Complex regulation of prolyl-4-hydroxylases impacts root hair expansion

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 (...

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Autores principales: Velasquez, S.M., Ricardi, M.M., Poulsen, C.P., Oikawa, A., Dilokpimol, A., Halim, A., Mangano, S., Denita Juarez, S.P., Marzol, E., Salgado Salter, J.D., Dorosz, J.G., Borassi, C., Möller, S.R., Buono, R., Ohsawa, Y., Matsuoka, K., Otegui, M.S., Scheller, H.V., Geshi, N., Petersen, B.L., Iusem, N.D., Estevez, J.M.
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_16742052_v8_n5_p734_Velasquez
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spelling todo:paper_16742052_v8_n5_p734_Velasquez2023-10-03T16:29:32Z Complex regulation of prolyl-4-hydroxylases impacts root hair expansion Velasquez, S.M. Ricardi, M.M. Poulsen, C.P. Oikawa, A. Dilokpimol, A. Halim, A. Mangano, S. Denita Juarez, S.P. Marzol, E. Salgado Salter, J.D. Dorosz, J.G. Borassi, C. Möller, S.R. Buono, R. Ohsawa, Y. Matsuoka, K. Otegui, M.S. Scheller, H.V. Geshi, N. Petersen, B.L. Iusem, N.D. Estevez, J.M. cell expansion cell walls enzymology proline hydroxylation protein targeting root hairs Arabidopsis thaliana Arabidopsis protein hydroxyproline procollagen proline 2 oxoglutarate 4 dioxygenase Arabidopsis enzymology gene expression regulation genetics glycosylation growth, development and aging hydroxylation metabolism multigene family plant root Arabidopsis Arabidopsis Proteins Gene Expression Regulation, Enzymologic Gene Expression Regulation, Plant Glycosylation Hydroxylation Hydroxyproline Multigene Family Plant Roots Prolyl Hydroxylases 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. © 2015 The Author. Fil:Velasquez, S.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Ricardi, M.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Salgado Salter, J.D. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Iusem, N.D. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. Fil:Estevez, J.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina. JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_16742052_v8_n5_p734_Velasquez
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
topic cell expansion
cell walls
enzymology
proline hydroxylation
protein targeting
root hairs
Arabidopsis thaliana
Arabidopsis protein
hydroxyproline
procollagen proline 2 oxoglutarate 4 dioxygenase
Arabidopsis
enzymology
gene expression regulation
genetics
glycosylation
growth, development and aging
hydroxylation
metabolism
multigene family
plant root
Arabidopsis
Arabidopsis Proteins
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
Glycosylation
Hydroxylation
Hydroxyproline
Multigene Family
Plant Roots
Prolyl Hydroxylases
spellingShingle cell expansion
cell walls
enzymology
proline hydroxylation
protein targeting
root hairs
Arabidopsis thaliana
Arabidopsis protein
hydroxyproline
procollagen proline 2 oxoglutarate 4 dioxygenase
Arabidopsis
enzymology
gene expression regulation
genetics
glycosylation
growth, development and aging
hydroxylation
metabolism
multigene family
plant root
Arabidopsis
Arabidopsis Proteins
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
Glycosylation
Hydroxylation
Hydroxyproline
Multigene Family
Plant Roots
Prolyl Hydroxylases
Velasquez, S.M.
Ricardi, M.M.
Poulsen, C.P.
Oikawa, A.
Dilokpimol, A.
Halim, A.
Mangano, S.
Denita Juarez, S.P.
Marzol, E.
Salgado Salter, J.D.
Dorosz, J.G.
Borassi, C.
Möller, S.R.
Buono, R.
Ohsawa, Y.
Matsuoka, K.
Otegui, M.S.
Scheller, H.V.
Geshi, N.
Petersen, B.L.
Iusem, N.D.
Estevez, J.M.
Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
topic_facet cell expansion
cell walls
enzymology
proline hydroxylation
protein targeting
root hairs
Arabidopsis thaliana
Arabidopsis protein
hydroxyproline
procollagen proline 2 oxoglutarate 4 dioxygenase
Arabidopsis
enzymology
gene expression regulation
genetics
glycosylation
growth, development and aging
hydroxylation
metabolism
multigene family
plant root
Arabidopsis
Arabidopsis Proteins
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
Glycosylation
Hydroxylation
Hydroxyproline
Multigene Family
Plant Roots
Prolyl Hydroxylases
description 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. © 2015 The Author.
format JOUR
author Velasquez, S.M.
Ricardi, M.M.
Poulsen, C.P.
Oikawa, A.
Dilokpimol, A.
Halim, A.
Mangano, S.
Denita Juarez, S.P.
Marzol, E.
Salgado Salter, J.D.
Dorosz, J.G.
Borassi, C.
Möller, S.R.
Buono, R.
Ohsawa, Y.
Matsuoka, K.
Otegui, M.S.
Scheller, H.V.
Geshi, N.
Petersen, B.L.
Iusem, N.D.
Estevez, J.M.
author_facet Velasquez, S.M.
Ricardi, M.M.
Poulsen, C.P.
Oikawa, A.
Dilokpimol, A.
Halim, A.
Mangano, S.
Denita Juarez, S.P.
Marzol, E.
Salgado Salter, J.D.
Dorosz, J.G.
Borassi, C.
Möller, S.R.
Buono, R.
Ohsawa, Y.
Matsuoka, K.
Otegui, M.S.
Scheller, H.V.
Geshi, N.
Petersen, B.L.
Iusem, N.D.
Estevez, J.M.
author_sort Velasquez, S.M.
title Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
title_short Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
title_full Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
title_fullStr Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
title_full_unstemmed Complex regulation of prolyl-4-hydroxylases impacts root hair expansion
title_sort complex regulation of prolyl-4-hydroxylases impacts root hair expansion
url http://hdl.handle.net/20.500.12110/paper_16742052_v8_n5_p734_Velasquez
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