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 Petersen; Norberto D Iusem; José M Estevez

doi:10.1016/j.molp.2014.11.017

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

37 Citations (Scopus)

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.

Original language	English
Journal	Molecular Plant
Volume	8
Issue number	5
Pages (from-to)	734-46
Number of pages	12
ISSN	1674-2052
DOIs	https://doi.org/10.1016/j.molp.2014.11.017
Publication status	Published - 4 May 2015

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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., ... Estevez, J. M. (2015). Complex Regulation of Prolyl-4-Hydroxylases Impacts Root Hair Expansion. Molecular Plant, 8(5), 734-46. https://doi.org/10.1016/j.molp.2014.11.017

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, no. 5, pp. 734-46. https://doi.org/10.1016/j.molp.2014.11.017

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title = "Complex Regulation of Prolyl-4-Hydroxylases Impacts Root Hair Expansion",

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.",

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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doi = "10.1016/j.molp.2014.11.017",

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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

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.

U2 - 10.1016/j.molp.2014.11.017

DO - 10.1016/j.molp.2014.11.017

M3 - Journal article

C2 - 25655826

SN - 1674-2052

VL - 8

SP - 734

EP - 746

JO - Molecular Plant

JF - Molecular Plant

IS - 5

ER -

Complex Regulation of Prolyl-4-Hydroxylases Impacts Root Hair Expansion

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