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 - Funding Information:
This work was supported by grants from ANPCyT ( PICT2011-054 , PICT2013-003 to J.M.E and PICT 2011-967 to N.D.I.), CONICET ( PIP0071 to J.M.E. and PIP0342 to N.D.I.), Mizutani Foundation for Glycoscience (Grant 130004 to J.M.E.), Fulbright-CONICET and Fulbright-Bunge and Born Fellowships (to J.M.E and S.M.V, respectively), EMBO short-term fellowship (to M.M.R.), the Danish Agency for Science and Technology ( 274-09-0082 , 2101-07-0071 ) to N.G., The Danish Council for Independent Research/Natural Sciences ( 12-125709 ) and The Danish Council for Strategic Research ( 12-131859 ) to B.L.P., The Danish National Research Foundation ( DNRF107 ) to A.H., a research grant from METI Japan (to K.M.), NSF 1157824 (to M.S.O.), and the U.S. Department of Energy , Office of Science , Office of Biological and Environmental Research , through contract DE-AC02-05CH11231 between Lawrence Berkeley National Laboratory and the U.S. Department of Energy (to H.V.S. and A.O.).
Publisher Copyright:
© 2015 The Author.
PY - 2015/5/4
Y1 - 2015/5/4
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 - cell expansion
KW - cell walls
KW - enzymology
KW - proline hydroxylation
KW - protein targeting
KW - root hairs
UR - http://www.scopus.com/inward/record.url?scp=84929044963&partnerID=8YFLogxK
U2 - 10.1016/j.molp.2014.11.017
DO - 10.1016/j.molp.2014.11.017
M3 - Article
C2 - 25655826
AN - SCOPUS:84929044963
SN - 1674-2052
VL - 8
SP - 734
EP - 746
JO - Molecular Plant
JF - Molecular Plant
IS - 5
ER -