Regulation of the Arabidopsis defense transcriptome

doi:10.1016/j.tplants.2004.12.006

Trends in Plant Science

Volume 10, Issue 2, February 2005, Pages 71-78

https://doi.org/10.1016/j.tplants.2004.12.006 Get rights and content

Transcriptional re-programming is a key step of plant defense in response to pathogen recognition. Microarray analyses combined with genetic and biochemical approaches are now enabling us to study basic principles and details of regulatory mechanisms controlling the defense transcriptome in Arabidopsis. Recent results show that signaling pathways used by different defense systems converge and target overlapping gene sets. Furthermore, a quantitative mechanism common to multiple defense systems modulates transcript levels of these defense-associated genes. Most importantly, some transcription factors have been proven to play a pivotal role in disease resistance. Regulatory circuits linking signaling and gene regulation are emerging, suggesting that a complex interplay of transcriptional activators and repressors fine-tunes expression of the defense transcriptome.

Introduction

Plant immune responses involve a multitude of physiological reactions that are induced by pathogen recognition. Such defense reactions include programmed cell death (hypersensitive reaction, HR), modifications of cell walls as well as the production of antimicrobial proteins and metabolites 1, 2. They are associated with up-regulation of pathogenesis-related (PR) genes [3]. Our knowledge about defense-associated gene expression is currently being extended substantially by novel large-scale gene expression profiling technologies 4, 5, 6. Microarray analyses examining transcriptional re-programming in Arabidopsis thaliana triggered by a variety of different pathogens, messenger molecules and elicitors have revealed that in addition to classical PR genes, several hundred to thousands of genes exhibit differential expression after activation of the defense program. Up to 25% of all Arabidopsis genes respond to pathogen infection by altering their transcript levels 7, 8.

The activation of the defense transcriptome is a complex, multidimensional process. Transcript amplitudes of large numbers of genes are modulated following defined spatial and temporal patterns 9, 10. Such comprehensive transcriptional re-programming must require a sophisticated regulatory system. Our understanding of this regulatory system has evolved substantially over recent years. Large-scale transcript profiling has uncovered key features of the Arabidopsis defense transcriptome and its regulation. In particular, transcriptional responses triggered during R-mediated resistance, basal defense and systemic acquired resistance (SAR) (Box 1) have been comprehensively characterized. Several types of transcription factors have been implicated in disease resistance (Box 2). Some of them were shown to be functionally linked to each other and to signal transducers, revealing for the first time regulatory circuits within a complex transcriptional network.

Section snippets

Related defense systems control qualitatively similar transcriptomes

R-mediated resistance, basal defense and SAR are related defense systems effective against biotrophic pathogens. They share regulatory components, such as NDR1, NPR1 and the messenger molecule salicylic acid (SA) (Box 1) 11, 12. Not surprisingly, these commonalities are reflected by similarities at the output level. As determined by microarray studies, all three defense systems target largely overlapping sets of genes 7, 8. Differences between transcript profiles associated with R-mediated

Regulation of the defense transcriptome: a broad role for WRKY factors

Members of several transcription factor families, such as WRKY, ERF, TGA, Whirly and Myb factors, were shown to bind to promoter elements of individual defense-related genes and to regulate their expression (Box 2). Transcriptome analyses have revealed that, in particular, putative binding sites of WRKY factors (W boxes) and related sequence motifs are ubiquitously conserved in upstream regions of genes up-regulated during SAR, R-mediated resistance or basal defenses 7, 17, 18, 19, 22, 23, 24.

