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SUN anchors pollen WIP-WIT complexes at the vegetative nuclear envelope and is necessary for pollen tube targeting and fertility.

ABSTRACT: LINC (linker of nucleoskeleton and cytoskeleton) complexes play an essential role in nuclear migration by connecting the nucleus to the cytoskeleton and/or motor proteins. Plant LINC complexes have recently been identified in Arabidopsis thaliana, with the inner nuclear membrane SUN and outer nuclear membrane WIP proteins comprising the first identified complex. A recent study identified a nuclear movement defect in Arabidopsis pollen vegetative nuclei linked to the outer nuclear envelope WIP and WIT proteins. However, the role that SUN proteins may play in pollen nuclear migration has yet to be addressed. To explore this question, a SUN2 lumenal domain that was targeted to the ER specifically in pollen was over-expressed. It is shown that the ER-targeted SUN2 lumenal domain was able to displace WIP and WIT proteins from the pollen vegetative nuclear envelope. Expression of this dominant-negative transgene led to impaired VN mobility, impaired pollen tube guidance, and defective pollen tube reception. The observed pollen defects are similar to phenotypes observed in a wip1-1 wip2-1 wip3-1 wit1-1 wit2-1 mutant. It is also shown that these defects were dependent on the KASH-binding function of the SUN2 lumenal domain. These data support a model where LINC complexes formed by SUN, WIP, and WIT at the VNE are responsible for VN migration and suggest an important function of SUN, WIP, and WIT in pollen tube guidance and reception.

SUBMITTER: Zhou X

PROVIDER: S-EPMC4765795 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Macroautophagy/autophagy, a major catabolic pathway in eukaryotes, participates in plant sexual reproduction including the processes of male gametogenesis and the self-incompatibility response. Rapid pollen tube growth is another essential reproductive process that is metabolically highly demanding to drive the vigorous cell growth for delivery of male gametes for fertilization in angiosperms. Whether and how autophagy operates to maintain the homeostasis of pollen tubes remains unknown. Here, we provide evidence that autophagy is elevated in growing pollen tubes and critically required during pollen tube growth and male fertility in Arabidopsis. We demonstrate that SH3P2, a critical non-ATG regulator of plant autophagy, colocalizes with representative ATG proteins during autophagosome biogenesis in growing pollen tubes. Downregulation of SH3P2 expression significantly disrupts Arabidopsis pollen germination and pollen tube growth. Further analysis of organelle dynamics reveals crosstalk between autophagosomes and prevacuolar compartments following the inhibition of phosphatidylinositol 3-kinase. In addition, time-lapse imaging and tracking of ATG8e-labeled autophagosomes and depolarized mitochondria demonstrate that they interact specifically via the ATG8-family interacting motif (AIM)-docking site to mediate mitophagy. Ultrastructural identification of mitophagosomes and two additional forms of autophagosomes imply that multiple types of autophagy are likely to function simultaneously within pollen tubes. Altogether, our results suggest that autophagy is functionally crucial for mediating mitochondrial quality control and canonical cytoplasm recycling during pollen tube growth.Abbreviations: AIM: ATG8-family interacting motif; ATG8: autophagy related 8; ATG5: autophagy related 5; ATG7: autophagy related 7; BTH: acibenzolar-S-methyl; DEX: dexamethasone; DNP: 2,4-dinitrophenol; GFP: green fluorescent protein; YFP: yellow fluorescent protein; PtdIns3K: phosphatidylinositol 3-kinase; PtdIns3P: phosphatidylinositol-3-phosphate; PVC: prevacuolar compartment; SH3P2: SH3 domain-containing protein 2.

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SUN anchors pollen WIP-WIT complexes at the vegetative nuclear envelope and is necessary for pollen tube targeting and fertility.

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