Inhibition of α-ketoglutarate dehydrogenase activity affects adventitious root growth in poplar via changes in GABA shunt
Blocking α-ketoglutarate dehydrogenase results in up-regulation of γ-aminobutyric acid (GABA) shunt activity, and inhibits the growth of poplar adventitious roots (ARs), indicating that AR growth is closely associated with GABA shunt.
γ-Aminobutyric acid (GABA) shunt starts from α-ketoglutarate in the tricarboxylic acid cycle, which is thought to represent the cross road between carbon and nitrogen metabolism. Previous studies (Araújo et al. 2012b, Plant Cell 24: 2328–2351) have shown that blocking α-ketoglutarate dehydrogenase (α-KGDH) affects the GABA shunt activity, and inhibits growth. However, its effects on the growth of adventitious roots (ARs) are unclear. In this study, the growth of ARs in tissue-cultured 84K poplar (Populus alba × Populus glandulosa cv. ‘84K’) was significantly inhibited when succinyl phosphate (SP), a specific inhibitor of α-KGDH, was supplied. The inhibition of ARs was associated with significant changes in the levels of soluble sugars, organic acids, and amino acids, and was coupled with the up-regulation of the GABA shunt activity at the transcriptional and translational levels. Exogenous GABA also inhibited AR growth following the increase of the endogenous GABA level. Transcriptomic analyses further showed that genes related to cell wall carbon metabolism and phytohormone (indoleacetic acid, ABA, and ethylene) signaling were affected by the changes of GABA shunt activity, resulting from the α-KGDH inhibition. Thus, our study indicates that the inhibition of poplar AR growth by blocking α-KGDH is closely associated with GABA shunt, which would benefit a better understanding of GABA’s roles in plant development and stress response.
Keywordsγ-aminobutyric acid Carbon metabolism Hormones α-KGDH Signal transduction
Differentially expressed genes
Tricarboxylic acid cycle
We acknowledge the support from the Fundamental Research Funds for the Central Non-profit Research Institution of CAF (CAFYBB2014ZX001-3), Research Funds of Key Laboratory of Tree Breeding and Cultivation of State Forestry Administration (ZDRIF201707), National Key R&D Program of China (Grant No. 2016YFD0600105), and the National Natural Science Foundation of China (31100490). We also thank Dr. Mengzhu Lu for the suggestion of data analysis about ARs; Dr. Jennifer Smith, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.
- Araújo WL, Tohge T, Osorio S, Lohse M, Balbo I, Krahnert I, Sienkiewicz-Porzucek A, Usadel B, Nunes-Nesi A, Fernie AR (2012b) Antisense inhibition of the 2-oxoglutarate dehydrogenase complex in tomato demonstrates its importance for plant respiration and during leaf senescence and fruit maturation. Plant Cell 24:2328–2351CrossRefGoogle Scholar
- Batushansky A, Kirma M, Grillich N, Toubiana D, Pham PA, Balbo I, Fromm H, Galili G, Fernie AR, Fait A (2014) Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic. Mol Plant 7:1065–1068CrossRefGoogle Scholar
- Bunik VI, Mkrtchyan G, Grabarska A, Oppermann H, Daloso D, Araujo WL, Juszczak M, Rzeski W, Bettendorff L, Fernie AR, Meixensberger J, Stepulak A, Gaunitz F (2016) Inhibition of mitochondrial 2-oxoglutarate dehydrogenase impairs viability of cancer cells in a cell-specific metabolism-dependent manner. Oncotarget 7:26400–26421CrossRefGoogle Scholar
- Ramesh SA, Tyerman SD, Gilliham M, Xu B (2016) γ-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74:1–27Google Scholar
- Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C, Busov VB, Martin F, Kohler A, Bhalerao R, Legué V (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006CrossRefGoogle Scholar
- Scagel CF (2004) Changes in cutting composition during early stages of adventitious rooting of miniature rose altered by inoculation with arbuscular mycorrhizal fungi. J Am Soc Hortic Sci 129:624–634Google Scholar