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Plant-specific Dof transcription factors VASCULAR-RELATED DOF1 and VASCULAR-RELATED DOF2 regulate vascular cell differentiation and lignin biosynthesis in Arabidopsis

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Plant-specific Dof transcription factors VDOF1 and VDOF2 are novel regulators of vascular cell differentiation through the course of a lifetime in Arabidopsis, with shifting their transcriptional target genes.

Abstract

Vascular system is one of critical tissues for vascular plants to transport low-molecular compounds, such as water, minerals, and the photosynthetic product, sucrose. Here, we report the involvement of two Dof transcription factors, named VASCULAR-RELATED DOF1 (VDOF1)/VDOF4.6 and VDOF2/VDOF1.8, in vascular cell differentiation and lignin biosynthesis in Arabidopsis. VDOF genes were expressed in vascular tissues, but the detailed expression sites were partly different between VDOF1 and VDOF2. Vein patterning and lignin analysis of VDOF overexpressors and double mutant vdof1 vdof2 suggested that VDOF1 and VDOF2 would function as negative regulators of vein formation in seedlings, and lignin deposition in inflorescence stems. Interestingly, effects of VDOF overexpression in lignin deposition were different by developmental stages of inflorescence stems, and total lignin contents were increased and decreased in VDOF1 and VDOF2 overexpressors, respectively. RNA-seq analysis of inducible VDOF overexpressors demonstrated that the genes for cell wall biosynthesis, including lignin biosynthetic genes, and the transcription factor genes related to stress response and brassinosteroid signaling were commonly affected by VDOF1 and VDOF2 overexpression. Taken together, we concluded that VDOF1 and VDOF2 are novel regulators of vascular cell differentiation through the course of a lifetime, with shifting their transcriptional target genes: in seedlings, the VDOF genes negatively regulate vein formation, while at reproductive stages, the VDOF proteins target lignin biosynthesis.

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Abbreviations

2D NMR :

Two-dimensional nuclear magnetic resonance

BR :

Brassinosteroid

GUS :

β-Glucuronidase

NAC :

NAC SECONDARY WALL THICKENING PROMOTING FACTOR

PEAR :

PHLOEM EARLY DOF

VDOF :

VASCULAR-RELATED DOF

VND :

VASCULAR-RELATED NAC-DOMAIN

YFP:

Yellow fluorescent protein

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Acknowledgements

We thank the Arabidopsis Biological Research Center for providing Arabidopsis seeds. We also thank Dr. Shunsuke Miyashima (Nara Institute of Science and Technology, Japan) for technical support in the localization analysis of VDOF-YFP proteins, Dr. Minoru Kubo, Dr. Ko Kato, Dr. Toshiro Ito and Dr. Masaaki Umeda (Nara Institute of Science and Technology, Japan) and Dr. Lacey A. Samuels (University of British Columbia, Canada) for fruitful discussions, Dr. Hironori Kaji and Ms. Ayaka Maeno (Kyoto University) for their support in the NMR experiments, Ms. Megumi Ozaki (Kyoto University) for her technical assistance for lignin determination, and Ms. Shizuka Nishida and Ms. Eriko Tanaka (Nara Institute of Science and Technology, Japan) for their technical supports to grow plants. This work was supported in part by JSPS KAKENHI (grant numbers JP25291062 and JP18H02466 to T.D., JP20H03271 to M.O.), the MEXT KAKENHI (Grant Numbers JP24114002 to T.D., JP25114520, JP15H01235, and JP20H05405 to M.O., JP18H05484 and JP18H05489 to M.O. and T.D.), JST ERATO Grant Number JPMJER1602, the Hamaguchi Foundation for the Advancement of Biochemistry, and the Asahi Glass Foundation to M.O., and Japan Advanced Plant Science Network. A part of this study was conducted using the facilities in the DASH/FBAS at RISH, Kyoto University, and the NMR spectrometer in JURC at ICR, Kyoto University.

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  1. Graduate School of Science and Technology, Nara Institute of Science and Technology, Ikoma, Nara, 630-0192, Japan

    Vasagi Ramachandran, Ryosuke Sano, Taku Demura & Misato Ohtani

  2. Research Institute for Sustainable Humanosphere, Kyoto University, Uji, Kyoto, 611-0011, Japan

    Yuki Tobimatsu, Yamamura Masaomi & Toshiaki Umezawa

  3. Research Unit for Development of Global Sustainability, Kyoto University, Uji, Gokasho, Kyoto, 611-0011, Japan

    Toshiaki Umezawa

  4. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, 277-8562, Japan

    Misato Ohtani

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  1. Vasagi Ramachandran
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  3. Yamamura Masaomi
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  4. Ryosuke Sano
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  5. Toshiaki Umezawa
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Contributions

VR, TD, and MO designed the research; VR performed the experiments; VR, YT, MY, and TU carried out lignin analysis; VR, RS and MO analyzed the RNA-seq data; VR, TD, and MO wrote the manuscript and YT and TU helped the manuscript preparation.

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Correspondence to Taku Demura or Misato Ohtani.

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Ramachandran, V., Tobimatsu, Y., Masaomi, Y. et al. Plant-specific Dof transcription factors VASCULAR-RELATED DOF1 and VASCULAR-RELATED DOF2 regulate vascular cell differentiation and lignin biosynthesis in Arabidopsis. Plant Mol Biol 104, 263–281 (2020). https://doi.org/10.1007/s11103-020-01040-9

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