One Poplar 5-Enolpyruvylshikimate 3-Phosphate (EPSP) Synthase Moonlight as Transcriptional Repressor to Regulate Lignin Biosynthesis

The Science

Understand how lignin biosynthesis is regulated in poplar.

• Used GWAS to define the linkage of PtrEPSP-TF and lignin biosynthesis.
• Validated linkage by assessing PtrEPSP-TF overexpressing poplars for lignin deposition, secondary metabolism, and gene expression levels.
• Investigated underlying molecular mechanism by protoplast-based assays.

The Impact

• EPSP synthase shown to co-function as a transcriptional repressor.
• PtrEPSP-TF overexpressing poplars had increased lignin deposition, accumulation of lignin-related metabolites, and expression of lignin-related genes.
• PtrEPSP-TF directly represses the expression of PtrhAT. PtrhAT then directly represses the expression of PtrMYB021. Consequently, PtrEPSP-TF positively regulates PtrMYB021 expression and lignin biosynthesis in poplar.

Summary

Long-lived perennial plants, with distinctive habits of inter-annual growth, defense, and physiology, are of great economic and ecological importance. However, some biological mechanisms resulting from genome duplication and functional divergence of genes in these systems remain poorly studied. Here, researchers discovered an association between a poplar (Populus trichocarpa) 5-enolpyruvylshikimate 3-phosphate synthase gene (PtrEPSP) and lignin biosynthesis. Functional characterization of PtrEPSP revealed that this isoform possesses a helix-turn-helix motif in the N terminus and can function as a transcriptional repressor that regulates expression of genes in the phenylpropanoid pathway in addition to performing its canonical biosynthesis function in the shikimate pathway. Researchers demonstrated that this isoform can localize in the nucleus and specifically binds to the promoter and represses the expression of a SLEEPER-like transcriptional regulator, which itself specifically binds to the promoter and represses the expression of PtrMYB021 (known as MYB46 in Arabidopsis thaliana), a master regulator of the phenylpropanoid pathway and lignin biosynthesis. These results demonstrate that PtrEPSP in its regulatory form and PtrhAT form a transcriptional hierarchy regulating phenylpropanoid pathway and lignin biosynthesis in Populus.

References

Xie, M., W. Muchero, A. C. Bryan, K. Yee, H.-B. Guo, J. Zhang, T. J. Tschaplinski, V. R. Singan, E. Lindquist, R. S. Payyavula, J. Barros-Rios, R. A. Dixon, N. Engle, R. W. Sykes, M. Davis, S. S. Jawdy, L. E. Gunter, O. Thompson, S. P. DiFazio, L. M. Evans, K. Winkeler, C. Collins, J. Schmutz, H. Guo, U. Kalluri, M. Rodriguez, K. Feng, J.G. Chen, G. A. Tuskan. 2018. “A 5-Enolpyruvylshikimate 3-Phosphate Synthase Functions as a Transcriptional Repressor in Populus,” The Plant Cell 30(7), 1645–1660. DOI:10.1105/tpc.18.00168.