A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus

Priyanka Paul; Sanjay K. Singh; Barunava Patra; Xueyi Sui; Sitakanta Pattanaik; Ling Yuan

doi:10.1111/nph.14252

A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus

Priyanka Paul, Sanjay K. Singh, Barunava Patra, Xueyi Sui, Sitakanta Pattanaik, Ling Yuan

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

143 Scopus citations

Abstract

Catharanthus roseus produces bioactive terpenoid indole alkaloids (TIAs), including the chemotherapeutics, vincristine and vinblastine. Transcriptional regulation of TIA biosynthesis is not fully understood. The jasmonic acid (JA)-responsive AP2/ERF transcription factor (TF), ORCA3, and its regulator, CrMYC2, play key roles in TIA biosynthesis. ORCA3 forms a physical cluster with two uncharacterized AP2/ERFs, ORCA4 and 5. Here, we report that (1) the ORCA gene cluster is differentially regulated; (2) ORCA4, while overlapping functionally with ORCA3, modulates an additional set of TIA genes. Unlike ORCA3, ORCA4 overexpression resulted in dramatic increase of TIA accumulation in C. roseus hairy roots. In addition, CrMYC2 is capable of activating ORCA3 and co-regulating TIA pathway genes concomitantly with ORCA3. The ORCA gene cluster and CrMYC2 act downstream of a MAP kinase cascade that includes a previously uncharacterized MAP kinase kinase, CrMAPKK1. Overexpression of CrMAPKK1 in C. roseus hairy roots upregulated TIA pathways genes and increased TIA accumulation. This work provides detailed characterization of a TF gene cluster and advances our understanding of the transcriptional and post-translational regulatory mechanisms that govern TIA biosynthesis in C. roseus.

Original language	English
Pages (from-to)	1107-1123
Number of pages	17
Journal	New Phytologist
Volume	213
Issue number	3
DOIs	https://doi.org/10.1111/nph.14252
State	Published - Feb 1 2017

Bibliographical note

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

Funding

We thank John May (Department of Civil Engineering and Environmental Research Training Laboratories, University of Kentucky, USA) for assistance in LC-MS/MS analysis and Kathy Shen for critical reading of the manuscript. This work is supported partially by the Harold R. Burton Endowed Professorship to L.Y. and by the National Science Foundation under Cooperative Agreement no. 1355438, to L.Y.

Funders	Funder number
Department of Civil Engineering and Environmental Research Training Laboratories
National Science Foundation (NSF)
Office of the Director	1355438
University of Kentucky

Keywords

AP2/ERF gene cluster
Catharanthus roseus (Madagascar periwinkle)
MAP kinase
phosphorylation
terpenoid indole alkaloids (TIAs)
transcriptional regulation

ASJC Scopus subject areas

Physiology
Plant Science

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10.1111/nph.14252

Cite this

@article{6e17b8c9a6ff4814bc2ecc68135f4aeb,

title = "A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus",

abstract = "Catharanthus roseus produces bioactive terpenoid indole alkaloids (TIAs), including the chemotherapeutics, vincristine and vinblastine. Transcriptional regulation of TIA biosynthesis is not fully understood. The jasmonic acid (JA)-responsive AP2/ERF transcription factor (TF), ORCA3, and its regulator, CrMYC2, play key roles in TIA biosynthesis. ORCA3 forms a physical cluster with two uncharacterized AP2/ERFs, ORCA4 and 5. Here, we report that (1) the ORCA gene cluster is differentially regulated; (2) ORCA4, while overlapping functionally with ORCA3, modulates an additional set of TIA genes. Unlike ORCA3, ORCA4 overexpression resulted in dramatic increase of TIA accumulation in C. roseus hairy roots. In addition, CrMYC2 is capable of activating ORCA3 and co-regulating TIA pathway genes concomitantly with ORCA3. The ORCA gene cluster and CrMYC2 act downstream of a MAP kinase cascade that includes a previously uncharacterized MAP kinase kinase, CrMAPKK1. Overexpression of CrMAPKK1 in C. roseus hairy roots upregulated TIA pathways genes and increased TIA accumulation. This work provides detailed characterization of a TF gene cluster and advances our understanding of the transcriptional and post-translational regulatory mechanisms that govern TIA biosynthesis in C. roseus.",

