Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development

Arabinogalactan glycoproteins (AGPs) are implicated in virtually all aspects of plant growth and development, yet their precise role remains unknown. Classical AGPs cover the plasma membrane and are highly glycosylated by numerous acidic arabinogalactan polysaccharides O-linked to hydroxyproline. Their heterogeneity and complexity hindered a structural approach until the recent determination of a highly conserved repetitive consensus structure for a 15-sugar residue arabinogalactan subunit with paired glucuronic carboxyls. Based on NMR data and molecular dynamics simulations, we identify these carboxyls as potential intramolecular Ca2+-binding sites. Using rapid ultrafiltration assays and mass spectrometry, we verified that AGPs bind Ca2+ tightly (Kd 6.5 mu M) and stoichiometrically at pH 5. Ca2+ binding is reversible in a pH-dependent manner. As typical AGPs contain c. 30 Ca2+-binding subunits and are bulk components of the periplasm, they represent a Ca2+ capacitor discharged at low pH by stretch-activated plasma membrane H+-ATPases, hence a substantial source of cytosolic Ca2+. We propose that these Ca2+ waves prime the calcium oscillator, a signal generator essential to the global Ca2+ signalling pathway of green plants.