Molecular Insights into MpAGO1 and Its Regulatory miRNA, miR11707, in the High-Temperature Acclimation of Marchantia polymorpha
Journal
Plant And Cell Physiology
Journal Volume
65
Journal Issue
9
Start Page
1414-1433
ISSN
0032-0781
1471-9053
Date Issued
2024-07-11
Author(s)
Syuan-Fei Hong
Wei-Lun Wei
Zhao-Jun Pan
Jia-Zhen Yu
Shiuan Cheng
Yu-Ling Hung
Veny Tjita
Hao-Ching Wang
Aino Komatsu
Ryuichi Nishihama
Takayuki Kohchi
Ho-Ming Chen
Wan-Chieh Chen
Jing-Chi Lo
Yen-Hsin Chiu
Ho-Chun Yang
Mei-Yeh Lu
Abstract
As a model plant for bryophytes, Marchantia polymorpha offers insights into the role of RNA silencing in aiding early land plants navigate the challenges posed by high-temperature environments. Genomic analysis revealed unique ARGONAUTE1 ortholog gene (MpAGO1) in M. polymorpha, which is regulated by two species-specific microRNAs (miRNAs), miR11707.1 and miR11707.2. Comparative studies of small RNA profiles from M. polymorpha cellular and MpAGO1 immunoprecipitation (MpAGO1-IP) profiles at various temperatures, along with analyses of Arabidopsis AGO1 (AtAGO1), revealed that MpAGO1 has a low selectivity for a diverse range of small RNA species than AtAGO1. Protein structural comparisons revealed no discernible differences in the guide strand small RNA recognition middle domain, MID domain, of MpAGO1 and AtAGO1, suggesting the complexity of miRNA species specificity and necessitating further exploration. Small RNA profiling and size exclusion chromatography have pinpointed a subset of M. polymorpha miRNAs, notably miR11707, that remain in free form within the cell at 22°C but are loaded into MpAGO1 at 28°C to engage in RNA silencing. Investigations into the mir11707 gene editing (mir11707ge) mutants provided evidence of the regulation of miR11707 in MpAGO1. Notably, while MpAGO1 mRNA expression decreases at 28°C, the stability of the MpAGO1 protein and its associated miRNAs is essential for enhancing the RNA-inducing silencing complex (RISC) activity, revealing the importance of RNA silencing in enabling M. polymorpha to survive thermal stress. This study advances our understanding of RNA silencing in bryophytes and provides groundbreaking insights into the evolutionary resilience of land plants to climatic adversities.
Publisher
Oxford University Press (OUP)
Type
journal article