TY - JOUR
T1 - Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
AU - Velasquez, Silvia M.
AU - Ricardi, Martiniano M
AU - Poulsen, Christian Peter
AU - Oikawa, Ai
AU - Dilokpimol, Adiphol
AU - Halim, Adnan
AU - Mangano, Silvina
AU - Denita Juarez, Silvina Paola
AU - Marzol, Eliana
AU - Salgado Salter, Juan D.
AU - Dorosz, Javier Gloazzo
AU - Borassi, Cecilia
AU - Möller, Svenning Rune
AU - Buono, Rafael
AU - Ohsawa, Yukiko
AU - Matsuoka, Ken
AU - Otegui, Marisa S.
AU - Scheller, Henrik V.
AU - Geshi, Naomi
AU - Petersen, Bent Larsen
AU - Iusem, Norberto D.
AU - Estevez, José M.
N1 - Copyright © 2015 The Author. Published by Elsevier Inc. All rights reserved.
PY - 2015/5
Y1 - 2015/5
N2 - Root hairs are single cells that develop by tip growth, a process shared with pollen tubes, axons, and fungal hyphae. However, structural plant cell walls impose constraints to accomplish tip growth. In addition to polysaccharides, plant cell walls are composed of hydroxyproline-rich glycoproteins (HRGPs), which include several groups of O-glycoproteins, including extensins (EXTs). Proline hydroxylation, an early post-translational modification (PTM) of HRGPs catalyzed by prolyl 4-hydroxylases (P4Hs), defines their subsequent O-glycosylation sites. In this work, our genetic analyses prove that P4H5, and to a lesser extent P4H2 and P4H13, are pivotal for root hair tip growth. Second, we demonstrate that P4H5 has in vitro preferred specificity for EXT substrates rather than for other HRGPs. Third, by P4H promoter and protein swapping approaches, we show that P4H2 and P4H13 have interchangeable functions but cannot replace P4H5. These three P4Hs are shown to be targeted to the secretory pathway, where P4H5 forms dimers with P4H2 and P4H13. Finally, we explore the impact of deficient proline hydroxylation on the cell wall architecture. Taken together, our results support a model in which correct peptidyl-proline hydroxylation on EXTs, and possibly in other HRGPs, is required for proper cell wall self-assembly and hence root hair elongation in Arabidopsis thaliana.
AB - Root hairs are single cells that develop by tip growth, a process shared with pollen tubes, axons, and fungal hyphae. However, structural plant cell walls impose constraints to accomplish tip growth. In addition to polysaccharides, plant cell walls are composed of hydroxyproline-rich glycoproteins (HRGPs), which include several groups of O-glycoproteins, including extensins (EXTs). Proline hydroxylation, an early post-translational modification (PTM) of HRGPs catalyzed by prolyl 4-hydroxylases (P4Hs), defines their subsequent O-glycosylation sites. In this work, our genetic analyses prove that P4H5, and to a lesser extent P4H2 and P4H13, are pivotal for root hair tip growth. Second, we demonstrate that P4H5 has in vitro preferred specificity for EXT substrates rather than for other HRGPs. Third, by P4H promoter and protein swapping approaches, we show that P4H2 and P4H13 have interchangeable functions but cannot replace P4H5. These three P4Hs are shown to be targeted to the secretory pathway, where P4H5 forms dimers with P4H2 and P4H13. Finally, we explore the impact of deficient proline hydroxylation on the cell wall architecture. Taken together, our results support a model in which correct peptidyl-proline hydroxylation on EXTs, and possibly in other HRGPs, is required for proper cell wall self-assembly and hence root hair elongation in Arabidopsis thaliana.
KW - Arabidopsis/enzymology
KW - Arabidopsis Proteins/genetics
KW - Gene Expression Regulation, Enzymologic
KW - Gene Expression Regulation, Plant
KW - Glycosylation
KW - Hydroxylation
KW - Hydroxyproline/metabolism
KW - Multigene Family
KW - Plant Roots/enzymology
KW - Prolyl Hydroxylases/genetics
U2 - 10.1016/j.molp.2014.11.017
DO - 10.1016/j.molp.2014.11.017
M3 - Article
C2 - 25655826
SN - 1674-2052
VL - 8
SP - 734
EP - 746
JO - Molecular Plant
JF - Molecular Plant
IS - 5
ER -