Promoting the promoter

doi:10.1016/j.plantsci.2010.09.009

Plant Science

Volume 180, Issue 2, February 2011, Pages 182-189

https://doi.org/10.1016/j.plantsci.2010.09.009 Get rights and content

Abstract

Recent evolutionary studies clearly indicate that evolution is mainly driven by changes in the complex mechanisms of gene regulation and not solely by polymorphism in protein-encoding genes themselves. After a short description of the cis-regulatory mechanism, we intend in this review to argue that by applying newly available technologies and by merging research areas such as evolutionary and developmental biology, population genetics, ecology and molecular cell biology it is now possible to study evolution in an integrative way. We contend that, by analysing the effects of promoter sequence variation on phenotypic diversity in natural populations, we will soon be able to break the barrier between the study of extant genetic variability and the study of major developmental changes. This will lead to an integrative view of evolution at different scales. Because of their sessile nature and their continuous development, plants must permanently regulate their gene expression to react to their environment, and can, therefore, be considered as a remarkable model for these types of studies.

Research highlights

▶ New high-throupout techniques provide huge amounts of cis-regulatory sequences and their associate proteins. ▶ Large sets of cis-regulatory sequences and their transcription factors can be studied from different evolutionary field perspectives. ▶ These different evolutionary study aspects might explain both micro- and macro-evlution. ▶ This leads to an integrative understanding of evolution.

Section snippets

cis-Regulation: a central role in evolution

Because of their sessile character and their continuous development, plants must constantly regulate and modulate their developmental and homeostatic gene expression throughout their entire life. These features allow them to react remarkably well to the environment by physiological changes caused by the underlying molecular regulation. Already previous studies have stressed the fact that plant science might bridge molecular biology, ecology and evolution [1] by using the model system

The transcription process, the promoter structures and how to find them

The next three paragraphs are a review of basic molecular biology knowledge about promoters. Expert readers may directly jump to the beginning of the 4th paragraph.

Studying cis-regulatory sequences offers new perspectives for understanding evolution

Most studies of promoter regions stress the limits of our capacity and tools to study them. Thanks to recent technological advances, we are offered new possibilities to study cis-regulatory regions. Some are already feasible but not widely applied yet; others will be in the near future. Here we will detail the innovative perspectives to understand macro- and micro-evolutionary processes from an integrative point of view.

A step further: future developments

Some complementary ideas, more speculative, using tools expected to be developed in the near future, could enrich cis-regulatory sequence studies by investigating molecular evolution from a wider perspective.

The specificity between a TF and its binding site depends on cell state and determines the role of the gene in a given organism. Therefore, characterising the affinity of variants of promoters to a specific TF, or the affinity of a specific promoter to different TFs, by highly sensitive

Conclusion

Studying transcriptional regulatory sequences is central to understanding of both micro- and macro-evolution. By combining Evo-Devo and population-genetic approaches, the barrier between these two research areas can be cracked, and mechanisms of evolution can be studied in an integrative way. Due to their complexity and their multiple interactions, cis-regulatory sequences should also be studied in their ecological contexts, in situ, to avoid any experimental bias. Specifically,

Acknowledgements

The authors are grateful to Ana Stambolia-Kovach and Carol Loopstra from scientific advices on promoter works. We also thank four anonymous reviewers who gave constructive and helpful comments on the manuscript. This research was funded by INRA (Institut National pour la Recherche Agronomique) “Hagneré” post-doc program and the EU-funded ENERGIRAVI project.

