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Arabidopsis Group IIId ERF proteins positively regulate primary cell wall-type CESA genes

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Abstract

The cell wall determines morphology and the environmental responses of plant cells. The primary cell wall (PCW) is produced during cell division and expansion, determining the cell shape and volume. After cell expansion, specific types of plant cells produce a lignified wall, known as a secondary cell wall (SCW). We functionally analyzed Group IIId Arabidopsis AP2/EREBP genes, namely ERF34, ERF35, ERF38, and ERF39, which are homologs of a rice ERF gene previously proposed to be related to SCW biosynthesis. Expression analysis revealed that these four genes are expressed in regions related to cell division and/or cell differentiation in seedlings (i.e., shoot apical meristems, the primordia of leaves and lateral roots, trichomes, and central cylinder of primary roots) and flowers (i.e., vascular tissues of floral organs and replums and/or valve margins of pistils). Overexpression of ERF genes significantly upregulated PCW-type, but not SCW-type, CESA genes encoding cellulose synthase catalytic subunits in Arabidopsis seedlings. Transient co-expression reporter analysis indicated that ERF35, ERF38, and ERF39 possess transcriptional activator activity, and that ERF34, ERF35, ERF38, and ERF39 upregulated the promoter activity of CESA1, a PCW-type CESA gene, through the DRECRTCOREAT elements, the core cis-acting elements known to be recognized by AP2/ERF proteins. Together, our findings show that Group IIId ERF genes are positive transcriptional regulators of PCW-type CESA genes in Arabidopsis and are possibly involved in modulating cellulose biosynthesis in response to developmental requirements and environmental stimuli.

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Abbreviations

CESA:

Cellulose synthase

ERF:

Ethylene response factor

GUS:

β-glucuronidase

LUC:

Luciferase

NST:

NAC SECONDARY WALL THICKENING PROMOTING FACTOR

PCW:

Primary cell wall

SCW:

Secondary cell wall

VND:

VASCULAR-RELATED NAC-DOMAIN

YFP:

Yellow fluorescent protein

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Acknowledgements

We thank Dr. Geoffrey O. Wasteneys and Dr. Miki Fujita (University of British Columbia), Dr. Nobutaka Mitsuda (AIST, Japan), Dr. Arata Yoneda, Dr. Ko Kato, and Dr. Minoru Kubo (Nara Institute of Science and Technology, Japan) for their fruitful discussions, and Ms. Shizuka Nishida and Ms. Eriko Tanaka (Nara Institute of Science and Technology, Japan) for the technical support. This work was supported in part by Japan Society for the Promotion of Science (KAKENHI Grant Number 25291062 to T.D.), the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Grant-in-Aid for Scientific Research on Innovative Areas “The Plant Cell Wall as Information Processing System” Grant numbers 25114520 and 15H01235 to M.O., 24114002 to T.D., “Plant-Structure Optimization Strategy” Grant numbers 18H05484 and 18H05489 to M.O. and T.D., and Grants-in-Aid from the NC-CARP project to T.D.), and the Exploratory Research for Advanced Technology (ERATO) from Japan Science and Technology Agency (JST) (Grant number JPMJER1602 to M.O.) and Japan Advanced Plant Science Network.

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  1. Tian Tian Tan

    Present address: Centre for Research in Biotechnology for Agriculture, University of Malaya, 50603, Kuala Lumpur, Malaysia

  2. Masatoshi Yamaguchi

    Present address: Graduate School of Science and Engineering, Saitama University, Saitama, Saitama, 338-8570, Japan

  3. Laddawan Saelim and Nobuhiro Akiyoshi contributed equally.

Authors and Affiliations

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

    Laddawan Saelim, Nobuhiro Akiyoshi, Tian Tian Tan, Ayumi Ihara, Masatoshi Yamaguchi, Taku Demura & Misato Ohtani

  2. Bioscience and Biotechnology Center, Nagoya University, Nagoya, Aichi, 464-8601, Japan

    Ko Hirano & Makoto Matsuoka

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  1. Laddawan Saelim
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Correspondence to Taku Demura or Misato Ohtani.

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Saelim, L., Akiyoshi, N., Tan, T.T. et al. Arabidopsis Group IIId ERF proteins positively regulate primary cell wall-type CESA genes. J Plant Res 132, 117–129 (2019). https://doi.org/10.1007/s10265-018-1074-1

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