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

Silvia M. Velasquez, Martiniano M. Ricardi, Christian Peter Poulsen, Ai Oikawa, Adiphol Dilokpimol, Adnan Halim, Silvina Mangano, Silvina Paola Denita Juarez, Eliana Marzol, Juan D. Salgado Salter, Javier Gloazzo Dorosz, Cecilia Borassi, Svenning Rune Möller, Rafael Buono, Yukiko Ohsawa, Ken Matsuoka, Marisa S. Otegui, Henrik V. Scheller, Naomi Geshi, Bent Larsen PetersenNorberto D. Iusem, José M. Estevez

Resultado de la investigación: Article

20 Citas (Scopus)

Resumen

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.

Idioma originalEnglish
Páginas (desde-hasta)734-746
Número de páginas13
PublicaciónMolecular Plant
Volumen8
N.º5
DOI
EstadoPublished - 4 may 2015

Huella dactilar

procollagen-proline dioxygenase
Prolyl Hydroxylases
root hairs
hydroxyproline
Hydroxyproline
glycoproteins
extensin
Glycoproteins
Cell Wall
hydroxylation
Hydroxylation
Proline
cell walls
proline
Plant Cells
Growth
Pollen Tube
Meristem
Hyphae
Secretory Pathway

ASJC Scopus subject areas

  • Molecular Biology
  • Plant Science

Citar esto

Velasquez, S. M., Ricardi, M. M., Poulsen, C. P., Oikawa, A., Dilokpimol, A., Halim, A., ... Estevez, J. M. (2015). Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. Molecular Plant, 8(5), 734-746. https://doi.org/10.1016/j.molp.2014.11.017
Velasquez, Silvia M. ; Ricardi, Martiniano M. ; Poulsen, Christian Peter ; Oikawa, Ai ; Dilokpimol, Adiphol ; Halim, Adnan ; Mangano, Silvina ; Denita Juarez, Silvina Paola ; Marzol, Eliana ; Salgado Salter, Juan D. ; Dorosz, Javier Gloazzo ; Borassi, Cecilia ; Möller, Svenning Rune ; Buono, Rafael ; Ohsawa, Yukiko ; Matsuoka, Ken ; Otegui, Marisa S. ; Scheller, Henrik V. ; Geshi, Naomi ; Petersen, Bent Larsen ; Iusem, Norberto D. ; Estevez, José M. / Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. En: Molecular Plant. 2015 ; Vol. 8, N.º 5. pp. 734-746.
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abstract = "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.",
keywords = "cell expansion, cell walls, enzymology, proline hydroxylation, protein targeting, root hairs",
author = "Velasquez, {Silvia M.} and Ricardi, {Martiniano M.} and Poulsen, {Christian Peter} and Ai Oikawa and Adiphol Dilokpimol and Adnan Halim and Silvina Mangano and {Denita Juarez}, {Silvina Paola} and Eliana Marzol and {Salgado Salter}, {Juan D.} and Dorosz, {Javier Gloazzo} and Cecilia Borassi and M{\"o}ller, {Svenning Rune} and Rafael Buono and Yukiko Ohsawa and Ken Matsuoka and Otegui, {Marisa S.} and Scheller, {Henrik V.} and Naomi Geshi and Petersen, {Bent Larsen} and Iusem, {Norberto D.} and Estevez, {Jos{\'e} M.}",
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Velasquez, SM, Ricardi, MM, Poulsen, CP, Oikawa, A, Dilokpimol, A, Halim, A, Mangano, S, Denita Juarez, SP, Marzol, E, Salgado Salter, JD, Dorosz, JG, Borassi, C, Möller, SR, Buono, R, Ohsawa, Y, Matsuoka, K, Otegui, MS, Scheller, HV, Geshi, N, Petersen, BL, Iusem, ND & Estevez, JM 2015, 'Complex regulation of prolyl-4-hydroxylases impacts root hair expansion', Molecular Plant, vol. 8, n.º 5, pp. 734-746. https://doi.org/10.1016/j.molp.2014.11.017

Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. / Velasquez, Silvia M.; Ricardi, Martiniano M.; Poulsen, Christian Peter; Oikawa, Ai; Dilokpimol, Adiphol; Halim, Adnan; Mangano, Silvina; Denita Juarez, Silvina Paola; Marzol, Eliana; Salgado Salter, Juan D.; Dorosz, Javier Gloazzo; Borassi, Cecilia; Möller, Svenning Rune; Buono, Rafael; Ohsawa, Yukiko; Matsuoka, Ken; Otegui, Marisa S.; Scheller, Henrik V.; Geshi, Naomi; Petersen, Bent Larsen; Iusem, Norberto D.; Estevez, José M.

En: Molecular Plant, Vol. 8, N.º 5, 04.05.2015, p. 734-746.

Resultado de la investigación: Article

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.

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

VL - 8

SP - 734

EP - 746

JO - Molecular Plant

JF - Molecular Plant

SN - 1674-2052

IS - 5

ER -

Velasquez SM, Ricardi MM, Poulsen CP, Oikawa A, Dilokpimol A, Halim A y otros. Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. Molecular Plant. 2015 may 4;8(5):734-746. https://doi.org/10.1016/j.molp.2014.11.017