The Novel Nuclear Envelope Protein KAKU4 Modulates Nuclear Morphology in<i>Arabidopsis</i>

Goto, Chiaki; Tamura, Kentaro; Fukao, Yoichiro; Shimada, Tomoo; Hara‐Nishimura, Ikuko

doi:10.1105/tpc.113.122168

Cited by 85 publications

(149 citation statements)

References 58 publications

Supporting

Mentioning

137

Contrasting

Order By: Relevance

“…KAKU4 is a newly identified inner nuclear membrane-associated protein that interacts with CRWN1. 27 KAKU4 mutants have spherical epidermal nuclei. 27 Overexpressing KAKU4 caused nuclear membrane deformation, Figure 2.…”

Section: Model For Nuclear Shape Determinationmentioning

confidence: 99%

Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1

Zhou

Groves

Meier

2015

Nucleus

View full text Add to dashboard Cite

Nuclei undergo dynamic shape changes during plant development, but the mechanism is unclear. In Arabidopsis, Sad1/UNC-84 (SUN) proteins, WPP domain-interacting proteins (WIPs), WPP domain-interacting tail-anchored proteins (WITs), myosin XI-i, and CROWDED NUCLEI 1 (CRWN1) have been shown to be essential for nuclear elongation in various epidermal cell types. It has been proposed that WITs serve as adaptors linking myosin XI-i to the SUN-WIP complex at the nuclear envelope (NE). Recently, an interaction between Arabidopsis SUN1 and SUN2 proteins and CRWN1, a plant analog of lamins, has been reported. Therefore, the CRWN1-SUN-WIP-WIT-myosin XI-i interaction may form a linker of the nucleoskeleton to the cytoskeleton complex. In this study, we investigate this proposed mechanism in detail for nuclei of Arabidopsis root hairs and trichomes. We show that WIT2, but not WIT1, plays an essential role in nuclear shape determination by recruiting myosin XI-i to the SUN-WIP NE bridges. Compared with SUN2, SUN1 plays a predominant role in nuclear shape. The NE localization of SUN1, SUN2, WIP1, and a truncated WIT2 does not depend on CRWN1. While crwn1 mutant nuclei are smooth, the nuclei of sun or wit mutants are invaginated, similar to the reported myosin XI-i mutant phenotype. Together, this indicates that the roles of the respective WIT and SUN paralogs have diverged in trichomes and root hairs, and that the SUN-WIP-WIT2-myosin XI-i complex and CRWN1 independently determine elongated nuclear shape. This supports a model of nuclei being shaped both by cytoplasmic forces transferred to the NE and by nucleoplasmic filaments formed under the NE.

show abstract

Section: Model For Nuclear Shape Determinationmentioning

confidence: 99%

Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1

Zhou

Groves

Meier

2015

Nucleus

View full text Add to dashboard Cite

show abstract

“…Furthermore, possible candidates for lamin-like and lamin-binding proteins have been identified and are known, respectively, as CROWDED NUCLEI (CRWN) (Dittmer et al, 2007;Wang et al, 2013) and KAKU4 (Goto et al, 2014). Strikingly, sun, wip, kaku4 and crwn mutants all display nuclear shape and/or nuclear size modifications suggesting that mechanical constraints such as those applied by the cytoskeleton at the NE may be released in mutant backgrounds (Dittmer et al, 2007;Goto et al, 2014;Oda and Fukuda, 2011;van Zanten et al, 2011;Zhou et al, 2012). Finally, the SUN-WIP-WIT2-myosin-XI-i complex and CRWN1 have been proposed to independently determine elongated nuclear shape, highlighting the function of cytoskeleton and nucleoskeleton in nuclear morphology (Zhou et al, 2015b).…”

Section: Introductionmentioning

confidence: 99%

“…Plants encode a LINC complex consisting of SUN (Sad1 and Unc-84 homology) Graumann et al, 2014) and KASH (Klarsicht, Anc-1 and Syne homology) proteins including WPP domain-interacting proteins (WIPs), SUNinteracting nuclear envelope (SINEs) and TIK (Zhou et al, 2012(Zhou et al, , 2015aGraumann et al, 2014). Furthermore, possible candidates for lamin-like and lamin-binding proteins have been identified and are known, respectively, as CROWDED NUCLEI (CRWN) (Dittmer et al, 2007;Wang et al, 2013) and KAKU4 (Goto et al, 2014). Strikingly, sun, wip, kaku4 and crwn mutants all display nuclear shape and/or nuclear size modifications suggesting that mechanical constraints such as those applied by the cytoskeleton at the NE may be released in mutant backgrounds (Dittmer et al, 2007;Goto et al, 2014;Oda and Fukuda, 2011;van Zanten et al, 2011;Zhou et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…Plants are amenable models to study nuclear organisation as natural variations in nuclear morphology occur in various tissues such as epidermis, trichomes and root hairs (Qian et al, 2009;Traas et al, 1998) or during seed formation and germination (van Zanten et al, 2011), as well as in mutants in which the NE or lamin-like components are altered (Dittmer et al, 2007;Goto et al, 2014;Janski et al, 2012;Tamura and Hara-Nishimura, 2011;Zhou et al, 2012). Plants encode a LINC complex consisting of SUN (Sad1 and Unc-84 homology) Graumann et al, 2014) and KASH (Klarsicht, Anc-1 and Syne homology) proteins including WPP domain-interacting proteins (WIPs), SUNinteracting nuclear envelope (SINEs) and TIK (Zhou et al, 2012(Zhou et al, , 2015aGraumann et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants

