Characterization of a plant lamin-like protein in liverwort

The nuclear lamina (NL) is a complex network of nuclear lamins and lamin-associated nuclear membrane proteins, which scaffold the nucleus to maintain structural integrity. In animals, type V intermediate filaments are the main constituents of nuclear lamina. Plant genomes do not encode any homologs of these intermediate filaments, yet plant nuclei contain lamina-like structures. In Arabidopsis thaliana, Nuclear Matrix Constituent proteins (NMCPs), which are required for maintaining structural integrity of the nucleus and specific perinuclear chromatin anchoring, function as nuclear lamins. Recent studies revealed additional roles of Arabidopsis NMCPs in modulating plant response to pathogen and abiotic stress. However, detailed analyses of Arabidopsis NMCP activities are difficult due to the presence of multiple homologs and their functional redundancy. In this study, we investigated the sole NMCP gene in the liverwort Marchantia polymorpha (MpNMCP). We found that MpNMCP proteins preferentially were localized to the nuclear periphery. Using CRISPR-Cas9 techniques, we generated MpNMCP loss-of-function mutant, which displayed reduced growth rate and curly thallus lobe. Transcriptome analyses indicated that MpNMCP was involved in regulating biotic and abiotic stress responses. Besides, a highly repetitive genomic region on the male sex chromosome, which was preferentially tethered at the nuclear periphery in wild-type thalli, decondensed and located in the nuclear interior. This perinuclear chromatin anchoring, however, was not directly controlled by MpNMCP. Altogether, our results unveiled that NMCP in plants have conserved functions in modulating stress responses.

核纤层（nuclear lamina，NL）是由核纤层蛋白及核纤层结合型核膜蛋白构成的复杂网络，可为细胞核提供结构支撑以维持其结构完整性。在动物体内，V型中间丝是核纤层的主要组成成分。植物基因组并不编码这类中间丝的同源蛋白，但植物细胞核中却存在类似核纤层的结构。在拟南芥（Arabidopsis thaliana）中，核基质组成蛋白（Nuclear Matrix Constituent proteins，NMCPs）可发挥核纤层蛋白的功能，其对于维持细胞核结构完整性以及特定的核周染色质锚定过程不可或缺。近期研究进一步揭示了拟南芥NMCPs在调控植物应对病原菌侵染与非生物胁迫中的额外功能。然而，由于拟南芥存在多个NMCP同源基因且功能冗余，对其活性进行细致分析存在较大难度。本研究针对地钱（Marchantia polymorpha）中唯一的NMCP基因（MpNMCP）展开了探究。研究发现，MpNMCP蛋白优先定位于细胞核周区域。本研究利用CRISPR-Cas9技术构建了MpNMCP功能缺失突变体，该突变体表现出生长速率降低及叶状体裂片卷曲的表型。转录组分析结果显示，MpNMCP参与调控生物与非生物胁迫应答过程。此外，雄性性染色体上的一段高度重复基因组区域，在野生型地钱叶状体中优先锚定在核周区域；而在MpNMCP功能缺失突变体中，该区域发生解凝并移位至细胞核内部。但该核周染色质锚定过程并非由MpNMCP直接调控。综上，本研究结果表明，植物中的NMCP在调控胁迫应答过程中存在保守功能。