The C-Domain of the NAC Transcription Factor ANAC019 Is Necessary for pH-Tuned DNA Binding through a Histidine Switch in the N-Domain

Mooseok Kang; Sangyeol Kim; Hyo Jung Kim; Pravesh Shrestha; Ji hye Yun; Bong Kwan Phee; Weontae Lee; Hong Gil Nam; Iksoo Chang

doi:10.1016/j.celrep.2018.01.002

The C-Domain of the NAC Transcription Factor ANAC019 Is Necessary for pH-Tuned DNA Binding through a Histidine Switch in the N-Domain

Mooseok Kang, Sangyeol Kim, Hyo Jung Kim, Pravesh Shrestha, Ji hye Yun, Bong Kwan Phee, Weontae Lee, Hong Gil Nam, Iksoo Chang

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

4 Citations (Scopus)

Abstract

The affinity of transcription factors (TFs) for their target DNA is a critical determinant of gene expression. Whether the DNA-binding domain (DBD) of TFs alone can regulate binding affinity to DNA is an important question for identifying the design principle of TFs. We studied ANAC019, a member of the NAC TF family of proteins in Arabidopsis, and found a well-conserved histidine switch located in its DBD, which regulates both homodimerization and transcriptional control of the TF through H135 protonation. We found that the removal of a C-terminal intrinsically disordered region (IDR) in the TF abolished the pH-dependent binding of the N-terminal DBD to DNA. We propose a mechanism in which long-range electrostatic interactions between DNA and the negatively charged C-terminal IDR turns on the pH dependency of the DNA-binding affinity of the N-terminal DBD. Kang et al. find a histidine switch in the DNA-binding N-domain of the transcription factor ANAC019 that regulates both pH-dependent homodimerization and DNA binding. They propose that long-range electrostatic interactions between DNA and the negatively charged C-terminal turns on the pH dependency of the DNA-binding affinity of the N-terminal DNA-binding domain.

Original language	English
Pages (from-to)	1141-1150
Number of pages	10
Journal	Cell Reports
Volume	22
Issue number	5
DOIs	https://doi.org/10.1016/j.celrep.2018.01.002
Publication status	Published - 2018 Jan 30

Bibliographical note

Funding Information:
This work was funded by the Creative Research Initiatives of the National Research Foundation (NRF) of Korea (2008-0061984 to M.K., S.K., and I.C.) and the DGIST Core Protein Resources Center (N0001822 to I.C.). H.J.K., B.-K.P., and H.G.N. were supported by the Institute for Basic Science (IBS-R013-D1). J.-h.Y., P.S., and W.L. were supported by Mid-career Researcher Program (2017R1A2B2008483 to W.L.) and Basic Science Research Program (2016R1A6A3A04010213 to J.-h.Y.) of NRF. We acknowledge the DGIST Supercomputing and Big Data Center for the dedicated allocation of supercomputing time.

Funding Information:
This work was funded by the Creative Research Initiatives of the National Research Foundation (NRF) of Korea ( 2008-0061984 to M.K., S.K., and I.C.) and the DGIST Core Protein Resources Center ( N0001822 to I.C.). H.J.K., B.-K.P., and H.G.N. were supported by the Institute for Basic Science ( IBS-R013-D1 ). J.-h.Y., P.S., and W.L. were supported by Mid-career Researcher Program ( 2017R1A2B2008483 to W.L.) and Basic Science Research Program ( 2016R1A6A3A04010213 to J.-h.Y.) of NRF . We acknowledge the DGIST Supercomputing and Big Data Center for the dedicated allocation of supercomputing time.

