Gene syntaxes modulate gene expression and circuit behavior on plasmids

Abstract Achieving consistent and predictable gene expression from plasmids remains challenging. While much attention has focused on intra-genetic elements like promoters and ribosomal binding sites, the spatial arrangement of genes within plasmids—referred to as gene syntax—also plays a crucial rol...

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Main Authors: Yijie Deng, Hannah E. Maurais, Kai Etheridge, Rahul Sarpeshkar
Format: Article
Language:English
Published: BMC 2025-03-01
Series:Journal of Biological Engineering
Subjects:
Online Access:https://doi.org/10.1186/s13036-025-00493-0
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author Yijie Deng
Hannah E. Maurais
Kai Etheridge
Rahul Sarpeshkar
author_facet Yijie Deng
Hannah E. Maurais
Kai Etheridge
Rahul Sarpeshkar
author_sort Yijie Deng
collection DOAJ
description Abstract Achieving consistent and predictable gene expression from plasmids remains challenging. While much attention has focused on intra-genetic elements like promoters and ribosomal binding sites, the spatial arrangement of genes within plasmids—referred to as gene syntax—also plays a crucial role in shaping gene expression dynamics. This study addresses the largely overlooked impact of gene syntaxes on gene expression variability and accuracy. Utilizing a dual-fluorescent protein system, we systematically investigated how different gene orientations and orders affect expression profiles including mean levels, relative expression ratios, and cell-to-cell variations. We found that arbitrary gene placement on a plasmid can cause significantly different expression means and ratios. Genes aligned in the same direction as a plasmid’s origin of replication (Ori) typically exhibit higher expression levels; adjacent genes in the divergent orientation tend to suppress each other’s expression; altering gene order without changing orientation can yield varied expression. Despite unchanged total cell-to-cell variation across different syntaxes, gene syntaxes can also influence intrinsic and extrinsic noise. Interestingly, cell-to-cell variation appears to depend on the reporter proteins, with RFP consistently showing higher variation than GFP. Moreover, the effects of gene syntax can propagate to downstream circuits, strongly affecting the performance of incoherent feedforward loops and contributing to unpredictable outcomes in genetic networks. Our findings reveal that gene syntaxes on plasmids modulate gene expression and circuit behavior, providing valuable insights for the rational design of plasmids and genetic circuits.
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spelling doaj-art-3dd34b9f10a3435cbd96d3031e6f7cbe2025-08-20T02:49:23ZengBMCJournal of Biological Engineering1754-16112025-03-0119111510.1186/s13036-025-00493-0Gene syntaxes modulate gene expression and circuit behavior on plasmidsYijie Deng0Hannah E. Maurais1Kai Etheridge2Rahul Sarpeshkar3Thayer School of Engineering, Dartmouth CollegeThayer School of Engineering, Dartmouth CollegeThayer School of Engineering, Dartmouth CollegeThayer School of Engineering, Dartmouth CollegeAbstract Achieving consistent and predictable gene expression from plasmids remains challenging. While much attention has focused on intra-genetic elements like promoters and ribosomal binding sites, the spatial arrangement of genes within plasmids—referred to as gene syntax—also plays a crucial role in shaping gene expression dynamics. This study addresses the largely overlooked impact of gene syntaxes on gene expression variability and accuracy. Utilizing a dual-fluorescent protein system, we systematically investigated how different gene orientations and orders affect expression profiles including mean levels, relative expression ratios, and cell-to-cell variations. We found that arbitrary gene placement on a plasmid can cause significantly different expression means and ratios. Genes aligned in the same direction as a plasmid’s origin of replication (Ori) typically exhibit higher expression levels; adjacent genes in the divergent orientation tend to suppress each other’s expression; altering gene order without changing orientation can yield varied expression. Despite unchanged total cell-to-cell variation across different syntaxes, gene syntaxes can also influence intrinsic and extrinsic noise. Interestingly, cell-to-cell variation appears to depend on the reporter proteins, with RFP consistently showing higher variation than GFP. Moreover, the effects of gene syntax can propagate to downstream circuits, strongly affecting the performance of incoherent feedforward loops and contributing to unpredictable outcomes in genetic networks. Our findings reveal that gene syntaxes on plasmids modulate gene expression and circuit behavior, providing valuable insights for the rational design of plasmids and genetic circuits.https://doi.org/10.1186/s13036-025-00493-0Plasmid designGenetic contextGene syntaxGenetic circuitsGene noiseIncoherent feedforward loops
spellingShingle Yijie Deng
Hannah E. Maurais
Kai Etheridge
Rahul Sarpeshkar
Gene syntaxes modulate gene expression and circuit behavior on plasmids
Journal of Biological Engineering
Plasmid design
Genetic context
Gene syntax
Genetic circuits
Gene noise
Incoherent feedforward loops
title Gene syntaxes modulate gene expression and circuit behavior on plasmids
title_full Gene syntaxes modulate gene expression and circuit behavior on plasmids
title_fullStr Gene syntaxes modulate gene expression and circuit behavior on plasmids
title_full_unstemmed Gene syntaxes modulate gene expression and circuit behavior on plasmids
title_short Gene syntaxes modulate gene expression and circuit behavior on plasmids
title_sort gene syntaxes modulate gene expression and circuit behavior on plasmids
topic Plasmid design
Genetic context
Gene syntax
Genetic circuits
Gene noise
Incoherent feedforward loops
url https://doi.org/10.1186/s13036-025-00493-0
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AT hannahemaurais genesyntaxesmodulategeneexpressionandcircuitbehavioronplasmids
AT kaietheridge genesyntaxesmodulategeneexpressionandcircuitbehavioronplasmids
AT rahulsarpeshkar genesyntaxesmodulategeneexpressionandcircuitbehavioronplasmids