How plants LINC the SUN to KASH

Zhou, Xiao; Meier, Iris

doi:10.4161/nucl.24088

Cited by 45 publications

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“…SUN and KASH proteins form the linkers of the nucleoskeleton and the cytoskeleton complexes at the nuclear envelope (NE) and transfer cytoplasmic forces to the nucleus (1)(2)(3). In plants, nuclear migration is associated with a number of developmental events and environmental responses, including fertilization, root and leaf hair formation, and plant-microbe interactions (4,5). So far, little is known about the mechanism of plant nuclear migration.…”

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Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Zhou

Meier

2014

Proc. Natl. Acad. Sci. U.S.A.

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Increasing evidence suggests that nuclear migration is important for eukaryotic development. Although nuclear migration is conserved in plants, its importance for plant development has not yet been established. The most extraordinary plant nuclear migration events involve plant fertilization, which is starkly different from that of animals. Instead of evolving self-propelled sperm cells (SCs), plants use pollen tubes to deliver SCs, in which the pollen vegetative nucleus (VN) and the SCs migrate as a unit toward the ovules, a fundamental but barely understood process. Here, we report that WPP domain-interacting proteins (WIPs) and their binding partners the WPP domain-interacting tail-anchored proteins (WITs) are essential for pollen nuclear migration. Loss-offunction mutations in WIT and/or WIP gene families resulted in impaired VN movement, inefficient SC delivery, and defects in pollen tube reception. WIPs are Klarsicht/ANC-1/Syne-1 Homology (KASH) analogs in plants. KASH proteins are key players in animal nuclear migration. Thus, this study not only reveals an important nuclear migration mechanism in plant fertilization but also, suggests that similar nuclear migration machinery is conserved between plants and animals.nuclear envelope | Arabidopsis | male gametophyte | LINC complex N uclear migration is essential for cell differentiation, polarization, and migration, which influence organism development (1-3). Examples range from Caenorhabditis elegans P-cell development to mammalian neural development (1-3). The key players in opisthokont nuclear migration are the inner nuclear membrane Sad1/UNC-84 (SUN) proteins and outer nuclear membrane Klarsicht/ANC-1/Syne-1 Homology (KASH) proteins. SUN and KASH proteins form the linkers of the nucleoskeleton and the cytoskeleton complexes at the nuclear envelope (NE) and transfer cytoplasmic forces to the nucleus (1-3). In plants, nuclear migration is associated with a number of developmental events and environmental responses, including fertilization, root and leaf hair formation, and plant-microbe interactions (4, 5). So far, little is known about the mechanism of plant nuclear migration. Although SUN proteins are conserved in plants (6, 7), absence of animal KASH homologs in plants suggests that plants may have evolved different molecular solutions to achieve nuclear migration. Recently, WPP domaininteracting proteins (WIPs) were identified as KASH proteins in plants (8), and their outer nuclear membrane binding partners WPP domain-interacting tail anchored proteins (WITs) were shown to interact with myosin XI-I (9). The WIT-myosin XI

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confidence: 99%

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Zhou

Meier

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Nevertheless, the SUN domain of AtSUN1 can be modeled onto the structure of human SUN2. Although there is very little sequence conservation in the region that comprises the 'KASH lid' in human SUN2, the computed KASH-binding surface of AtSUN1 was successfully used for site-directed mutagenesis to produce plant SUN mutants that are disrupted in KASH-domain binding, suggesting that the domain is functionally conserved (Zhou and Meier, 2013;.…”

Section: Plant Sun Proteinsmentioning

confidence: 99%

“…Homologs of AtSUN1 and AtSUN2 were found throughout the land plants, including Lycophytes and moss, indicating that they are broadly conserved and evolutionary old (Zhou and Meier, 2013). Amino acid sequence comparisons of plant homologs of AtSUN1 and AtSUN2 with that of human SUN2 showed that plant SUN proteins have an N-terminally expanded conserved SUN domain, but the function of this extension is not known (Zhou and Meier, 2013). Nevertheless, the SUN domain of AtSUN1 can be modeled onto the structure of human SUN2.…”

