The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation

Claudia Cosio; Philippe Ranocha; Edith Francoz; Vincent Burlat; Yumei Zheng; Sharyn E. Perry; Juan Jose Ripoll; Martin Yanofsky; Christophe Dunand

doi:10.1111/nph.14127

The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation

Claudia Cosio, Philippe Ranocha, Edith Francoz, Vincent Burlat, Yumei Zheng, Sharyn E. Perry, Juan Jose Ripoll, Martin Yanofsky, Christophe Dunand

Plant and Soil Sciences

Research output: Contribution to journal › Article › peer-review

63 Scopus citations

Abstract

Several physiological functions have been attributed to class III peroxidases (PRXs) in plants, but the in planta role of most members of this family still remains undetermined. Here, we report the first functional characterization of PRX17 (At2g22420), one of the 73 members of this family in Arabidopsis thaliana. Localization of PRX17 was examined by transient expression in Nicotiana benthamiana. Loss- and gain-of-function mutants in A. thaliana were studied. Regulation at the gene and protein levels was analyzed using β-glucuronidase (GUS) activity, quantitative reverse transcriptase (qRT)-PCR, zymography, and chromatin immunoprecipitation. Phenotypes were characterized including lignin and xylan contents. PRX17 was expressed in various tissues, including vascular tissues, and PRX17 was localized to the cell wall. In prx17, the lignin content was reduced in the stem and siliques and bolting was delayed, while the opposite phenotype was observed in 35S:PRX17 plants, together with a significant increase of lignin and xylan immunofluorescence signal. Finally, we demonstrated that the transcription factor AGAMOUS-LIKE15 (AGL15) binds to the PRX17 promoter and regulates PRX17 expression level. This converging set of structural, transcriptomic and physiological data suggests that PRX17, under the control of AGL15, contributes to developmental programs by playing an essential role in regulating age-dependent lignified tissue formation, including changes in cell wall properties.

Original language	English
Pages (from-to)	250-263
Number of pages	14
Journal	New Phytologist
Volume	213
Issue number	1
DOIs	https://doi.org/10.1111/nph.14127
State	Published - Jan 1 2017

Bibliographical note

Funding Information:
C.C. and C.D. were supported by the Swiss National Science Foundation (grant no. 31-068003.02). C.C. was in addition supported by the Schmidheiny Foundation and a grant from the Swiss National Science Foundation during her work at UCSD (grant no. PA00P3-126244). Work in S.E.P.'s lab was supported by the National Science Foundation (grant no. IOS-9984274) and by the University of Kentucky. C.D., P.R., V.B. and E.F. are grateful to the Paul Sabatier Toulouse 3 University and to the Centre National de la Recherche Scientifique (CNRS) for funding their work. The authors are grateful to Donna Fernandez for providing seeds of the AGL15 lines used in this study. The authors would also like to thank Adélaïde Jacq (LRSV CNRS/UPS, Auzeville, France) and Aurélie Le Ru (Toulouse Réseau Imagerie (TRI), FRAIB, Auzeville, France) for their help in performing and imaging the transient expression experiments. Nanozoomer virtual microscopy was performed using the TRI, FRAIB facilities. We are grateful to Professor Claude Penel, now retired, for his financial and scientific support in the early years of this work.

Publisher Copyright:
© 2016 The Authors. New Phytologist © 2016 New Phytologist Trust

Keywords

Arabidopsis thaliana
chromatin immunoprecipitation-with DNA microarray (ChIP-chip)
development
flower
isoelectric focusing (IEF)
peroxidase
silique
stem

ASJC Scopus subject areas

Physiology
Plant Science

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10.1111/nph.14127

Cite this

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title = "The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation",

abstract = "Several physiological functions have been attributed to class III peroxidases (PRXs) in plants, but the in planta role of most members of this family still remains undetermined. Here, we report the first functional characterization of PRX17 (At2g22420), one of the 73 members of this family in Arabidopsis thaliana. Localization of PRX17 was examined by transient expression in Nicotiana benthamiana. Loss- and gain-of-function mutants in A. thaliana were studied. Regulation at the gene and protein levels was analyzed using β-glucuronidase (GUS) activity, quantitative reverse transcriptase (qRT)-PCR, zymography, and chromatin immunoprecipitation. Phenotypes were characterized including lignin and xylan contents. PRX17 was expressed in various tissues, including vascular tissues, and PRX17 was localized to the cell wall. In prx17, the lignin content was reduced in the stem and siliques and bolting was delayed, while the opposite phenotype was observed in 35S:PRX17 plants, together with a significant increase of lignin and xylan immunofluorescence signal. Finally, we demonstrated that the transcription factor AGAMOUS-LIKE15 (AGL15) binds to the PRX17 promoter and regulates PRX17 expression level. This converging set of structural, transcriptomic and physiological data suggests that PRX17, under the control of AGL15, contributes to developmental programs by playing an essential role in regulating age-dependent lignified tissue formation, including changes in cell wall properties.",

keywords = "Arabidopsis thaliana, chromatin immunoprecipitation-with DNA microarray (ChIP-chip), development, flower, isoelectric focusing (IEF), peroxidase, silique, stem",

author = "Claudia Cosio and Philippe Ranocha and Edith Francoz and Vincent Burlat and Yumei Zheng and Perry, {Sharyn E.} and Ripoll, {Juan Jose} and Martin Yanofsky and Christophe Dunand",