References (81)

D.J. Miller et al.
Cnidarians and ancestral genetic complexity in the animal kingdom
Trends Genet.
(2005)
U. Technau et al.
Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians
Trends Genet.
(2005)
Y. Zhao et al.
A developmental view of microRNA function
Trends Biochem. Sci.
(2007)
M.W. Rhoades et al.
Prediction of plant miRNA targets
Cell
(2002)
E. Allen et al.
miRNA-directed phasing during trans-acting siRNA biogenesis in plants
Cell
(2005)
P. Korber et al.
The histone chaperone Asf1 increases the rate of histone eviction at the yeast PHO5 and PHO8 promoters
J. Biol. Chem.
(2006)
M.W. Adkins et al.
Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes
Mol. Cell
(2004)
Z.Y. Ni et al.
Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes
Mol. Cell
(2004)
A.G. Pedersen et al.
The biology of eukaryotic promoter prediction – a review
Comput. Chem.
(1999)
H.D. Priest et al.
cis-Regulatory elements in plant cell signaling
Curr. Opin. Plant Biol.
(2009)

J.S. Fassler et al.

Promoters and basal transcription machinery in eubacteria and eukaryotes: concepts, definitions, and analogies, RNA polymerase and associated factors

Methods Enzymol.

(1996)

S.T. Smale

Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes

Biochim. Biophys. Acta

(1997)

J.M. Gottesfeld et al.

Mitotic repression of the transcriptional machinery

Trends Biochem. Sci.

(1997)

D.S. Prestridge

Predicting Pol-II promoter sequences using transcription factor-binding sites

J. Mol. Biol.

(1995)

M.J. Buck et al.

ChIP-chip: considerations for the design, analysis, and application of genome-wide chromatin immunoprecipitation experiments

Genomics

(2004)

R. Schaffer et al.

Monitoring genome-wide expression in plants

Curr. Opin. Biotechnol.

(2000)

M.C. Urban et al.

The evolutionary ecology of metacommunities

Trends Ecol. Evol.

(2008)

J. Silvertown

Plant coexistence and the niche

Trends Ecol. Evol.

(2004)

Z.W. Zhu et al.

A specialized nucleosome modulates transcription factor access to a C-glabrata metal responsive promoter

Cell

(1996)

K. Liu et al.

DNA sequence encodes information for nucleosome array formation

J. Mol. Biol.

(1997)

T. Mitchell-Olds et al.

Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis

Nature

(2006)

R. DeCook et al.

Genetic regulation of gene expression during shoot development in Arabidopsis

Genetics

(2006)

J. de Meaux et al.

Allele-specific assay reveals functional variation in the chalcone synthase promoter of Arabidopsis thaliana that is compatible with neutral evolution

Plant Cell

(2005)

S.B. Carroll

Evolution at two levels: on genes and forms

PLos Biol.

(2005)

G.A. Wray

Transcriptional regulation and the evolution of development

Int. J. Dev. Biol.

(2003)

G.P. Wagner et al.

Evolutionary novelties

Curr. Biol.

(2010)

H.E. Hoekstra et al.

The locus of evolution: Evo-Devo and the genetics of adaptation

Evolution

(2007)

E. Pennisi

Deciphering the genetics of evolution

Science

(2008)

I. Tirosh et al.

Promoter architecture and the evolvability of gene expression

J. Biol.

(2009)

M.D. Shapiro et al.

Genetic and developmental basis of evolutionary pelvic reduction in three spine sticklebacks

Nature

(2004)

A.V. Badyaev et al.

The evolution of sexual size dimorphism in the house finch. V. Maternal effects, evolution

Int. J. Org. Evol.

(2003)

N. Gompel et al.

Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila

Nature

(2005)

M.C. King et al.

Evolution at two levels in humans and chimpanzees

Science

(1975)

M. Akam

Hox genes and the evolution of diverse body plans

Philos. Trans. R. Soc. Lond. B: Biol. Sci.

(1995)

M. Akam

Arthropods: developmental diversity within a (super) phylum

Proc. Natl. Acad. Sci. U.S.A.

(2000)

W. Arthur

The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology

(1997)

E.M. Meyerowitz

Comparative genomics – plants compared to animals: the broadest comparative study of development

Science

(2002)

R.L. Wang et al.

The limits of selection during maize domestication

Nature

(1999)

H. Wang et al.

The origin of the naked grains of maize

Nature

(2005)

S.B. Carroll et al.