Whirly, Myb, ERF and TGA factors are also required for defense reactions

Recent genetic analyses have shown that additional transcription factors also have important roles in plant immune responses. The Whirly-type transcription factor AtWhy1 is required for SA-dependent R-mediated resistance, basal resistance and SAR 39, 40. In response to SA treatment, AtWhy1 tetramers bind to single-stranded GTCAAAA/T-containing DNA. In contrast to TGA factors that operate downstream from NPR1 (see below; Box 1), AtWhy1 acts in an NPR1-independent manner. Single mutations in both

Salicylate, NPR1, TGA and WRKY factors are part of a molecular switch that activates PR1 expression

PR1 is a well characterized marker of defense-responses. Its expression and regulation is discussed here as a paradigm representing a large group of co-regulated genes [7]. A molecular cascade relaying salicylate (SA)-dependent signals to PR1 via NPR1, WRKY and TGA transcription factors has been well established (Figure 2a). This cascade appears to be commonly used by SAR, basal defenses and some R genes. There is a large body of evidence to support the following chain of molecular events.

Conclusions

Considerable progress has been made in recent years concerning our knowledge about gene regulation during plant immune responses. In particular, our understanding of SA and NPR1-dependent regulatory processes has substantially advanced. However, many gaps still need to be filled. The SA-NPR1-dependent regulatory cascade impressively illustrates the degree of sophistication required to use and control the destructive power of immune responses efficiently. A complex interplay between activating

Acknowledgements

I thank Colleen Knoth, Sonia Zarate, Isgouhi Kaloshian and Alexandre Evrard (all UC-Riverside) very much for their critical reading of the manuscript and helpful discussions.

References (95)

I.E. Somssich et al.
Pathogen defense in plants – a paradigm of biological complexity
Trends Plant Sci.
(1998)
S-H. Wu
Plant gene expression profiling with DNA microarrays
Plant Physiol. Biochem.
(2001)
K.M. Ramonell et al.
The genomics parade of defense responses: to infinity and beyond
Curr. Opin. Plant Biol.
(2002)
T. Zhu
Global analysis of gene expression using GeneChip microarrays
Curr. Opin. Plant Biol.
(2003)
J. Glazebrook
Genes controlling expression of defense responses in Arabidopsis – 2001 status
Curr. Opin. Plant Biol.
(2001)
X. Dong
Genetic dissection of systemic acquired resistance
Curr. Opin. Plant Biol.
(2001)
M. Petersen
Arabidopsis map kinase 4 negatively regulates systemic acquired resistance
Cell
(2000)
R.S. Cormack
Leucine zipper-containing WRKY proteins widen the spectrum of immediate early elicitor-induced WRKY transcription factors in parsley
Biochim. Biophys. Acta
(2002)
T. Lahaye
The Arabidopsis RRS1-R disease resistance gene – uncovering the plant's nucleus as the new battlefield of plant defense?
Trends Plant Sci.
(2002)
D. Desveaux
A “Whirly” transcription factor is required for salicylic acid-dependent disease resistance in Arabidopsis
Dev. Cell
(2004)

P.J. Rushton et al.

Transcriptional control of plant genes responsive to pathogens

Curr. Opin. Plant Biol.

(1998)

R. Stracke

The R2R3-MYB gene family in Arabidopsis thaliana

Curr. Opin. Plant Biol.

(2001)

C. Martin et al.

MYB transcription factors in plants

Trends Genet.

(1997)

Z. Mou

Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes

Cell

(2003)

K. Singh

Transcription factors in plant defense and stress responses

Curr. Opin. Plant Biol.

(2002)

R.C. Foley et al.

TGA5 acts as a positive and TGA4 acts as a negative regulator of ocs element activity in Arabidopsis roots in response to defence signals

FEBS Lett

(2004)

L. Gomez-Gomez et al.

Flagellin perception: a paradigm for innate immunity

Trends Plant Sci.

(2002)

T. Eulgem

The WRKY superfamily of plant transcription factors

Trends Plant Sci.

(2000)

M. Jakoby

bZIP transcription factors in Arabidopsis

Trends Plant Sci.

(2002)

N. Gutterson et al.

Regulation of disease resistance pathways by AP2/ERF transcription factors

Curr. Opin. Plant Biol.

