GATA and phytochrome interacting factor transcription factors regulate light-induced vindoline biosynthesis in Catharanthus roseus

Yongliang Liu; Barunava Patra; Sitakanta Pattanaik; Ying Wang; Ling Yuan

doi:10.1104/pp.19.00489

GATA and phytochrome interacting factor transcription factors regulate light-induced vindoline biosynthesis in Catharanthus roseus

Yongliang Liu, Barunava Patra, Sitakanta Pattanaik, Ying Wang, Ling Yuan

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

34 Scopus citations

Abstract

Catharanthus roseus is the exclusive source of an array of terpenoid indole alkaloids including the anticancer drugs vincristine and vinblastine, derived from the coupling of catharanthine and vindoline. Leaf-synthesized vindoline is regulated by light. A seven-step enzymatic process is involved in the sequential conversion of tabersonine to vindoline; however, the regulatory mechanism controlling the expression of genes encoding these enzymes has not been elucidated. Here, we identified CrGATA1, an Leu-Leu-Met domain GATA transcription factor that regulates light-induced vindoline biosynthesis in C. roseus seedlings. Expression of CrGATA1 and the vindoline pathway genes T16H2, T3O, T3R, D4H, and DAT was significantly induced by light. In addition, CrGATA1 activated the promoters of five light-responsive vindoline pathway genes in plant cells. Two GATC motifs in the D4H promoter were critical for CrGATA1-mediated transactivation. Transient overexpression of CrGATA1 in C. roseus seedlings resulted in up-regulation of vindoline pathway genes and increased vindoline accumulation. Conversely, virus-induced gene silencing of CrGATA1 in young C. roseus leaves significantly repressed key vindoline pathway genes and reduced vindoline accumulation. Furthermore, we showed that a C. roseus Phytochrome Interacting Factor, CrPIF1, is a repressor of CrGATA1 and vindoline biosynthesis. Transient overexpression or virus-induced gene silencing of CrPIF1 in C. roseus seedlings altered CrGATA1 and vindoline pathway gene expression in the dark. CrPIF1 repressed CrGATA1 and DAT promoter activity by binding to G/E-box/PBE elements. Our findings reveal a regulatory module involving Phytochrome Interacting Factor -GATA that governs light-mediated biosynthesis of specialized metabolites.

Original language	English
Pages (from-to)	1336-1350
Number of pages	15
Journal	Plant Physiology
Volume	180
Issue number	3
DOIs	https://doi.org/10.1104/pp.19.00489
State	Published - Jul 2019

Bibliographical note

Funding Information:
1This work was supported in part by the Harold R. Burton Endowed Professorship to L.Y. and by the National Science Foundation (cooperative agreement no. 1355438 to L.Y.). 2These authors contributed equally to the article. 3Senior authors. 4Author for contact: lyuan3@uky.edu. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Ling Yuan (lyuan3@uky.edu). L.Y., B.P., S.P., and Y.W. designed the research; Y.L., B.P., and S.P. performed experiments; Y.L. and B.P. analyzed data; Y.L., B.P., S.P., Y.W., and L.Y. wrote the article. [OPEN]Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.19.00489

Publisher Copyright:
© 2019 American Society of Plant Biologists.

ASJC Scopus subject areas

Physiology
Genetics
Plant Science

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title = "GATA and phytochrome interacting factor transcription factors regulate light-induced vindoline biosynthesis in Catharanthus roseus",

abstract = "Catharanthus roseus is the exclusive source of an array of terpenoid indole alkaloids including the anticancer drugs vincristine and vinblastine, derived from the coupling of catharanthine and vindoline. Leaf-synthesized vindoline is regulated by light. A seven-step enzymatic process is involved in the sequential conversion of tabersonine to vindoline; however, the regulatory mechanism controlling the expression of genes encoding these enzymes has not been elucidated. Here, we identified CrGATA1, an Leu-Leu-Met domain GATA transcription factor that regulates light-induced vindoline biosynthesis in C. roseus seedlings. Expression of CrGATA1 and the vindoline pathway genes T16H2, T3O, T3R, D4H, and DAT was significantly induced by light. In addition, CrGATA1 activated the promoters of five light-responsive vindoline pathway genes in plant cells. Two GATC motifs in the D4H promoter were critical for CrGATA1-mediated transactivation. Transient overexpression of CrGATA1 in C. roseus seedlings resulted in up-regulation of vindoline pathway genes and increased vindoline accumulation. Conversely, virus-induced gene silencing of CrGATA1 in young C. roseus leaves significantly repressed key vindoline pathway genes and reduced vindoline accumulation. Furthermore, we showed that a C. roseus Phytochrome Interacting Factor, CrPIF1, is a repressor of CrGATA1 and vindoline biosynthesis. Transient overexpression or virus-induced gene silencing of CrPIF1 in C. roseus seedlings altered CrGATA1 and vindoline pathway gene expression in the dark. CrPIF1 repressed CrGATA1 and DAT promoter activity by binding to G/E-box/PBE elements. Our findings reveal a regulatory module involving Phytochrome Interacting Factor -GATA that governs light-mediated biosynthesis of specialized metabolites.",

author = "Yongliang Liu and Barunava Patra and Sitakanta Pattanaik and Ying Wang and Ling Yuan",

note = "Funding Information: 1This work was supported in part by the Harold R. Burton Endowed Professorship to L.Y. and by the National Science Foundation (cooperative agreement no. 1355438 to L.Y.). 2These authors contributed equally to the article. 3Senior authors. 4Author for contact: lyuan3@uky.edu. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Ling Yuan (lyuan3@uky.edu). L.Y., B.P., S.P., and Y.W. designed the research; Y.L., B.P., and S.P. performed experiments; Y.L. and B.P. analyzed data; Y.L., B.P., S.P., Y.W., and L.Y. wrote the article. [OPEN]Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.19.00489 Publisher Copyright: {\textcopyright} 2019 American Society of Plant Biologists.",

