Arabinogalactan protein–rare earth element complexes activate plant endocytosis

Abstract

Endocytosis is essential to all eukaryotes, but how cargoes are selected for internalization remains poorly characterized. Extracellular cargoes are thought to be selected by transmembrane receptors that bind intracellular adaptors proteins to initiate endocytosis. Here, we report a mechanism for clathrin-mediated endocytosis (CME) of extracellular lanthanum [La(III)] cargoes, which requires extracellular arabinogalactan proteins (AGPs) that are anchored on the outer face of the plasma membrane. AGPs were colocalized with La(III) on the cell surface and in La(III)-induced endocytic vesicles inArabidopsisleaf cells. Superresolution imaging showed that La(III) triggered AGP movement across the plasma membrane. AGPs were then colocalized and physically associated with the μ subunit of the intracellular adaptor protein 2 (AP2) complexes. The AGP-AP2 interaction was independent of CME, whereas AGP’s internalization required CME and AP2. Moreover, we show that AGP-dependent endocytosis in the presence of La(III) also occurred in human cells. These findings indicate that extracellular AGPs act as conserved CME cargo receptors, thus challenging the current paradigm about endocytosis of extracellular cargoes.

Rare earth elements induce cytoskeleton-dependent and PI4P-associated rearrangement of SYT1/SYT5 endoplasmic reticulum–plasma membrane contact site complexes in Arabidopsis

“…The dynamics of SYT1–GFP and SYT5–GFP relocalization are consistent with EPCS remodeling being triggered by the slow internalization of REEs to the cytosol (L. Wang et al, 2014 , 2016 , 2019 ). In this scenario, the addition of EGTA, a polydentate chelator that forms stable complexes with both Ca 2+ and REEs ( Tei et al , 2010 ), should maintain REEs in the extracellular space and prevent the REE-induced SYT1–GFP and SYT5–GFP relocalization.…”

Effects of Ceria Nanoparticles and CeCl3 on Plant Growth, Biological and Physiological Parameters, and Nutritional Value of Soil Grown Common Bean (Phaseolus vulgaris)

“…[ 63 ] Some possible mechanisms include: 1) rare earth ions (RE 3+ ) induced hormesis, [ 64 ] 2) directly or indirectly affect photosynthesis, [ 56 ] 3) RE 3+ interfere with the biological effects of Ca 2+ by inhibiting or replacing Ca 2+ at the cellular level, [ 52 ] 4) activate endocytosis in plant cells. [ 65 ] Increases of the contents of soluble protein, soluble sugar, starch, and vitamin C found in this study can be attributed to the above mentioned stimulant effect of Ce 3+ ions on photosynthesis. However, Ce 3+ ion treatments decreased the contents of reducing sugars and phenolic compounds which have strong antioxidant properties.…”

A putative ER-PM contact site complex relocalizes in response to Rare Earth Elements –induced endocytosis

“…In mammals, E-Syt1 aggregates and concentrates at membrane junctions following a rise in [Ca 2+ ] cyt [28] . However, in Arabidopsis, a similar behavior is observed when PM Ca 2+ channel blockers [39-42] /endocytosis inductors [43, 44] are used. This differential behavior is difficult to reconcile unless endocytosed REEs were able to trigger intracellular Ca 2+ signals, effectively offsetting their effect as PM Ca 2+ channel blockers.…”

“…Previous reports have shown that long-term treatments with REEs induce endocytosis and promote the release of REEs to the cytosol [43, 44] , so we asked whether REE-endocytosis underlies the observed changes in SYT1-GFP and SYT5-GFP localization following such a treatment. Figures 5A-5C show that the REE treatments promote the accumulation and internalization of phosphatidylinositol-4-phosphate (PI4P) containing-vesicles, as indicated by the ratiometric sensor citrine 1xPH FAPP1 [45] .…”