RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription

Li, Lingting; Molodtsov, Vadim; Lin, Wei; Ebright, Richard H.; Zhang, Yu

doi:10.1073/pnas.1920747117

Title: RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription

Abstract

All organisms—bacteria, archaea, and eukaryotes—have a transcription initiation factor that contains a structural module that binds within the RNA polymerase (RNAP) active-center cleft and interacts with template-strand single-stranded DNA (ssDNA) in the immediate vicinity of the RNAP active center. This transcription initiation-factor structural module preorganizes template-strand ssDNA to engage the RNAP active center, thereby facilitating binding of initiating nucleotides and enabling transcription initiation from initiating mononucleotides. However, this transcription initiation-factor structural module occupies the path of nascent RNA and thus presumably must be displaced before or during initial transcription. In this paper, we report four sets of crystal structures of bacterial initially transcribing complexes that demonstrate and define details of stepwise, RNA-extension-driven displacement of the “σ-finger” of the bacterial transcription initiation factor σ. The structures reveal that—for both the primary σ-factor and extracytoplasmic (ECF) σ-factors, and for both 5'-triphosphate RNA and 5'-hydroxy RNA—the “σ-finger” is displaced in stepwise fashion, progressively folding back upon itself, driven by collision with the RNA 5'-end, upon extension of nascent RNA from ~5 nt to ~10 nt.

Authors:

Li, Lingting ^[1]; Molodtsov, Vadim ^[2]; Lin, Wei ^[2];

^[2];

^[3]

Chinese Academy of Sciences (CAS), Shanghai (China); Univ. of Chinese Academy of Sciences, Beijing (China)
Rutgers Univ., Piscataway, NJ (United States)
Chinese Academy of Sciences (CAS), Shanghai (China); Rutgers Univ., Piscataway, NJ (United States)

Publication Date:: Tue Mar 03 00:00:00 EST 2020

Research Org.:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: Chinese Academy of Sciences (CAS); National Natural Science Foundation of China (NSFC); National Institutes of Health (NIH)

OSTI Identifier:: 1608866

Grant/Contract Number:: 31670067; 31822001; QYZDB-SSWSMC005; GM041376

Resource Type:: Accepted Manuscript

Journal Name:: Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:: Journal Volume: 117; Journal Issue: 11; Journal ID: ISSN 0027-8424

Publisher:: National Academy of Sciences

Country of Publication:: United States

Language:: ENGLISH

Subject:: 59 BASIC BIOLOGICAL SCIENCES; transcription initiation; initial transcription; promoter escape; sigma factor; initiation factor

Citation Formats


                    Li, Lingting, Molodtsov, Vadim, Lin, Wei, Ebright, Richard H., and Zhang, Yu. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription.  United States: N. p., 2020. 
Web.  doi:10.1073/pnas.1920747117.

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                    Li, Lingting, Molodtsov, Vadim, Lin, Wei, Ebright, Richard H., & Zhang, Yu. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription.  United States.  https://doi.org/10.1073/pnas.1920747117

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                    Li, Lingting, Molodtsov, Vadim, Lin, Wei, Ebright, Richard H., and Zhang, Yu. Tue .  
"RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription".  United States.  https://doi.org/10.1073/pnas.1920747117.  https://www.osti.gov/servlets/purl/1608866.

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@article{osti_1608866,

  title        = {RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription},

  author       = {Li, Lingting and Molodtsov, Vadim and Lin, Wei and Ebright, Richard H. and Zhang, Yu},

  abstractNote = {All organisms—bacteria, archaea, and eukaryotes—have a transcription initiation factor that contains a structural module that binds within the RNA polymerase (RNAP) active-center cleft and interacts with template-strand single-stranded DNA (ssDNA) in the immediate vicinity of the RNAP active center. This transcription initiation-factor structural module preorganizes template-strand ssDNA to engage the RNAP active center, thereby facilitating binding of initiating nucleotides and enabling transcription initiation from initiating mononucleotides. However, this transcription initiation-factor structural module occupies the path of nascent RNA and thus presumably must be displaced before or during initial transcription. In this paper, we report four sets of crystal structures of bacterial initially transcribing complexes that demonstrate and define details of stepwise, RNA-extension-driven displacement of the “σ-finger” of the bacterial transcription initiation factor σ. The structures reveal that—for both the primary σ-factor and extracytoplasmic (ECF) σ-factors, and for both 5'-triphosphate RNA and 5'-hydroxy RNA—the “σ-finger” is displaced in stepwise fashion, progressively folding back upon itself, driven by collision with the RNA 5'-end, upon extension of nascent RNA from ~5 nt to ~10 nt.},

