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

研究成果: ジャーナルへの寄稿記事

21 引用 (Scopus)

抄録

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.

元の言語英語
ページ(範囲)734-746
ページ数13
ジャーナルMolecular Plant
8
発行部数5
DOI
出版物ステータス出版済み - 5 4 2015

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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

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Plant Science

これを引用

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

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.

:: Molecular Plant, 巻 8, 番号 5, 04.05.2015, p. 734-746.

研究成果: ジャーナルへの寄稿記事

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, 巻. 8, 番号 5, pp. 734-746. https://doi.org/10.1016/j.molp.2014.11.017
Velasquez SM, Ricardi MM, Poulsen CP, Oikawa A, Dilokpimol A, Halim A その他. Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. Molecular Plant. 2015 5 4;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. :: Molecular Plant. 2015 ; 巻 8, 番号 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.",
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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

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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.

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