hairpin RNA silencing in tomato fruits, Plant Biotechnology Journal, 7, 3, (298-309), (2009).
- Vikrant Gupta, Saloni Mathur, Amolkumar U. Solanke, Manoj K. Sharma, Rahul Kumar, Shailendra Vyas, Paramjit Khurana, Jitendra P. Khurana, Akhilesh K. Tyagi and Arun K. Sharma, Genome analysis and genetic enhancement of tomato, Critical Reviews in Biotechnology, 29, 2, (152), (2009).
- Songhu Wang, Jikai Liu, Yuanyuan Feng, Xiangli Niu, Jim Giovannoni and Yongsheng Liu, Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1‐interacting protein CUL4, The Plant Journal, 55, 1, (89-103), (2008).
- Giovanni Giuliano, Raffaela Tavazza, Gianfranco Diretto, Peter Beyer and Mark A. Taylor, Metabolic engineering of carotenoid biosynthesis in plants, Trends in Biotechnology, 26, 3, (139), (2008).
- Guiliang Tang, Gad Galili and Xun Zhuang, RNAi and microRNA: breakthrough technologies for the improvement of plant nutritional value and metabolic engineering, Metabolomics, 3, 3, (357), (2007).
- George G. Harrigan, Susan Martino-Catt and Kevin C. Glenn, Metabolomics, metabolic diversity and genetic variation in crops, Metabolomics, 10.1007/s11306-007-0076-0, 3, 3, (259-272), (2007).
- Alon Samach and Hamutal Lotan, The transition to flowering in tomato, Plant Biotechnology, 24, 1, (71), (2007).
- Katsuyoshi Shimamura, Shin-ichiro Oka, Yumi Shimotori, Takashi Ohmori and Hiroaki Kodama, Generation of secondary small interfering RNA in cell-autonomous and non-cell autonomous RNA silencing in tobacco, Plant Molecular Biology, 63, 6, (803), (2007).
- Filippos Ververidis, Emmanouil Trantas, Carl Douglas, Guenter Vollmer, Georg Kretzschmar and Nickolas Panopoulos, Biotechnology of flavonoids and other phenylpropanoid‐derived natural products. Part II: Reconstruction of multienzyme pathways in plants and microbes, Biotechnology Journal, 2, 10, (1235-1249), (2007).
- Patricia Botella‐Pavía and Manuel Rodríguez‐Concepción, Carotenoid biotechnology in plants for nutritionally improved foods, Physiologia Plantarum, 126, 3, (369-381), (2006).
- Keiko Yonekura- Sakakibara and Kazuki Saito, Review: genetically modified plants for the promotion of human health, Biotechnology Letters, 28, 24, (1983), (2006).
- Nicolas Schauer, Yaniv Semel, Ute Roessner, Amit Gur, Ilse Balbo, Fernando Carrari, Tzili Pleban, Alicia Perez-Melis, Claudia Bruedigam, Joachim Kopka, Lothar Willmitzer, Dani Zamir and Alisdair R Fernie, Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement, Nature Biotechnology, 24, 4, (447), (2006).
- Richard A Dixon, A two-for-one in tomato nutritional enhancement, Nature Biotechnology, 23, 7, (825), (2005).
- Florence Bouvier, Alain Rahier and Bilal Camara, Biogenesis, molecular regulation and function of plant isoprenoids, Progress in Lipid Research, 10.1016/j.plipres.2005.09.003, 44, 6, (357-429), (2005).
- Ganga Rao Davuluri, Ageeth van Tuinen, Paul D Fraser, Alessandro Manfredonia, Robert Newman, Diane Burgess, David A Brummell, Stephen R King, Joe Palys, John Uhlig, Peter M Bramley, Henk M J Pennings and Chris Bowler, Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes, Nature Biotechnology, 23, 7, (890), (2005).
