Background The nuclear envelope not only serves as a physical barrier separating nuclear content from the cytoplasm but also plays critical roles in modulating the three-dimensional organization of genomic DNA. For both plants and animals, the nuclear periphery is a functional compartment enriched with heterochromatin. To date, how plants manage to selectively tether chromatin at the nuclear periphery is unclear. Results By conducting dual-color fluorescence in situ hybridization experiments on 2C nuclei, we show that in Arabidopsis thaliana , specific chromatin positioning at the nuclear periphery requires plant lamin-like proteins CROWDED NUCLEI 1 (CRWN1), CRWN4, and DNA methylation in CHG and CHH contexts. With chromosome painting and Hi-C analyses, we show global attenuation of spatial chromatin compartmentalization and chromatin positioning patterns at the nuclear periphery in both the crwn1 and crwn4 mutants. Furthermore, ChIP-seq analysis indicates that CRWN1 directly interacts with chromatin domains localized at the nuclear periphery, which mainly contains non-accessible chromatin. Conclusions In summary, we conclude that CRWN1 is a key component of the lamina-chromatin network in plants. It is functionally equivalent to animal lamins, playing critical roles in modulating patterns of chromatin positioning at the nuclear periphery. Electronic supplementary material The online version of this article (10.1186/s13059-019-1694-3) contains supplementary material, which is available to authorized users.

The RNA exosome is a key 3’−5’ exoribonuclease with an evolutionarily conserved structure and function. Its cytosolic functions require the co-factors SKI7 and the Ski complex. Here we demonstrate by co-purification experiments that the ARM-repeat protein RESURRECTION1 (RST1) and RST1 INTERACTING PROTEIN (RIPR) connect the cytosolic Arabidopsis RNA exosome to the Ski complex. rst1 and ripr mutants accumulate RNA quality control siRNAs (rqc-siRNAs) produced by the post-transcriptional gene silencing (PTGS) machinery when mRNA degradation is compromised. The small RNA populations observed in rst1 and ripr mutants are also detected in mutants lacking the RRP45B/CER7 core exosome subunit. Thus, molecular and genetic evidence supports a physical and functional link between RST1, RIPR and the RNA exosome. Our data reveal the existence of additional cytosolic exosome co-factors besides the known Ski subunits. RST1 is not restricted to plants, as homologues with a similar domain architecture but unknown function exist in animals, including humans.

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The nuclear lamina (NL) is a complex network of nuclear lamins and lamina-associated nuclear membrane proteins, which scaffold the nucleus to maintain structural integrity. In animals, type V intermediate filaments are the main constituents of NL. Plant genomes do not encode any homologs of these intermediate filaments, yet plant nuclei contain lamina-like structures that are present in their nuclei. In Arabidopsis thaliana, CROWDED NUCLEI (CRWN), which are required for maintaining structural integrity of the nucleus and specific perinuclear chromatin anchoring, are strong candidates for plant lamin proteins. Recent studies revealed additional roles of Arabidopsis Nuclear Matrix Constituent Proteins (NMCPs) in modulating plants’ response to pathogen and abiotic stresses. However, detailed analyses of Arabidopsis NMCP activities are challenging 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 an MpNMCP loss-of-function mutant, which displayed reduced growth rate and curly thallus lobes. At an organelle level, MpNMCP mutants did not show any alteration in nuclear morphology. Transcriptome analyses indicated that MpNMCP was involved in regulating biotic and abiotic stress responses. Additionally, a highly repetitive genomic region on the male sex chromosome, which was preferentially tethered at the nuclear periphery in wild-type thalli, decondensed in the MpNMCP mutants 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.

21The RNA exosome is a key 3'-5' exoribonuclease with an evolutionarily conserved structure 22The Ski complex consists of the MTR4-related RNA helicase SKI2, the tetratricopeptide 1 repeat protein SKI3 and two copies of the WD40-repeat protein SKI8 [31][32][33] . Association of the 2 Ski complex with the exosome core complex requires an additional protein, SKI7 34 . In yeast, 3 the genes encoding Ski7 and Hbs1, which binds to Dom34 (PELOTA in humans and plants) 4for the release of stalled ribosomes 35 , arose from a whole genome duplication event. In other 5 eukaryotes including mammals and plants, the SKI7 and HBS1 proteins are produced by 6 alternative splicing from a single locus [36][37][38] . 7The Ski complex is conserved in Arabidopsis thaliana 39 , but its physical association with 8 the exosome core has not been investigated yet. An initial experiment to affinity-capture 9 factors associated with the Arabidopsis exosome identified the homologue of DIS3 and two 10 nuclear RNA helicases, AtMTR4 and its closely related homologue HEN2 23 . In addition, 11Arabidopsis Exo9 systematically co-purified with a 1840 amino acid ARM repeat protein of 12 unknown molecular function named RESURRECTION 1 (RST1) 23 . RST1 was originally 13identified in a genetic screen for factors involved in the biosynthesis of epicuticular waxes 40 . 14 Epicuticular waxes are a protective layer of aliphatic very long chain (VLC) hydrocarbons 15 that cover the outer surface of land plants 41,42 . rst1 mutants have less wax on floral stems than 16 wild-type plants, and about 70% of the seeds produced by rst1 mutants are shrunken due to 17 aborted embryogenesis 40 . The molecular function of RST1 remains unknown. Interestingly, 18 one of the two RRP45 exosome core subunits encoded in the Arabidopsis genome, named 19 RRP45B or CER7 (for ECERIFERUM 7) was also identified in a genetic screen aimed at 20 identifying enzymes or regulators of wax biosynthesis 43 . The wax-deficient phenotype of 21 rrp45b/cer7 mutants (cer7 from now on) is suppressed by mutations in genes encoding RNA 22