A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors

Špela Tomaž; Marko Petek; Tjaša Lukan; Karmen Pogačar; Katja Stare; Erica Teixeira Prates; Daniel A. Jacobson; Jan Zrimec; Gregor Bajc; Matej Butala; Maruša Pompe Novak; Quentin Dudley; Nicola Patron; Ajda Taler-Verčič; Aleksandra Usenik; Dušan Turk; Salomé Prat; Anna Coll; Kristina Gruden

doi:10.1093/plphys/kiac579

A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors

Špela Tomaž, Marko Petek, Tjaša Lukan, Karmen Pogačar, Katja Stare, Erica Teixeira Prates, Daniel A. Jacobson, Jan Zrimec, Gregor Bajc, Matej Butala, Maruša Pompe Novak, Quentin Dudley, Nicola Patron, Ajda Taler-Verčič, Aleksandra Usenik, Dušan Turk, Salomé Prat, Anna Coll, Kristina Gruden

Computational and Predictive Biology

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

4 Scopus citations

Abstract

TGA (TGACG-binding) transcription factors, which bind their target DNA through a conserved basic region leucine zipper (bZIP) domain, are vital regulators of gene expression in salicylic acid (SA)-mediated plant immunity. Here, we investigated the role of StTGA2.1, a potato (Solanum tuberosum) TGA lacking the full bZIP, which we named a mini-TGA. Such truncated proteins have been widely assigned as loss-of-function mutants. We, however, confirmed that StTGA2.1 overexpression compensates for SA-deficiency, indicating a distinct mechanism of action compared with model plant species. To understand the underlying mechanisms, we showed that StTGA2.1 can physically interact with StTGA2.2 and StTGA2.3, while its interaction with DNA was not detected. We investigated the changes in transcriptional regulation due to StTGA2.1 overexpression, identifying direct and indirect target genes. Using in planta transactivation assays, we confirmed that StTGA2.1 interacts with StTGA2.3 to activate StPRX07, a member of class III peroxidases (StPRX), which are known to play role in immune response. Finally, via structural modeling and molecular dynamics simulations, we hypothesized that the compact molecular architecture of StTGA2.1 distorts DNA conformation upon heterodimer binding to enable transcriptional activation. This study demonstrates how protein truncation can lead to distinct functions and that such events should be studied carefully in other protein families.

Original language	English
Pages (from-to)	1934-1952
Number of pages	19
Journal	Plant Physiology
Volume	191
Issue number	3
DOIs	https://doi.org/10.1093/plphys/kiac579
State	Published - Mar 2023

Funding

This work was supported by the Slovenian Research Agency through the research core funding no. P4-0165, the projects no. J4-1777 and J1-2467, the contract no. 1000-22-0105, in accordance with the agreement on (co) financing research activity in 2022, as well as by the European Union Horizon 2020 Framework Programme under grant agreement no. 862858, project ADAPT. Funding was also provided by the Plant-Microbe Interfaces (PMI) Scientific Focus Area in the Genomic Sciences Program of from the US Department of Energy, Office of Science, Office of Biological and Environmental Research. This manuscript has been coauthored by UT-Battelle, LLC under contract no. DE-AC05-00OR22725 with the US Department of Energy. The United States Government retains and the publisher, by accepting the article for publication, acknowledges that the United States Government retains a nonexclusive, paid-up, irrevocable, world-wide license to publish or reproduce the published form of this manuscript, or allow others to do so, for United States Government purposes. The Department of Energy will provide public access to these results of federally sponsored research in accordance with the DOE Public Access Plan (http://energy.gov/downloads/doe-public-access-plan, last accessed September 16, 2020).

Funders	Funder number
Plant-Microbe Interfaces
U.S. Department of Energy
Office of Science
Biological and Environmental Research
Horizon 2020 Framework Programme	862858
UT-Battelle	DE-AC05-00OR22725
Javna Agencija za Raziskovalno Dejavnost RS	J4-1777, J1-2467, P4-0165, 1000-22-0105

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Tomaž, Š., Petek, M., Lukan, T., Pogačar, K., Stare, K., Prates, E. T., Jacobson, D. A., Zrimec, J., Bajc, G., Butala, M., Novak, M. P., Dudley, Q., Patron, N., Taler-Verčič, A., Usenik, A., Turk, D., Prat, S., Coll, A., & Gruden, K. (2023). A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors. Plant Physiology, 191(3), 1934-1952. https://doi.org/10.1093/plphys/kiac579

@article{c5cca1739b72428f97782aebf667ec85,

title = "A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors",

abstract = "TGA (TGACG-binding) transcription factors, which bind their target DNA through a conserved basic region leucine zipper (bZIP) domain, are vital regulators of gene expression in salicylic acid (SA)-mediated plant immunity. Here, we investigated the role of StTGA2.1, a potato (Solanum tuberosum) TGA lacking the full bZIP, which we named a mini-TGA. Such truncated proteins have been widely assigned as loss-of-function mutants. We, however, confirmed that StTGA2.1 overexpression compensates for SA-deficiency, indicating a distinct mechanism of action compared with model plant species. To understand the underlying mechanisms, we showed that StTGA2.1 can physically interact with StTGA2.2 and StTGA2.3, while its interaction with DNA was not detected. We investigated the changes in transcriptional regulation due to StTGA2.1 overexpression, identifying direct and indirect target genes. Using in planta transactivation assays, we confirmed that StTGA2.1 interacts with StTGA2.3 to activate StPRX07, a member of class III peroxidases (StPRX), which are known to play role in immune response. Finally, via structural modeling and molecular dynamics simulations, we hypothesized that the compact molecular architecture of StTGA2.1 distorts DNA conformation upon heterodimer binding to enable transcriptional activation. This study demonstrates how protein truncation can lead to distinct functions and that such events should be studied carefully in other protein families.",