  doi          = {10.1073/pnas.1920747117},

  journal      = {Proceedings of the National Academy of Sciences of the United States of America},

  number       = 11,

  volume       = 117,

  place        = {United States},

  year         = {Tue Mar 03 00:00:00 EST 2020},

  month        = {Tue Mar 03 00:00:00 EST 2020}

}

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Title: RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription

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Near-atomic resolution visualization of human transcription promoter opening journal, May 2016

The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) σ factor protein family: ECF σ factor classification journal, September 2009

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journal, February 2014

Structures of the RNA polymerase- 54 reveal new and conserved regulatory strategies
journal, August 2015

GE23077 binds to the RNA polymerase ‘i’ and ‘i+1’ sites and prevents the binding of initiating nucleotides
journal, April 2014

Structural mechanism of ATP-independent transcription initiation by RNA polymerase I
journal, June 2017

Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution
journal, May 2002

Structural Basis of Transcription Initiation
journal, October 2012

Extra Cytoplasmic Function sigma factors, recent structural insights into promoter recognition and regulation
journal, February 2015

The Structural Basis for Promoter −35 Element Recognition by the Group IV σ Factors
journal, August 2006

Structure of an RNA Polymerase II–TFIIB Complex and the Transcription Initiation Mechanism
journal, November 2009

Bacterial Sigma Factors: A Historical, Structural, and Genomic Perspective
journal, September 2014

Transcription initiation complex structures elucidate DNA opening
journal, May 2016

Structural Basis of Transcription Initiation: RNA Polymerase Holoenzyme at 4 Å Resolution
journal, May 2002

Growth phase-dependent control of transcription start site selection and gene expression by nanoRNAs
journal, July 2012

Region 3.2 of the σ Subunit Contributes to the Binding of the 3′-Initiating Nucleotide in the RNA Polymerase Active Center and Facilitates Promoter Clearance during Initiation
journal, May 2006

RNA Polymerase Accommodates a Pause RNA Hairpin by Global Conformational Rearrangements that Prolong Pausing
journal, March 2018

Structures of E . coli σ ^S -transcription initiation complexes provide new insights into polymerase mechanism
journal, March 2016

Structure of a bacterial RNA polymerase holoenzyme open promoter complex
journal, September 2015

Conserved Region 3 of Escherichia coli σ ⁷⁰ Is Implicated in the Process of Abortive Transcription
journal, August 1996

X-ray Crystal Structure of Escherichia coli RNA Polymerase σ ⁷⁰ Holoenzyme
journal, February 2013

Backtracked and paused transcription initiation intermediate of Escherichia coli RNA polymerase
journal, October 2016

Structures and mechanism of transcription initiation by bacterial ECF factors
journal, May 2019

Structural basis of ECF-σ-factor-dependent transcription initiation
journal, February 2019

Structural basis for transcription initiation by bacterial ECF σ factors
journal, March 2019

Pausing controls branching between productive and non-productive pathways during initial transcription in bacteria
journal, April 2018

Structural Insights into the Eukaryotic Transcription Initiation Machinery
journal, May 2017

Distinct functions of the RNA polymerase σ subunit region 3.2 in RNA priming and promoter escape
journal, January 2014

Transcription Factor B Contacts Promoter DNA Near the Transcription Start Site of the Archaeal Transcription Initiation Complex
journal, November 2003

Near-atomic resolution visualization of human transcription promoter opening
journal, May 2017

Bacterial Sigma Factors: A Historical, Structural, and Genomic Perspective
journal, September 2014