ARGONAUTE1-binding Tudor domain proteins function in small interfering RNA production for RNA-directed DNA methylation

Takahito Takei; Michio Tsukada; Kentaro Tamura; Ikuko Hara-Nishimura; Yoichiro Fukao; Yukio Kurihara; Minami Matsui; Hidetoshi Saze; Masayuki Tsuzuki; Yuichiro Watanabe; Takahiro Hamada

doi:10.1093/plphys/kiae135

ARGONAUTE1-binding Tudor domain proteins function in small interfering RNA production for RNA-directed DNA methylation

Plant Physiol. 2024 Mar 6:kiae135. doi: 10.1093/plphys/kiae135. Online ahead of print.

Authors

Takahito Takei^{1

2}, Michio Tsukada³, Kentaro Tamura⁴, Ikuko Hara-Nishimura⁵, Yoichiro Fukao⁶, Yukio Kurihara^{3

7}, Minami Matsui^{7

8}, Hidetoshi Saze⁹, Masayuki Tsuzuki¹⁰, Yuichiro Watanabe³, Takahiro Hamada²

Affiliations

¹ Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan.
² Department of Bioscience, Faculty of Life Science, Okayama University of Science, Okayama, Japan.
³ Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan.
⁴ Department of Environmental and Life Sciences, School of Food and Nutritional Sciences, University of Shizuoka, Shizuoka, Japan.
⁵ Faculty of Science and Engineering, Konan University, Kobe, Japan.
⁶ Graduate School of Life Science, Ritsumeikan University, Kusatsu, Shiga, Japan.
⁷ Synthetic Genomics Research Group, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan.
⁸ Graduate School of Nanobioscience, Department of Life and Environmental System Science, Yokohama City University, Yokohama, Kanagawa, Japan.
⁹ Plant Epigenetics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan.
¹⁰ Faculty of Agriculture and Marine Science, Kochi University, Kochi, Japan.

PMID: 38446745
DOI: 10.1093/plphys/kiae135

Abstract

Transposable elements (TEs) contribute to plant evolution, development, and adaptation to environmental changes, but the regulatory mechanisms are largely unknown. RNA-directed DNA methylation (RdDM) is one TE regulatory mechanism in plants. Here, we identified that novel ARGONAUTE 1 (AGO1)-binding Tudor domain proteins Precocious dissociation of sisters C/E (PDS5C/E) are involved in 24-nt siRNA production to establish RdDM on TEs in Arabidopsis thaliana PDS5 family proteins are subunits of the eukaryote-conserved cohesin complex. However, the double mutant lacking angiosperm-specific subfamily PDS5C and PDS5E (pds5c/e) exhibited different developmental phenotypes and transcriptome compared with those of the double mutant lacking eukaryote-conserved subfamily PDS5A and PDS5B (pds5a/b), suggesting that the angiosperm-specific PDS5C/E subfamily has a unique function in angiosperm plants. Proteome and imaging analyses revealed that PDS5C/E interact with AGO1. The pds5c/e double mutant had defects in 24-nt siRNA accumulation and CHH DNA methylation on TEs. In addition, some lncRNAs that accumulated in the pds5c/e mutant were targeted by AGO1-loading 21-nt miRNAs and 21-nt siRNAs. These results indicate that PDS5C/E and AGO1 participate in 24-nt siRNA production for RdDM in the cytoplasm. These findings indicate that angiosperm plants evolved a new regulator, the PDS5C/E subfamily, to control the increase in TEs during angiosperm evolution.