A lamin‐like protein OsNMCP1 regulates drought resistance and root growth through chromatin accessibility modulation by interacting with a chromatin remodeller OsSWI3C in rice

Abstract

Summary Lamin proteins in animals are implicated in important nuclear functions, including chromatin organization, signalling transduction, gene regulation and cell differentiation. Nuclear Matrix Constituent Proteins (NMCPs) are lamin analogues in plants, but their regulatory functions remain largely unknown. We report that OsNMCP1 is localized at the nuclear periphery in rice (Oryza sativa) and induced by drought stress. OsNMCP1 overexpression resulted in a deeper and thicker root system, and enhanced drought resistance compared to the wild‐type control. An assay for transposase accessible chromatin with sequencing (ATAC‐seq) analysis revealed that OsNMCP1‐overexpression altered chromatin accessibility in hundreds of genes related to drought resistance and root growth, including OsNAC10, OsERF48, OsSGL, SNAC1 and OsbZIP23. OsNMCP1 can interact with SWITCH/SUCROSE NONFERMENTING (SWI/SNF) chromatin remodelling complex subunit OsSWI3C. The reported drought resistance or root growth‐related genes that were positively regulated by OsNMCP1 were negatively regulated by OsSWI3C under drought stress conditions, and OsSWI3C overexpression led to decreased drought resistance. We propose that the interaction between OsNMCP1 and OsSWI3C under drought stress conditions may lead to the release of OsSWI3C from the SWI/SNF gene silencing complex, thus changing chromatin accessibility in the genes related to root growth and drought resistance.

Characterization of a Plant Nuclear Matrix Constituent Protein in Liverwort

“…We next examined nuclear localization patterns of MpNMCP proteins by immunohistostaining, in which functional MpNMCP:2HA fusion proteins were visualized with fluorophore-conjugated anti-HA antibodies. As shown by representative images in Figure 3A, MpNMCP is preferentially localized at the nuclear periphery in vivo, which is similar to many NMCP proteins from various plants species (Ciska et al, 2013;Sakamoto and Takagi, 2013;Yang et al, 2020;McKenna et al, 2021). Besides, we found that MpNMCP proteins were not evenly distributed at the nuclear periphery but exhibited a punctate-like pattern, which was similar to that from onion (Ciska et al, 2013).…”

“…In total, 571 and 472 genes were annotated as up-and downregulated genes shared between two independent mutant lines, respectively (Supplementary Figure 2 and Supplementary Table 1). As the function of NMCP genes in both Arabidopsis and rice has been linked to stress response (Guo et al, 2017;Choi et al, 2019;Jarad et al, 2019;Yang et al, 2020), we postulated that the Mpnmcp mutant transcriptome would show correlation to those stress conditions. To this end, we compared differentially expressed genes (DEGs) in Mpnmcp mutants and several published stress-related Marchantia transcriptomes.…”

“…With the use of proteomic approaches, CRWN1 has been shown to interact with transcriptional regulators, such as Polycomb Repressive Complex 2-associated factor PWO1 (Mikulski et al, 2019) and NAC transcription factor NTL9 (Guo et al, 2017). A CRWN homolog in rice, OsNMCP1, has been found to interact with a subunit belonging to SWITCH/SUCROSE NON-FERMENTING (SWI/SNF) chromatin remodeling complex to modulate drought stress response (Yang et al, 2020).…”

Advancing knowledge of the plant nuclear periphery and its application for crop science

“…Further analysis of the mutants, in a line in which topoisomerase initiated homologous recombination was disrupted, suggested that OsSUN1 and OsSUN2 are not completely redundant in function as the Ossun1 single mutant had a normal phenotype but meiosis was disrupted in the Ossun2 mutant. Finally, Yang et al [86] have recently described the interaction between OsNMCP1 and Oriza sativa SWITCH/SUCROSE NONFERMENTING (SWI/SNF) silencing complex. This interaction occurs between OsNMCP1 and OsSWI3C under drought stress conditions leads to the release of OsSWI3C from the SWI/SNF gene silencing complex, thus changing chromatin NUCLEUS accessibility in the genes related to root growth and drought resistance.…”

OsLFR is essential for early endosperm and embryo development by interacting with SWI/SNF complex members in Oryza sativa

“…In crops, only rice SNF2 helicase ENDOSPERMLESS 1 (ENL1) has been reported to be involved in syncytial endosperm development, however, as it maintains chromosomal segregation (Hara et al ., 2015). Cereal Snf2 ATPases, such as CHD3/Mi‐2 chromatin‐remodeling factor CHR729/OsCHR4/Rolled Fine Striped (RFS) (Ma et al ., 2015; Cho et al ., 2018), the INO80/SWR ATPase OsINO80 (Li et al ., 2018) and the SMARCAL1 subfamily protein CHR721 (Zhang et al ., 2020) or SWI/SNF accessory component OsSWI3C (Yang et al ., 2020) in rice, as well as ZmCHB101 in maize ( Zea mays ) (Yu et al ., 2016; Yu et al ., 2018; Yu et al ., 2019; Meng et al ., 2020), are involved in vegetative and reproductive development or stress responses. Although the functions of certain chromatin‐remodeling factors have already been identified in rice, little is known about the roles of these and other proteins involved in seed development.…”