From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design

(2005)

Cited by (15)

Cotton promoters for controlled gene expression
2023, Electronic Journal of Biotechnology
Cotton (Gossypium hirsutum) is one of the most important crops and is the main source of fiber for the textile industry, but its productivity is still hampered by several challenges, such as pests, diseases and abiotic stresses. This scenario has increased interest in achieving cotton events with greater productivity and sustainability through biotechnological approaches. An essential component of these strategies is the controlled expression of the gene of interest, suggesting that promoters are a key element. These promoters are generally divided into three types: constitutive, spatiotemporal, and inducible. However, to date, this diversity of promoter activity has not been as widely explored in cotton improvement. In this review, we provide an overview of cotton promoters that can be used to achieve fine-tuning of expression, facilitating decision-making and improving the ability to develop desirable traits in cotton plants. In addition, we present new approaches to identify promoters that may be useful for the development of new tools for cotton improvement.
How to cite: Atella AL, Grossi-de-Sá MF, Alves-Ferreira M. Cotton promoters for controlled gene expression. Electron J Biotechnol 2023;62. https://doi.org/10.1016/j.ejbt.2022.12.002.
Systematic analysis and comparison of ABC proteins superfamily confer structural, functional and evolutionary insights into four cotton species
2022, Industrial Crops and Products
Citation Excerpt :
Possibly, overexpression of a few of these genes might impart stress tolerance in transgenic plants. The ABC transporter gene family is widely characterized in various plants, with 179 ABC genes in Brassica rapa (Yan et al., 2017), 154 members in tomato (Ofori et al., 2018), 135 members in Vitis vinifera (Çakır and Kılıçkaya, 2013), 131 in Arabidopsis thaliana (Verrier et al., 2008), 130 in Zea mays (Pang et al., 2013), and 121 ABC genes in Oryza sativa (Rea, 2007; Vedel and Scotti, 2011) (Table 1). In comparison, G. hirsutum encompasses the highest number of ABC transporters, which is not unexpected since G. hirsutum is a polyploidy and has experienced two whole genome duplications during evolution, along with substantial segmental and tandem duplications for its large-scale expansion.
ATP binding cassette transporters (ABCTs) is one of the largest gene superfamily comprising of integral membrane proteins that are ubiquitously found in all domains of life and implicated in ATP dependent active transport of ligands across the concentration gradient. We present here the identification and distribution of ABC proteins from seven plant species into four groups (Full, Half, Quarter and ABC2 molecules), eight families (ABCA to ABCG and ABCI) and twelve sub families (MDR, PDR, MRP, PMP, AOH, ATH, ATM, TAP, WBC, RLI, GCN and NAP) based on topology, orientation, size, and phylogenetic relationships with main focus on four cotton species especially tetraploid Gossypium hirsutum (Gh) encoding 320 ORFs. Dynamics of complex formation of structurally characterized ABCTs from each subfamily shows their kinetic and molecular mechanisms to combine the ATP hydrolysis and binding for substrate translocation, portraying a "structure to function relationship". Analysis of protein motif and genomic organizations displayed structural and functional conservation within same subfamily but diverged among the different subfamilies. Abundance of small sized single ABCs signifies the higher gene death/birth rate and ongoing evolution for functional advancements and environmental adaptability. Gene duplication relationship analysis illustrates the major role of tandem and segmental duplication in large scale expansion of ABC gene family in mentioned species. The overall Ka/Ks ratio indicated the intense purifying selection of ABC genes in four cotton species during evolution. In addition, tissue specific expression profiling, abiotic stress resistance and Co-expression networking of GhABCs infers their role in diverse range of molecular, cellular and biological processes. Cis-elements and gene enrichments also supported their predicted roles in substrates translocation, xenobiotic detoxiﬁcation, lipid metabolism, hormonal and abiotic stresses responses. Forward and reverse genetics along with evolutionary trajectories, structural dynamics and validated expression profiling will provide much-needed clarity and a qualitative molecular framework for future research. This study will further broaden our insights into the evolution and functional elucidation of ABC gene family in cotton.
A novel pairwise comparison method for in silico discovery of statistically significant cis-regulatory elements in eukaryotic promoter regions: Application to Arabidopsis
2015, Journal of Theoretical Biology
Citation Excerpt :
The interaction of transcription factors with CREs, located within promoter regions, leads to modulate transcription of target genes. Indeed, promoters contain functional DNA sequences which receive and integrate signals from multiple transcription factors by their modular and combinatorial nature (Vedel and Scotti, 2011; Werner, 2001). Identification of CREs and their organization modules has opened a new vista in understanding gene expression and regulation (Deihimi et al., 2012; Hosseinpour et al., 2013).