Section: Plant Sun Proteinsmentioning

confidence: 99%

“…Because of the overall domain similarity and location, AtWIP1, AtWIP2 and AtWIP3 were tested for SUN binding in a combination of coimmunoprecipitation and yeast-two-hybrid experiments, and found to indeed bind to AtSUN1 and AtSUN2 (Zhou et al, 2012). Here, the 9-amino-acid tail located C-terminal of the transmembrane domain is required both for binding to SUN proteins and nuclear envelope localization, and binding depends on the domain of AtSUN1 and AtSUN2 that is equivalent to the KASH-binding lid in opisthokont SUN proteins (Zhou and Meier, 2013). The Arabidopsis WIP proteins also showed reduced nuclear envelope association in a SUN-mutant background and can therefore be considered plant analogs of KASH proteins, despite the lack of sequence similarity.…”

Section: Plant Kash Proteinsmentioning

confidence: 99%

“…Although the sequences and the KASH-binding properties of opisthokont SUN proteins are conserved in plants, plant genomes do not code for homologs of known opisthokont KASH proteins (Zhou and Meier, 2013). WPP-domain-interacting proteins (WIPs) are a class of outer nuclear-envelope-associated plant-specific proteins that are involved in anchoring plant RanGAP to the nuclear envelope.…”

Section: Plant Kash Proteinsmentioning

confidence: 99%

See 2 more Smart Citations

LINCing the eukaryotic tree of life – towards a broad evolutionary comparison of nucleocytoplasmic bridging complexes

Meier

2016

Journal of Cell Science

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The nuclear envelope is much more than a simple barrier between nucleoplasm and cytoplasm. Nuclear envelope bridging complexes are protein complexes spanning both the inner and outer nuclear envelope membranes, thus directly connecting the cytoplasm with the nucleoplasm. In metazoans, they are involved in connecting the cytoskeleton with the nucleoskeleton, and act as anchoring platforms at the nuclear envelope for the positioning and moving of both nuclei and chromosomes. Recently, nucleocytoplasmic bridging complexes have also been identified in more evolutionarily diverse organisms, including land plants. Here, I discuss similarities and differences among and between eukaryotic supergroups, specifically of the proteins forming the cytoplasmic surface of these complexes. I am proposing a structure and function for a hypothetical ancestral nucleocytoplasmic bridging complex in the last eukaryotic common ancestor, with the goal to stimulate research in more diverse emerging model organisms.

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The Linker of Nucleoskeleton and Cytoskeleton Complex in Higher Plants

Evans

Graumann

2018

Annual Plant Reviews Online

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The linker of nucleoskeleton and cytoskeleton (LINC) complex provides a multi‐functional bridge across the nuclear envelope, connecting nucleoskeleton and cytoskeleton. This article considers the evidence for a LINC complex in higher plants and describes its key components, their functions, and interactions. Evidence is presented that the complex is based on two families of Sad1/UNC84 homology (SUN) domain proteins in the inner nuclear envelope (C‐ter SUNs and mid‐SUNs) and three major groups of Klarsicht/ANC‐1/Syne homology (KASH) domain proteins, WPP‐domain‐interacting proteins (WIPs), SUN‐interacting nuclear envelope proteins (SINEs), and Toll Interleukin Receptor domain KASH protein (TIK). Recent advances in analyzing the function of the complex in establishing nuclear shape and size, nuclear movement, and connecting nucleoskeleton and cytoskeleton are described, together with its role in mitosis and meiosis.

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How plants LINC the SUN to KASH

Cited by 45 publications

References 100 publications

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

Efficient plant male fertility depends on vegetative nuclear movement mediated by two families of plant outer nuclear membrane proteins

LINCing the eukaryotic tree of life – towards a broad evolutionary comparison of nucleocytoplasmic bridging complexes

The Linker of Nucleoskeleton and Cytoskeleton Complex in Higher Plants

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