Journal
DEVELOPMENT
Volume 137, Issue 19, Pages 3245-3255Publisher
COMPANY OF BIOLOGISTS LTD
DOI: 10.1242/dev.052456
Keywords
Polar auxin transport; PIN efflux carrier; PID; WAG1; WAG2; Basal and apical recycling; Polar trafficking; Transcytosis; Endocytosis-related Rab5 pathway; Arabidopsis
Categories
Funding
- Chinese Science Council
- Research Council for Earth and Life Sciences [NWO-ALW 813.06.004]
- NWO
- Netherlands Organization for Health Research and Development [NWO-ZON 050-71-023]
- Netherlands Organization of Scientific Research (NWO)
- Human Frontier Science Program fellowship
- EMBO
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Polar membrane cargo delivery is crucial for establishing cell polarity and for directional transport processes. In plants, polar trafficking mediates the dynamic asymmetric distribution of PIN FORMED (PIN) carriers, which drive polar cell-to-cell transport of the hormone auxin, thereby generating auxin maxima and minima that control development. The Arabidopsis PINOID (PID) protein kinase instructs apical PIN localization by phosphorylating PINs. Here, we identified the PID homologs WAG1 and WAG2 as new PIN polarity regulators. We show that the AGC3 kinases PID, WAG1 and WAG2, and not other plant AGC kinases, instruct recruitment of PINs into the apical recycling pathway by phosphorylating the middle serine in three conserved TPRXS(N/S) motifs within the PIN central hydrophilic loop. Our results put forward a model by which apolarly localized PID, WAG1 and WAG2 phosphorylate PINs at the plasma membrane after default non-polar PIN secretion, and trigger endocytosis-dependent apical PIN recycling. This phosphorylation-triggered apical PIN recycling competes with ARF-GEF GNOM-dependent basal recycling to promote apical PIN localization. In planta, expression domains of PID, WAG1 and WAG2 correlate with apical localization of PINs in those cell types, indicating the importance of these kinases for apical PIN localization. Our data show that by directing polar PIN localization and PIN-mediated polar auxin transport, the three AGC3 kinases redundantly regulate cotyledon development, root meristem size and gravitropic response, indicating their involvement in both programmed and adaptive plant development.
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