Cis regulatory elements (CREs), located within promoter regions, play a significant role in the blueprint for transcriptional regulation of genes. There is a growing interest to study the combinatorial nature of CREs including presence or absence of CREs, the number of occurrences of each CRE, as well as of their order and location relative to their target genes. Comparative promoter analysis has been shown to be a reliable strategy to test the significance of each component of promoter architecture. However, it remains unclear what level of difference in the number of occurrences of each CRE is of statistical significance in order to explain different expression patterns of two genes. In this study, we present a novel statistical approach for pairwise comparison of promoters of Arabidopsis genes in the context of number of occurrences of each CRE within the promoters. First, using the sample of 1000 Arabidopsis promoters, the results of the goodness of fit test and non-parametric analysis revealed that the number of occurrences of CREs in a promoter sequence is Poisson distributed. As a promoter sequence contained functional and non-functional CREs, we addressed the issue of the statistical distribution of functional CREs by analyzing the ChIP-seq datasets. The results showed that the number of occurrences of functional CREs over the genomic regions was determined as being Poisson distributed. In accordance with the obtained distribution of CREs occurrences, we suggested the Audic and Claverie (AC) test to compare two promoters based on the number of occurrences for the CREs. Superiority of the AC test over Chi-square (2×2) and Fisher’s exact tests was also shown, as the AC test was able to detect a higher number of significant CREs. The two case studies on the Arabidopsis genes were performed in order to biologically verify the pairwise test for promoter comparison. Consequently, a number of CREs with significantly different occurrences was identified between the promoters. The results of the pairwise comparative analysis together with the expression data for the studied genes revealed the biological significance of the identified CREs.
Identification of fungus-responsive cis-acting element in the promoter of Brassica juncea chitinase gene, BjCHI1
2014, Plant Science
Citation Excerpt :
Another possible explanation is that the region (−409 to −337) might play a role of enhancers which enhance the activity of BjC-P by binding coactivators. Because enhancers could activate transcription by promoting the assembly of stable transcription complexes in a repressive chromatin environment and once such a complex is formed, it could overcome the chromatin-mediated transcriptional repression, so deletion of the region led to lose of the activation [56–58]. However, these need to be illustrated experimentally, and further investigation on roles of the region (−409 to −337) will be of great interest.
Chitinases are a group of pathogenesis-related proteins. The Brassica juncea chitinase gene BjCHI1 is highly inducible by pathogenic fungal infection, suggesting that the promoter of BjCHI1 might contain specific cis-acting element responsive to fungal attack. To identify the fungus-responsive element in BjCHI1 promoter (BjC-P), a series of binary plant transformation vectors were constructed by fusing the BjC-P or its deletion-derivatives to β-glucuronidase (GUS) reporter gene. Expression of the GUS reporter gene was systematically assayed by a transient gene expression system in Nicotiana benthamiana leaves treated with fungal elicitor Hexa-N-Acetyl-Chitohexaose, as well as in transgenic Arabidopsis plants inoculated with fungus Botrytis cinerea. The histochemical and quantitative GUS assays showed that the W-box-like element (GTAGTGACTCAT) in the region (−668 to −657) was necessary for the fungus-response, although there were another five W-box-like elements in BjC-P. In addition, gain-of-function analysis demonstrated that the fragment (−409 to −337) coupled to the W-box-like element was needed for full magnitude of the fungal induction. These results revealed the existence of a novel regulation mechanism of W-box-like element involved in plant pathogenic resistance, and will benefit the potential application of BjC-P in engineering crops.
From plant gene regulatory grids to network dynamics
2012, Biochimica et Biophysica Acta - Gene Regulatory Mechanisms
Citation Excerpt :
In plants, as in other eukaryotic systems, 50 bp upstream and 50 bp downstream of the transcriptional start site (TSS) have been considered enough to capture the “core” promoter responsible for recruiting the RNA polymerase and promoting basal transcription [53,54]. These “core” set of DNA elements, which remain ill defined in plants [55], are described as the minimum region required for transcription, and are expected to work in concert with other DNA-regulatory elements such as enhancers, silencers and boundary control elements to make up the full promoter [56]. The concept of the full promoter, encompassing all the cis elements modulating gene expression, is more fluid than that of the core promoter, and has evolved as our understanding of gene regulation has progressed (Fig. 3).
The regulation of gene expression is the most basic level at which genotypes encoded in DNA can manifest themselves into observable phenotypes. In eukaryotes, gene regulatory networks (GRNs) describe the regulatory web through which transcription factors and microRNAs tightly regulate the spatial and temporal expression of genes. In yeast, Escherichia coli, and animals the study of GRNs has uncovered many of the network properties responsible for creating complex regulatory behavior such as organism growth, development, and response to environmental stimuli. In plants, the study of GRNs is just starting to gain momentum thanks to new high quality genomes and the development of new tools for GRN mapping. Here, we review the latest advancements in the study of plant GRNs and describe the tools and techniques used to produce them. We also discuss the emerging field of network dynamics and the methods currently being developed to measure network dynamics and function in plants.
PDR9 allelic variation and MYB63 modulate nutrient-dependent coumarin homeostasis in Arabidopsis
2024, Plant Journal

