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.

The growing pollen tube has become one of the most fascinating model cell systems for investigations into cell polarity and polar cell growth in plants. Rapidly growing pollen tubes achieve tip-focused cell expansion by vigorous anterograde exocytosis, through which various newly synthesized macromolecules are directionally transported and deposited at the cell apex. Meanwhile, active retrograde endocytosis counter balances the exocytosis at the tip which is believed to recycle the excessive exocytic components for multiple rounds of secretion. Therefore, apical exocytosis and endocytosis are the frontline cellular processes which drive the polar growth of pollen tubes, although they represent opposite vesicular trafficking events with distinct underpinning mechanisms. Nevertheless, the molecular basis governing the spatiotemporal crosstalk and counterbalance of exocytosis and endocytosis during pollen tube polarization and growth remains elusive. Here we discuss recent insight into exocytosis and endocytosis in sculpturing high rates of polarized pollen tube growth. In addition, we especially introduce the novel integration of mathematical modeling in uncovering the mysteries of cell polarity and polar cell growth.

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