The nuclear pore and plant development

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All macromolecules that traffic between the nucleus and the cytoplasm traverse the nuclear pore. While yeast and mammalian nuclear pore structure and function have recently been substantially refined, our understanding of the plant nuclear pore is still far from comprehensive. Nevertheless, a number of nuclear pore and nucleocytoplasmic trafficking components have recently been identified as required for diverse developmental and signaling pathways. In addition, some aspects of the nuclear pore composition itself now appear under developmental control and nuclear pore components have recently surfaced as novel players in plant cytokinesis. Here, we review these new findings in context and attempt to correlate molecular functions with developmental processes.

Introduction

The nuclear pore complex (NPC) connects cytoplasm and nucleoplasm as the sole gateway for macromolecular exchange between the two compartments. It consists of multiple subunits of 30 nucleoporins (Nups), organized in a doughnut-shaped complex of eightfold symmetry (Figure 1; Table 1). Transporters of the karyopherin family bind to signal sequences of cargo proteins, either nuclear localization sequences (NLS) for import or nuclear export sequences (NES) for export (Figure 2). Nups containing hydrophobic phenylalanine–glycine (FG) repeats enable the access of the karyopherin–cargo complexes to the pore, possibly by forming a hydrogel with permeability properties that allow selective access of the transport complexes while rejecting other proteins of comparable size [1].

Recent breakthroughs in nuclear pore studies were driven by proteomics in yeast and mammalian systems, in combination with large-scale structural and functional investigations [2, 3, 4]. By contrast, our knowledge of the plant nuclear pore is still far from comprehensive [5]. Nevertheless, recently several mutant screens have found nucleoporins and nuclear transport components crucial for plant growth, development, and interactions with the environment. While this in itself is not surprising, given that any perturbed housekeeping machinery would be expected to negatively impact a number of pathways, it is the relatively mild impact and the specificity of the defects that are puzzling. Here, we review these latest reports in context and attempt to correlate the affected pathways with specific nuclear pore functions. In addition, we review recent evidence for developmental regulation of nuclear pore composition itself and the role of nuclear pore activities during cytokinesis.

Section snippets

Hormone and stress responses

AXR1 is a subunit of RUB-activating protein, the first enzyme of the pathway of RUB-conjugation of cullin, and is involved in forming a functional SCF complex for the auxin-dependent degradation of the Aux/IAA repressors [6]. Two suppressors of auxin-resistant 1 (axr1), SUPPRESSOR OF AXR1 1 and 3 (SAR1 and SAR 3) are the homologs of Nup160 and Nup96, respectively (Figure 1, Figure 2) [7••]. In sar1 and sar3, the morphological and molecular phenotypes of axr1 are partially restored, but

Plant–microbe interactions

R proteins are intracellular immune sensors, typically of the NB (nucleotide binding)-LRR (leucine-rich repeat) type, that act as regulatory signal transduction switches upon sensing isolate-specific pathogen effectors. A gain-of-function mutation in the Arabidopsis SNC1 R gene leads to constitutive SNC1 activity and constitutive defense response. Suppressors of snc1 (modifiers of snc1, mos) include MOS6 (importin α3) [16], MOS3 (Nup96/SAR3) [17], and MOS7 (Nup88) [18]. Candidates possibly

Flowering control, development, and RNA export at the nuclear pore

A number of the nucleoporin and transport factor mutants discussed above flower early and have similar, diverse developmental defects, including stunted growth, impaired stamen development, and altered juvenile/adult transition and phyllotaxy, including those in SAR1/Nup160, SAR3/MOS3, the nuclear basket protein NUA/AtTPR, the RNA exporters HASTY and PAUSED, the DEAD-box helicase LOS4 and ESD4 (EARLY IN SHORT DAYS), a SUMO protease associated with NUA/AtTPR [7••, 10•, 11, 17, 28, 29•, 30, 31••,

Developmental and cell-cycle regulation of the plant Ran cycle

The compartmentalized Ran GTPase-activating and nucleotide exchange activities create a steep gradient of RanGTP across the nuclear envelope. In yeast, RanGAP localization is restricted to the cytoplasm, while in metazoa and higher plants RanGAP is additionally concentrated around the NE. In metazoa, SUMOylated RanGAP1 is attached to the NPC via RanBP2 (Figure 1) [40]. Plant RanGAPs instead have a plant-specific N-terminal NE-association domain (WPP domain). Two distinct putative plant-specific

Conclusions

Breakthroughs in proteomics and large-scale structural modeling have recently substantially refined our understanding of yeast and mammalian nuclear pore structure and function. At the same time, our picture of the plant nuclear pore is still far from complete. The recent emergence of nuclear pore and nuclear transport components as developmental and signal transduction mutants now provides evidence for the involvement of this structure in a variety of processes in plant cells. While most

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

Funding by the National Science Foundation (MCB-0343167 and MCB-0641271) is greatly acknowledged. We apologize to all colleagues whose work could not be discussed because of space constraints.

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