Gene network reconstruction identifies the authentic trans‐prenyl diphosphate synthase that makes the solanesyl moiety of ubiquinone‐9 in Arabidopsis
Summary
Ubiquinone (coenzyme Q) is the generic name of a class of lipid‐soluble electron carriers formed of a redox active benzoquinone ring attached to a prenyl side chain. The length of the latter varies among species, and depends upon the product specificity of a trans‐long‐chain prenyl diphosphate synthase that elongates an allylic diphosphate precursor. In Arabidopsis, this enzyme is assumed to correspond to an endoplasmic reticulum‐located solanesyl diphosphate synthase, although direct genetic evidence was lacking. In this study, the reconstruction of the functional network of Arabidopsis genes linked to ubiquinone biosynthesis singled out an unsuspected solanesyl diphosphate synthase candidate – product of gene At2g34630 – that, extraordinarily, had been shown previously to be targeted to plastids and to contribute to the biosynthesis of gibberellins. Green fluorescent protein (GFP) fusion experiments in tobacco and Arabidopsis, and complementation of a yeast coq1 knockout lacking mitochondrial hexaprenyl diphosphate synthase demonstrated that At2g34630 is also targeted to mitochondria. At2g34630 is the main – if not sole – contributor to solanesyl diphosphate synthase activity required for the biosynthesis of ubiquinone, as demonstrated by the dramatic (75–80%) reduction of the ubiquinone pool size in corresponding RNAi lines. Overexpression of At2g34630 gave up to a 40% increase in ubiquinone content compared to wild‐type plants. None of the silenced or overexpressing lines, in contrast, displayed altered levels of plastoquinone. Phylogenetic analyses revealed that At2g34630 is the only Arabidopsis trans‐long‐chain prenyl diphosphate synthase that clusters with the Coq1 orthologs involved in the biosynthesis of ubiquinone in other eukaryotes.
Number of times cited: 17
- Scott Latimer, Yubing Li, Thuong T.H. Nguyen, Eric Soubeyrand, Abdelhak Fatihi, Christian G. Elowsky, Anna Block, Eran Pichersky and Gilles J. Basset, Metabolic reconstructions identify plant 3‐methylglutaconyl‐CoA hydratase that is crucial for branched‐chain amino acid catabolism in mitochondria, The Plant Journal, 95, 2, (358-370), (2018).
- Paola Andrade, Daniel Caudepón, Teresa Altabella, Montserrat Arró, Albert Ferrer and David Manzano, Complex interplays between phytosterols and plastid development, Plant Signaling & Behavior, 12, 11, (e1387708), (2017).
- Man Zhao, Xiangxian Ying, Jie Sun and Zhao Wang, Molecular evolution of Coq1 gene family in eukaryotes, Journal of Systematics and Evolution, 55, 5, (417-425), (2017).
- Eun-Ha Kim, Dae-Woo Lee, Kyeong-Ryeol Lee, Su-Jin Jung, Jong-Seong Jeon and Hyun Uk Kim, Conserved Function of Fibrillin5 in the Plastoquinone-9 Biosynthetic Pathway in Arabidopsis and Rice, Frontiers in Plant Science, 8, (2017).
- Junjie Wang, Yan Zhao, Ian Ray and Mingzhou Song, Transcriptome responses in alfalfa associated with tolerance to intensive animal grazing, Scientific Reports, 6, 1, (2016).
- Brigitte Ksas, Noëlle Becuwe, Anne Chevalier and Michel Havaux, Plant tolerance to excess light energy and photooxidative damage relies on plastoquinone biosynthesis, Scientific Reports, 5, 1, (2015).
- Qingwen Chen, Dongjie Fan and Guodong Wang, Heteromeric Geranyl(geranyl) Diphosphate Synthase Is Involved in Monoterpene Biosynthesis in Arabidopsis Flowers, Molecular Plant, 8, 9, (1434), (2015).
- Sanjay Singh Parmar, Anjali Jaiwal, Om Parkash Dhankher and Pawan K. Jaiwal, Coenzyme Q10 production in plants: current status and future prospects, Critical Reviews in Biotechnology, 35, 2, (152), (2015).
- M. R. Kant, W. Jonckheere, B. Knegt, F. Lemos, J. Liu, B. C. J. Schimmel, C. A. Villarroel, L. M. S. Ataide, W. Dermauw, J. J. Glas, M. Egas, A. Janssen, T. Van Leeuwen, R. C. Schuurink, M. W. Sabelis and J. M. Alba, Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities, Annals of Botany, 115, 7, (1015), (2015).
- Kazuhiro Hayashi, Yuki Ogiyama, Kazumasa Yokomi, Tsuyoshi Nakagawa, Tomohiro Kaino, Makoto Kawamukai and Takashi Toda, Functional Conservation of Coenzyme Q Biosynthetic Genes among Yeasts, Plants, and Humans, PLoS ONE, 9, 6, (e99038), (2014).
- Tariq A. Akhtar, Yuki Matsuba, Ines Schauvinhold, Geng Yu, Hazel A. Lees, Samuel E. Klein and Eran Pichersky, The tomato cis–prenyltransferase gene family, The Plant Journal, 73, 4, (640-652), (2012).
- Michael Gutensohn, Irina Orlova, Thuong T. H. Nguyen, Rachel Davidovich‐Rikanati, Mario G. Ferruzzi, Yaron Sitrit, Efraim Lewinsohn, Eran Pichersky and Natalia Dudareva, Cytosolic monoterpene biosynthesis is supported by plastid‐generated geranyl diphosphate substrate in transgenic tomato fruits, The Plant Journal, 75, 3, (351-363), (2013).
- Matthew O. Jones, Laura Perez-Fons, Francesca P. Robertson, Peter M. Bramley and Paul D. Fraser, Functional characterization of long-chain prenyl diphosphate synthases from tomato, Biochemical Journal, 449, 3, (729), (2013).
- Louis MT Bradbury, Tom D Niehaus and Andrew D Hanson, Comparative genomics approaches to understanding and manipulating plant metabolism, Current Opinion in Biotechnology, 24, 2, (278), (2013).
- Anna Block, Rikard Fristedt, Sara Rogers, Jyothi Kumar, Brian Barnes, Joshua Barnes, Christian G. Elowsky, Yashitola Wamboldt, Sally A. Mackenzie, Kevin Redding, Sabeeha S. Merchant and Gilles J. Basset, Functional Modeling Identifies Paralogous Solanesyl-diphosphate Synthases That Assemble the Side Chain of Plastoquinone-9 in Plastids, Journal of Biological Chemistry, 288, 38, (27594), (2013).
- Gilles Beck, Diana Coman, Edgar Herren, M. Águila Ruiz-Sola, Manuel Rodríguez-Concepción, Wilhelm Gruissem and Eva Vranová, Characterization of the GGPP synthase gene family in Arabidopsis thaliana, Plant Molecular Biology, 82, 4-5, (393), (2013).
- Miaomiao Liu and Shanfa Lu, Plastoquinone and Ubiquinone in Plants: Biosynthesis, Physiological Function and Metabolic Engineering, Frontiers in Plant Science, 10.3389/fpls.2016.01898, 7, (2016).
