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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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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