View all citing articles on Scopus

View full text

ReviewPromoting the promoter

Abstract

Research highlights

Section snippets

cis-Regulation: a central role in evolution

The transcription process, the promoter structures and how to find them

Studying cis-regulatory sequences offers new perspectives for understanding evolution

A step further: future developments

Conclusion

Acknowledgements

Trends Genet.

Trends Genet.

Trends Biochem. Sci.

Cell

Cell

J. Biol. Chem.

Mol. Cell

Mol. Cell

Comput. Chem.

Curr. Opin. Plant Biol.

Methods Enzymol.

Biochim. Biophys. Acta

Trends Biochem. Sci.

J. Mol. Biol.

Genomics

Curr. Opin. Biotechnol.

Trends Ecol. Evol.

Trends Ecol. Evol.

Cell

J. Mol. Biol.

Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis

Nature

Genetic regulation of gene expression during shoot development in Arabidopsis

Genetics

Allele-specific assay reveals functional variation in the chalcone synthase promoter of Arabidopsis thaliana that is compatible with neutral evolution

Plant Cell

Evolution at two levels: on genes and forms

PLos Biol.

Transcriptional regulation and the evolution of development

Int. J. Dev. Biol.

Evolutionary novelties

Curr. Biol.

The locus of evolution: Evo-Devo and the genetics of adaptation

Evolution

Deciphering the genetics of evolution

Science

Promoter architecture and the evolvability of gene expression

J. Biol.

Genetic and developmental basis of evolutionary pelvic reduction in three spine sticklebacks

Nature

The evolution of sexual size dimorphism in the house finch. V. Maternal effects, evolution

Int. J. Org. Evol.

Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila

Nature

Evolution at two levels in humans and chimpanzees

Science

Hox genes and the evolution of diverse body plans

Philos. Trans. R. Soc. Lond. B: Biol. Sci.

Arthropods: developmental diversity within a (super) phylum

Proc. Natl. Acad. Sci. U.S.A.

The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology

Comparative genomics – plants compared to animals: the broadest comparative study of development

Science

The limits of selection during maize domestication

Nature

The origin of the naked grains of maize

Nature

From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design

Review
Promoting the promoter