Poulet

Duc

Voisin

et al. 2017

Journal of Cell Science

View full text Add to dashboard Cite

The linker of nucleoskeleton and cytoskeleton (LINC) complex is an evolutionarily well-conserved protein bridge connecting the cytoplasmic and nuclear compartments across the nuclear membrane. While recent data support its function in nuclear morphology and meiosis, its involvement in chromatin organisation has not been studied in plants. Here, 3D imaging methods have been used to investigate nuclear morphology and chromatin organisation in interphase nuclei of the model plant Arabidopsis thaliana in which heterochromatin clusters in conspicuous chromatin domains called chromocentres. Chromocentres form a repressive chromatin environment contributing to transcriptional silencing of repeated sequences, a general mechanism needed for genome stability. Quantitative measurements of the 3D position of chromocentres indicate their close proximity to the nuclear periphery but that their position varies with nuclear volume and can be altered in specific mutants affecting the LINC complex. Finally, we propose that the plant LINC complex contributes to proper heterochromatin organisation and positioning at the nuclear periphery, since its alteration is associated with the release of transcriptional silencing as well as decompaction of heterochromatic sequences.

show abstract

“…Nevertheless, over the past few years, a group of plant-specific nuclear matrix constituent proteins (NMCPs), such as CROWDED NUCLEI (CRWN) in Arabidopsis, have emerged as "plant lamina" components (Ciska and Moreno Díaz de la Espina 2014; Zhou et al 2015). It appears that plant lamina components are distinct from those of animals, as another recently identified candidate, KAKU4, is also plant-specific (Goto et al 2014). Moreover, NPC components have been systematically identified and investigated (Tamura et al 2010;Tamura and Hara-Nishimura 2013;Parry 2015).…”

mentioning

confidence: 99%

Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery

Cheng

et al. 2017

Genome Res.

106

View full text Add to dashboard Cite

The nuclear space is not a homogeneous biochemical environment. Many studies have demonstrated that the transcriptional activity of a gene is linked to its positioning within the nuclear space. Following the discovery of lamin-associated domains (LADs), which are transcriptionally repressed chromatin regions, the nonrandom positioning of chromatin at the nuclear periphery and its biological relevance have been studied extensively in animals. However, it remains unknown whether comparable chromatin organizations exist in plants. Here, using a strategy using restriction enzyme-mediated chromatin immunoprecipitation, we present genome-wide identification of nonrandom domain organization of chromatin at the peripheral zone of Arabidopsis thaliana nuclei. We show that in various tissues, 10%-20% of the regions on the chromosome arms are anchored at the nuclear periphery, and these regions largely overlap between different tissues. Unlike LADs in animals, the identified domains in plants are not gene-poor or A/T-rich. These domains are enriched with silenced protein-coding genes, transposable element genes, and heterochromatic marks, which collectively define a repressed environment. In addition, these domains strongly correlate with our genome-wide chromatin interaction data set (Hi-C) by largely explaining the patterns of chromatin compartments, revealed on Hi-C maps. Moreover, our results reveal a spatial compartment of different DNA methylation pathways that regulate silencing of transposable elements, where the CHH methylation of transposable elements located at the nuclear periphery and in the interior are preferentially mediated by CMT2 and DRM methyltransferases, respectively. Taken together, the results demonstrate functional partitioning of the Arabidopsis genome in the nuclear space.

show abstract

The Novel Nuclear Envelope Protein KAKU4 Modulates Nuclear Morphology inArabidopsis

Cited by 85 publications

References 58 publications

Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1

Plant nuclear shape is independently determined by the SUN-WIP-WIT2-myosin XI-i complex and CRWN1

The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants

Nonrandom domain organization of the Arabidopsis genome at the nuclear periphery

Contact Info

Product

Resources

About