Publisher Copyright:
© 2018 The Authors

All Science Journal Classification (ASJC) codes

Biochemistry, Genetics and Molecular Biology(all)

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10.1016/j.celrep.2018.01.002

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title = "The C-Domain of the NAC Transcription Factor ANAC019 Is Necessary for pH-Tuned DNA Binding through a Histidine Switch in the N-Domain",

abstract = "The affinity of transcription factors (TFs) for their target DNA is a critical determinant of gene expression. Whether the DNA-binding domain (DBD) of TFs alone can regulate binding affinity to DNA is an important question for identifying the design principle of TFs. We studied ANAC019, a member of the NAC TF family of proteins in Arabidopsis, and found a well-conserved histidine switch located in its DBD, which regulates both homodimerization and transcriptional control of the TF through H135 protonation. We found that the removal of a C-terminal intrinsically disordered region (IDR) in the TF abolished the pH-dependent binding of the N-terminal DBD to DNA. We propose a mechanism in which long-range electrostatic interactions between DNA and the negatively charged C-terminal IDR turns on the pH dependency of the DNA-binding affinity of the N-terminal DBD. Kang et al. find a histidine switch in the DNA-binding N-domain of the transcription factor ANAC019 that regulates both pH-dependent homodimerization and DNA binding. They propose that long-range electrostatic interactions between DNA and the negatively charged C-terminal turns on the pH dependency of the DNA-binding affinity of the N-terminal DNA-binding domain.",

author = "Mooseok Kang and Sangyeol Kim and Kim, {Hyo Jung} and Pravesh Shrestha and Yun, {Ji hye} and Phee, {Bong Kwan} and Weontae Lee and Nam, {Hong Gil} and Iksoo Chang",

note = "Funding Information: This work was funded by the Creative Research Initiatives of the National Research Foundation (NRF) of Korea (2008-0061984 to M.K., S.K., and I.C.) and the DGIST Core Protein Resources Center (N0001822 to I.C.). H.J.K., B.-K.P., and H.G.N. were supported by the Institute for Basic Science (IBS-R013-D1). J.-h.Y., P.S., and W.L. were supported by Mid-career Researcher Program (2017R1A2B2008483 to W.L.) and Basic Science Research Program (2016R1A6A3A04010213 to J.-h.Y.) of NRF. We acknowledge the DGIST Supercomputing and Big Data Center for the dedicated allocation of supercomputing time. Funding Information: This work was funded by the Creative Research Initiatives of the National Research Foundation (NRF) of Korea ( 2008-0061984 to M.K., S.K., and I.C.) and the DGIST Core Protein Resources Center ( N0001822 to I.C.). H.J.K., B.-K.P., and H.G.N. were supported by the Institute for Basic Science ( IBS-R013-D1 ). J.-h.Y., P.S., and W.L. were supported by Mid-career Researcher Program ( 2017R1A2B2008483 to W.L.) and Basic Science Research Program ( 2016R1A6A3A04010213 to J.-h.Y.) of NRF . We acknowledge the DGIST Supercomputing and Big Data Center for the dedicated allocation of supercomputing time. Publisher Copyright: {\textcopyright} 2018 The Authors",

year = "2018",

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doi = "10.1016/j.celrep.2018.01.002",

language = "English",

volume = "22",

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The C-Domain of the NAC Transcription Factor ANAC019 Is Necessary for pH-Tuned DNA Binding through a Histidine Switch in the N-Domain. / Kang, Mooseok; Kim, Sangyeol; Kim, Hyo Jung; Shrestha, Pravesh; Yun, Ji hye; Phee, Bong Kwan; Lee, Weontae; Nam, Hong Gil; Chang, Iksoo.

In: Cell Reports, Vol. 22, No. 5, 30.01.2018, p. 1141-1150.