note = "Funding Information: C.C. and C.D. were supported by the Swiss National Science Foundation (grant no. 31-068003.02). C.C. was in addition supported by the Schmidheiny Foundation and a grant from the Swiss National Science Foundation during her work at UCSD (grant no. PA00P3-126244). Work in S.E.P.'s lab was supported by the National Science Foundation (grant no. IOS-9984274) and by the University of Kentucky. C.D., P.R., V.B. and E.F. are grateful to the Paul Sabatier Toulouse 3 University and to the Centre National de la Recherche Scientifique (CNRS) for funding their work. The authors are grateful to Donna Fernandez for providing seeds of the AGL15 lines used in this study. The authors would also like to thank Ad{\'e}la{\"i}de Jacq (LRSV CNRS/UPS, Auzeville, France) and Aur{\'e}lie Le Ru (Toulouse R{\'e}seau Imagerie (TRI), FRAIB, Auzeville, France) for their help in performing and imaging the transient expression experiments. Nanozoomer virtual microscopy was performed using the TRI, FRAIB facilities. We are grateful to Professor Claude Penel, now retired, for his financial and scientific support in the early years of this work. Publisher Copyright: {\textcopyright} 2016 The Authors. New Phytologist {\textcopyright} 2016 New Phytologist Trust",

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language = "English",

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T1 - The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation

AU - Cosio, Claudia

AU - Ranocha, Philippe

AU - Francoz, Edith

AU - Burlat, Vincent

AU - Zheng, Yumei

AU - Perry, Sharyn E.

AU - Ripoll, Juan Jose

AU - Yanofsky, Martin

AU - Dunand, Christophe

N1 - Funding Information: C.C. and C.D. were supported by the Swiss National Science Foundation (grant no. 31-068003.02). C.C. was in addition supported by the Schmidheiny Foundation and a grant from the Swiss National Science Foundation during her work at UCSD (grant no. PA00P3-126244). Work in S.E.P.'s lab was supported by the National Science Foundation (grant no. IOS-9984274) and by the University of Kentucky. C.D., P.R., V.B. and E.F. are grateful to the Paul Sabatier Toulouse 3 University and to the Centre National de la Recherche Scientifique (CNRS) for funding their work. The authors are grateful to Donna Fernandez for providing seeds of the AGL15 lines used in this study. The authors would also like to thank Adélaïde Jacq (LRSV CNRS/UPS, Auzeville, France) and Aurélie Le Ru (Toulouse Réseau Imagerie (TRI), FRAIB, Auzeville, France) for their help in performing and imaging the transient expression experiments. Nanozoomer virtual microscopy was performed using the TRI, FRAIB facilities. We are grateful to Professor Claude Penel, now retired, for his financial and scientific support in the early years of this work. Publisher Copyright: © 2016 The Authors. New Phytologist © 2016 New Phytologist Trust

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Several physiological functions have been attributed to class III peroxidases (PRXs) in plants, but the in planta role of most members of this family still remains undetermined. Here, we report the first functional characterization of PRX17 (At2g22420), one of the 73 members of this family in Arabidopsis thaliana. Localization of PRX17 was examined by transient expression in Nicotiana benthamiana. Loss- and gain-of-function mutants in A. thaliana were studied. Regulation at the gene and protein levels was analyzed using β-glucuronidase (GUS) activity, quantitative reverse transcriptase (qRT)-PCR, zymography, and chromatin immunoprecipitation. Phenotypes were characterized including lignin and xylan contents. PRX17 was expressed in various tissues, including vascular tissues, and PRX17 was localized to the cell wall. In prx17, the lignin content was reduced in the stem and siliques and bolting was delayed, while the opposite phenotype was observed in 35S:PRX17 plants, together with a significant increase of lignin and xylan immunofluorescence signal. Finally, we demonstrated that the transcription factor AGAMOUS-LIKE15 (AGL15) binds to the PRX17 promoter and regulates PRX17 expression level. This converging set of structural, transcriptomic and physiological data suggests that PRX17, under the control of AGL15, contributes to developmental programs by playing an essential role in regulating age-dependent lignified tissue formation, including changes in cell wall properties.

AB - Several physiological functions have been attributed to class III peroxidases (PRXs) in plants, but the in planta role of most members of this family still remains undetermined. Here, we report the first functional characterization of PRX17 (At2g22420), one of the 73 members of this family in Arabidopsis thaliana. Localization of PRX17 was examined by transient expression in Nicotiana benthamiana. Loss- and gain-of-function mutants in A. thaliana were studied. Regulation at the gene and protein levels was analyzed using β-glucuronidase (GUS) activity, quantitative reverse transcriptase (qRT)-PCR, zymography, and chromatin immunoprecipitation. Phenotypes were characterized including lignin and xylan contents. PRX17 was expressed in various tissues, including vascular tissues, and PRX17 was localized to the cell wall. In prx17, the lignin content was reduced in the stem and siliques and bolting was delayed, while the opposite phenotype was observed in 35S:PRX17 plants, together with a significant increase of lignin and xylan immunofluorescence signal. Finally, we demonstrated that the transcription factor AGAMOUS-LIKE15 (AGL15) binds to the PRX17 promoter and regulates PRX17 expression level. This converging set of structural, transcriptomic and physiological data suggests that PRX17, under the control of AGL15, contributes to developmental programs by playing an essential role in regulating age-dependent lignified tissue formation, including changes in cell wall properties.

KW - Arabidopsis thaliana

KW - chromatin immunoprecipitation-with DNA microarray (ChIP-chip)

KW - development

KW - flower

KW - isoelectric focusing (IEF)

KW - peroxidase

KW - silique

KW - stem

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U2 - 10.1111/nph.14127

DO - 10.1111/nph.14127

M3 - Article

C2 - 27513887

AN - SCOPUS:84981501509

VL - 213

SP - 250

EP - 263

IS - 1

ER -

The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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