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Planta

, Volume 248, Issue 4, pp 963–979 | Cite as

Inhibition of α-ketoglutarate dehydrogenase activity affects adventitious root growth in poplar via changes in GABA shunt

  • Jianyun Yue
  • Changjian Du
  • Jing Ji
  • Tiantian Xie
  • Wei Chen
  • Ermei Chang
  • Lanzhen Chen
  • Zeping Jiang
  • Shengqing Shi
Original Article

Abstract

Main conclusion

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.

Keywords

γ-aminobutyric acid Carbon metabolism Hormones α-KGDH Signal transduction 

Abbreviations

AR

Adventitious root

DEG

Differentially expressed genes

GABA

γ-Aminobutyric acid

α-KGDH

α-Ketoglutarate dehydrogenase

SP

Succinyl phosphate

TCA

Tricarboxylic acid cycle

Notes

Acknowledgements

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.

Supplementary material

425_2018_2929_MOESM1_ESM.docx (19 kb)
Method S1 Detailed experimental methods of RNA-seq analysis (DOCX 18 kb)
425_2018_2929_MOESM2_ESM.xlsx (12 kb)
Table S1 Primers for qRT-PCR (XLSX 12 kb)
425_2018_2929_MOESM3_ESM.xlsx (492 kb)
Table S2 DEGs of pair comparison in poplar leaf, stem and root (XLSX 491 kb)
425_2018_2929_MOESM4_ESM.xlsx (390 kb)
Table S3 DEGs for cluster of union data in poplar leaf, stem and root (XLSX 390 kb)
425_2018_2929_MOESM5_ESM.xlsx (45 kb)
Table S4 GO analysis of DEGs in poplar leaf, stem and root (XLSX 45 kb)
425_2018_2929_MOESM6_ESM.xlsx (23 kb)
Table S5 DEGs involved in secondary metabolism and chemical homeostasis (XLSX 23 kb)
425_2018_2929_MOESM7_ESM.xlsx (23 kb)
Table S6 KEGG pathways of DEGs in poplar leaf and root (XLSX 23 kb)
425_2018_2929_MOESM8_ESM.xlsx (423 kb)
Table S7 DEGs involved pathways in carbon and nitrogen metabolism (XLSX 423 kb)
425_2018_2929_MOESM9_ESM.xlsx (17 kb)
Table S8 DEGs involved pathways in hormone signal transduction (XLSX 17 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Tree Genetics and Breeding, Key Laboratory of Tree Breeding and Cultivation of State Forestry Administration, Research Institute of ForestryChinese Academy of ForestryBeijingChina
  2. 2.Institute of Forest Ecology, Environment and ProtectionChinese Academy of ForestryBeijingChina
  3. 3.Institute of Apicultural ResearchChinese Academy of Agricultural SciencesBeijingChina
  4. 4.Risk Assessment Laboratory for Bee ProductsQuality and Safety of Ministry of AgricultureBeijingChina

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