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

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T1 - The C-Domain of the NAC Transcription Factor ANAC019 Is Necessary for pH-Tuned DNA Binding through a Histidine Switch in the N-Domain

AU - Kang, Mooseok

AU - Kim, Sangyeol

AU - Kim, Hyo Jung

AU - Shrestha, Pravesh

AU - Yun, Ji hye

AU - Phee, Bong Kwan

AU - Lee, Weontae

AU - Nam, Hong Gil

AU - Chang, Iksoo

N1 - Funding Information: This work was funded by the Creative Research Initiatives of the National Research Foundation (NRF) of Korea (2008-0061984 to M.K., S.K., and I.C.) and the DGIST Core Protein Resources Center (N0001822 to I.C.). H.J.K., B.-K.P., and H.G.N. were supported by the Institute for Basic Science (IBS-R013-D1). J.-h.Y., P.S., and W.L. were supported by Mid-career Researcher Program (2017R1A2B2008483 to W.L.) and Basic Science Research Program (2016R1A6A3A04010213 to J.-h.Y.) of NRF. We acknowledge the DGIST Supercomputing and Big Data Center for the dedicated allocation of supercomputing time. Funding Information: This work was funded by the Creative Research Initiatives of the National Research Foundation (NRF) of Korea ( 2008-0061984 to M.K., S.K., and I.C.) and the DGIST Core Protein Resources Center ( N0001822 to I.C.). H.J.K., B.-K.P., and H.G.N. were supported by the Institute for Basic Science ( IBS-R013-D1 ). J.-h.Y., P.S., and W.L. were supported by Mid-career Researcher Program ( 2017R1A2B2008483 to W.L.) and Basic Science Research Program ( 2016R1A6A3A04010213 to J.-h.Y.) of NRF . We acknowledge the DGIST Supercomputing and Big Data Center for the dedicated allocation of supercomputing time. Publisher Copyright: © 2018 The Authors

PY - 2018/1/30

Y1 - 2018/1/30

N2 - The affinity of transcription factors (TFs) for their target DNA is a critical determinant of gene expression. Whether the DNA-binding domain (DBD) of TFs alone can regulate binding affinity to DNA is an important question for identifying the design principle of TFs. We studied ANAC019, a member of the NAC TF family of proteins in Arabidopsis, and found a well-conserved histidine switch located in its DBD, which regulates both homodimerization and transcriptional control of the TF through H135 protonation. We found that the removal of a C-terminal intrinsically disordered region (IDR) in the TF abolished the pH-dependent binding of the N-terminal DBD to DNA. We propose a mechanism in which long-range electrostatic interactions between DNA and the negatively charged C-terminal IDR turns on the pH dependency of the DNA-binding affinity of the N-terminal DBD. Kang et al. find a histidine switch in the DNA-binding N-domain of the transcription factor ANAC019 that regulates both pH-dependent homodimerization and DNA binding. They propose that long-range electrostatic interactions between DNA and the negatively charged C-terminal turns on the pH dependency of the DNA-binding affinity of the N-terminal DNA-binding domain.

AB - The affinity of transcription factors (TFs) for their target DNA is a critical determinant of gene expression. Whether the DNA-binding domain (DBD) of TFs alone can regulate binding affinity to DNA is an important question for identifying the design principle of TFs. We studied ANAC019, a member of the NAC TF family of proteins in Arabidopsis, and found a well-conserved histidine switch located in its DBD, which regulates both homodimerization and transcriptional control of the TF through H135 protonation. We found that the removal of a C-terminal intrinsically disordered region (IDR) in the TF abolished the pH-dependent binding of the N-terminal DBD to DNA. We propose a mechanism in which long-range electrostatic interactions between DNA and the negatively charged C-terminal IDR turns on the pH dependency of the DNA-binding affinity of the N-terminal DBD. Kang et al. find a histidine switch in the DNA-binding N-domain of the transcription factor ANAC019 that regulates both pH-dependent homodimerization and DNA binding. They propose that long-range electrostatic interactions between DNA and the negatively charged C-terminal turns on the pH dependency of the DNA-binding affinity of the N-terminal DNA-binding domain.

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The C-Domain of the NAC Transcription Factor ANAC019 Is Necessary for pH-Tuned DNA Binding through a Histidine Switch in the N-Domain

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