author = "{\v S}pela Toma{\v z} and Marko Petek and Tja{\v s}a Lukan and Karmen Poga{\v c}ar and Katja Stare and Prates, {Erica Teixeira} and Jacobson, {Daniel A.} and Jan Zrimec and Gregor Bajc and Matej Butala and Novak, {Maru{\v s}a Pompe} and Quentin Dudley and Nicola Patron and Ajda Taler-Ver{\v c}i{\v c} and Aleksandra Usenik and Du{\v s}an Turk and Salom{\'e} Prat and Anna Coll and Kristina Gruden",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2022.",

year = "2023",

month = mar,

doi = "10.1093/plphys/kiac579",

language = "English",

volume = "191",

pages = "1934--1952",

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Tomaž, Š, Petek, M, Lukan, T, Pogačar, K, Stare, K, Prates, ET, Jacobson, DA, Zrimec, J, Bajc, G, Butala, M, Novak, MP, Dudley, Q, Patron, N, Taler-Verčič, A, Usenik, A, Turk, D, Prat, S, Coll, A & Gruden, K 2023, 'A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors', Plant Physiology, vol. 191, no. 3, pp. 1934-1952. https://doi.org/10.1093/plphys/kiac579

TY - JOUR

T1 - A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors

AU - Tomaž, Špela

AU - Petek, Marko

AU - Lukan, Tjaša

AU - Pogačar, Karmen

AU - Stare, Katja

AU - Prates, Erica Teixeira

AU - Jacobson, Daniel A.

AU - Zrimec, Jan

AU - Bajc, Gregor

AU - Butala, Matej

AU - Novak, Maruša Pompe

AU - Dudley, Quentin

AU - Patron, Nicola

AU - Taler-Verčič, Ajda

AU - Usenik, Aleksandra

AU - Turk, Dušan

AU - Prat, Salomé

AU - Coll, Anna

AU - Gruden, Kristina

PY - 2023/3

Y1 - 2023/3

N2 - TGA (TGACG-binding) transcription factors, which bind their target DNA through a conserved basic region leucine zipper (bZIP) domain, are vital regulators of gene expression in salicylic acid (SA)-mediated plant immunity. Here, we investigated the role of StTGA2.1, a potato (Solanum tuberosum) TGA lacking the full bZIP, which we named a mini-TGA. Such truncated proteins have been widely assigned as loss-of-function mutants. We, however, confirmed that StTGA2.1 overexpression compensates for SA-deficiency, indicating a distinct mechanism of action compared with model plant species. To understand the underlying mechanisms, we showed that StTGA2.1 can physically interact with StTGA2.2 and StTGA2.3, while its interaction with DNA was not detected. We investigated the changes in transcriptional regulation due to StTGA2.1 overexpression, identifying direct and indirect target genes. Using in planta transactivation assays, we confirmed that StTGA2.1 interacts with StTGA2.3 to activate StPRX07, a member of class III peroxidases (StPRX), which are known to play role in immune response. Finally, via structural modeling and molecular dynamics simulations, we hypothesized that the compact molecular architecture of StTGA2.1 distorts DNA conformation upon heterodimer binding to enable transcriptional activation. This study demonstrates how protein truncation can lead to distinct functions and that such events should be studied carefully in other protein families.

AB - TGA (TGACG-binding) transcription factors, which bind their target DNA through a conserved basic region leucine zipper (bZIP) domain, are vital regulators of gene expression in salicylic acid (SA)-mediated plant immunity. Here, we investigated the role of StTGA2.1, a potato (Solanum tuberosum) TGA lacking the full bZIP, which we named a mini-TGA. Such truncated proteins have been widely assigned as loss-of-function mutants. We, however, confirmed that StTGA2.1 overexpression compensates for SA-deficiency, indicating a distinct mechanism of action compared with model plant species. To understand the underlying mechanisms, we showed that StTGA2.1 can physically interact with StTGA2.2 and StTGA2.3, while its interaction with DNA was not detected. We investigated the changes in transcriptional regulation due to StTGA2.1 overexpression, identifying direct and indirect target genes. Using in planta transactivation assays, we confirmed that StTGA2.1 interacts with StTGA2.3 to activate StPRX07, a member of class III peroxidases (StPRX), which are known to play role in immune response. Finally, via structural modeling and molecular dynamics simulations, we hypothesized that the compact molecular architecture of StTGA2.1 distorts DNA conformation upon heterodimer binding to enable transcriptional activation. This study demonstrates how protein truncation can lead to distinct functions and that such events should be studied carefully in other protein families.

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U2 - 10.1093/plphys/kiac579

DO - 10.1093/plphys/kiac579

M3 - Article

AN - SCOPUS:85150307728

SN - 0032-0889

VL - 191

SP - 1934

EP - 1952

JO - Plant Physiology

JF - Plant Physiology

IS - 3

ER -

A mini-TGA protein modulates gene expression through heterogeneous association with transcription factors

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