keywords = "AP2/ERF gene cluster, Catharanthus roseus (Madagascar periwinkle), MAP kinase, phosphorylation, terpenoid indole alkaloids (TIAs), transcriptional regulation",

author = "Priyanka Paul and Singh, {Sanjay K.} and Barunava Patra and Xueyi Sui and Sitakanta Pattanaik and Ling Yuan",

note = "Publisher Copyright: {\textcopyright} 2016 The Authors. New Phytologist {\textcopyright} 2016 New Phytologist Trust",

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A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus. / Paul, Priyanka; Singh, Sanjay K.; Patra, Barunava et al.
In: New Phytologist, Vol. 213, No. 3, 01.02.2017, p. 1107-1123.

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

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T1 - A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus

AU - Paul, Priyanka

AU - Singh, Sanjay K.

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AU - Sui, Xueyi

AU - Pattanaik, Sitakanta

AU - Yuan, Ling

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N2 - Catharanthus roseus produces bioactive terpenoid indole alkaloids (TIAs), including the chemotherapeutics, vincristine and vinblastine. Transcriptional regulation of TIA biosynthesis is not fully understood. The jasmonic acid (JA)-responsive AP2/ERF transcription factor (TF), ORCA3, and its regulator, CrMYC2, play key roles in TIA biosynthesis. ORCA3 forms a physical cluster with two uncharacterized AP2/ERFs, ORCA4 and 5. Here, we report that (1) the ORCA gene cluster is differentially regulated; (2) ORCA4, while overlapping functionally with ORCA3, modulates an additional set of TIA genes. Unlike ORCA3, ORCA4 overexpression resulted in dramatic increase of TIA accumulation in C. roseus hairy roots. In addition, CrMYC2 is capable of activating ORCA3 and co-regulating TIA pathway genes concomitantly with ORCA3. The ORCA gene cluster and CrMYC2 act downstream of a MAP kinase cascade that includes a previously uncharacterized MAP kinase kinase, CrMAPKK1. Overexpression of CrMAPKK1 in C. roseus hairy roots upregulated TIA pathways genes and increased TIA accumulation. This work provides detailed characterization of a TF gene cluster and advances our understanding of the transcriptional and post-translational regulatory mechanisms that govern TIA biosynthesis in C. roseus.

AB - Catharanthus roseus produces bioactive terpenoid indole alkaloids (TIAs), including the chemotherapeutics, vincristine and vinblastine. Transcriptional regulation of TIA biosynthesis is not fully understood. The jasmonic acid (JA)-responsive AP2/ERF transcription factor (TF), ORCA3, and its regulator, CrMYC2, play key roles in TIA biosynthesis. ORCA3 forms a physical cluster with two uncharacterized AP2/ERFs, ORCA4 and 5. Here, we report that (1) the ORCA gene cluster is differentially regulated; (2) ORCA4, while overlapping functionally with ORCA3, modulates an additional set of TIA genes. Unlike ORCA3, ORCA4 overexpression resulted in dramatic increase of TIA accumulation in C. roseus hairy roots. In addition, CrMYC2 is capable of activating ORCA3 and co-regulating TIA pathway genes concomitantly with ORCA3. The ORCA gene cluster and CrMYC2 act downstream of a MAP kinase cascade that includes a previously uncharacterized MAP kinase kinase, CrMAPKK1. Overexpression of CrMAPKK1 in C. roseus hairy roots upregulated TIA pathways genes and increased TIA accumulation. This work provides detailed characterization of a TF gene cluster and advances our understanding of the transcriptional and post-translational regulatory mechanisms that govern TIA biosynthesis in C. roseus.

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A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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