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AU - Liu, Yongliang

AU - Patra, Barunava

AU - Pattanaik, Sitakanta

AU - Wang, Ying

AU - Yuan, Ling

N1 - Funding Information: 1This work was supported in part by the Harold R. Burton Endowed Professorship to L.Y. and by the National Science Foundation (cooperative agreement no. 1355438 to L.Y.). 2These authors contributed equally to the article. 3Senior authors. 4Author for contact: lyuan3@uky.edu. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Ling Yuan (lyuan3@uky.edu). L.Y., B.P., S.P., and Y.W. designed the research; Y.L., B.P., and S.P. performed experiments; Y.L. and B.P. analyzed data; Y.L., B.P., S.P., Y.W., and L.Y. wrote the article. [OPEN]Articles can be viewed without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.19.00489 Publisher Copyright: © 2019 American Society of Plant Biologists.

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N2 - Catharanthus roseus is the exclusive source of an array of terpenoid indole alkaloids including the anticancer drugs vincristine and vinblastine, derived from the coupling of catharanthine and vindoline. Leaf-synthesized vindoline is regulated by light. A seven-step enzymatic process is involved in the sequential conversion of tabersonine to vindoline; however, the regulatory mechanism controlling the expression of genes encoding these enzymes has not been elucidated. Here, we identified CrGATA1, an Leu-Leu-Met domain GATA transcription factor that regulates light-induced vindoline biosynthesis in C. roseus seedlings. Expression of CrGATA1 and the vindoline pathway genes T16H2, T3O, T3R, D4H, and DAT was significantly induced by light. In addition, CrGATA1 activated the promoters of five light-responsive vindoline pathway genes in plant cells. Two GATC motifs in the D4H promoter were critical for CrGATA1-mediated transactivation. Transient overexpression of CrGATA1 in C. roseus seedlings resulted in up-regulation of vindoline pathway genes and increased vindoline accumulation. Conversely, virus-induced gene silencing of CrGATA1 in young C. roseus leaves significantly repressed key vindoline pathway genes and reduced vindoline accumulation. Furthermore, we showed that a C. roseus Phytochrome Interacting Factor, CrPIF1, is a repressor of CrGATA1 and vindoline biosynthesis. Transient overexpression or virus-induced gene silencing of CrPIF1 in C. roseus seedlings altered CrGATA1 and vindoline pathway gene expression in the dark. CrPIF1 repressed CrGATA1 and DAT promoter activity by binding to G/E-box/PBE elements. Our findings reveal a regulatory module involving Phytochrome Interacting Factor -GATA that governs light-mediated biosynthesis of specialized metabolites.

AB - Catharanthus roseus is the exclusive source of an array of terpenoid indole alkaloids including the anticancer drugs vincristine and vinblastine, derived from the coupling of catharanthine and vindoline. Leaf-synthesized vindoline is regulated by light. A seven-step enzymatic process is involved in the sequential conversion of tabersonine to vindoline; however, the regulatory mechanism controlling the expression of genes encoding these enzymes has not been elucidated. Here, we identified CrGATA1, an Leu-Leu-Met domain GATA transcription factor that regulates light-induced vindoline biosynthesis in C. roseus seedlings. Expression of CrGATA1 and the vindoline pathway genes T16H2, T3O, T3R, D4H, and DAT was significantly induced by light. In addition, CrGATA1 activated the promoters of five light-responsive vindoline pathway genes in plant cells. Two GATC motifs in the D4H promoter were critical for CrGATA1-mediated transactivation. Transient overexpression of CrGATA1 in C. roseus seedlings resulted in up-regulation of vindoline pathway genes and increased vindoline accumulation. Conversely, virus-induced gene silencing of CrGATA1 in young C. roseus leaves significantly repressed key vindoline pathway genes and reduced vindoline accumulation. Furthermore, we showed that a C. roseus Phytochrome Interacting Factor, CrPIF1, is a repressor of CrGATA1 and vindoline biosynthesis. Transient overexpression or virus-induced gene silencing of CrPIF1 in C. roseus seedlings altered CrGATA1 and vindoline pathway gene expression in the dark. CrPIF1 repressed CrGATA1 and DAT promoter activity by binding to G/E-box/PBE elements. Our findings reveal a regulatory module involving Phytochrome Interacting Factor -GATA that governs light-mediated biosynthesis of specialized metabolites.

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GATA and phytochrome interacting factor transcription factors regulate light-induced vindoline biosynthesis in Catharanthus roseus

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