(2004)

P. Veronese

In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy

Plant Physiol.

(2003)

E. Kombrink et al.

Pathogenesis-related proteins and plant defense

K. Maleck

The transcriptome of Arabidopsis thaliana during systemic acquired resistance

Nat. Genet.

(2000)

Y. Tao

Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae

Plant Cell

(2003)

E. Schmelzer

Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves

Plant Cell

(1989)

P.J. Rushton

Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling

Plant Cell

(2002)

C.J. Lamb

Emerging strategies for enhancing crop resistance to microbial pathogens

Biotechnology

(1992)

S. Kiedrowski

Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 resistance locus

EMBO J.

(1992)

A.D. Shapiro et al.

The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis

Plant Physiol.

(2001)

P. Tornero

RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed

Plant Cell

(2002)

T. Eulgem

Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance

Plant Physiol.

(2004)

L. Navarro

The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis

Plant Physiol.

(2004)

K. Ramonell

Microarray analysis of chitin elicitation in Arabidopsis thaliana

Mol. Plant Pathol.

(2002)

P.M. Schenk

Coordinated plant defense responses in Arabidopsis revealed by microarray analysis

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

(2000)

J. Glazebrook

Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping

Plant J.

(2003)

W. Chen

Expression profile matrices of Arabidopsis transcription factor genes predict their putative functions in response to environmental stresses

Plant Cell

(2002)

C. Zipfel

Bacterial disease resistance in Arabidopsis through flagellin perception

Nature

(2004)

T. Asai

MAP kinase signalling cascade in Arabidopsis innate immunity

Nature

(2002)

J. Wan

Activation of a mitogen-activated protein kinase pathway in Arabidopsis by chitin

Mol. Plant Pathol.

(2004)

J. Dong

Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response

Plant Mol. Biol.

(2003)

M. Kalde

Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways

Mol. Plant– Microbe Interact.

(2003)

C. Chen et al.

Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor

Plant Physiol.

(2002)

J. Li

The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense

Plant Cell

(2004)

T. Eulgem

Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors

EMBO J.

(1999)

S. Robatzek et al.

Targets of AtWRKY6 regulation during plant senescence and pathogen defense

Genes Dev.

(2002)

J.L. Dangl et al.

Plant pathogens and integrated defence responses to infection

Nature

(2001)

Z. Nimchuk

Recognition and response in the plant immune system

Annu. Rev. Genet.

(2003)

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Trends in Plant Science

Transcriptional networks in plantsRegulation of the Arabidopsis defense transcriptome

Introduction

Section snippets

Related defense systems control qualitatively similar transcriptomes

Regulation of the defense transcriptome: a broad role for WRKY factors

Whirly, Myb, ERF and TGA factors are also required for defense reactions

Salicylate, NPR1, TGA and WRKY factors are part of a molecular switch that activates PR1 expression

Conclusions

Acknowledgements

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Curr. Opin. Plant Biol.

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Cell

Curr. Opin. Plant Biol.

FEBS Lett

Trends Plant Sci.

Trends Plant Sci.

Trends Plant Sci.

Curr. Opin. Plant Biol.

In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy

Plant Physiol.

Pathogenesis-related proteins and plant defense

The transcriptome of Arabidopsis thaliana during systemic acquired resistance

Nat. Genet.

Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae

Plant Cell

Temporal and spatial patterns of gene expression around sites of attempted fungal infection in parsley leaves

Plant Cell

Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling

Plant Cell

Emerging strategies for enhancing crop resistance to microbial pathogens

Biotechnology

Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 resistance locus

EMBO J.

The role of NDR1 in avirulence gene-directed signaling and control of programmed cell death in Arabidopsis

Plant Physiol.

RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed

Plant Cell

Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance

Plant Physiol.

The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis

Plant Physiol.

Microarray analysis of chitin elicitation in Arabidopsis thaliana

Mol. Plant Pathol.

Coordinated plant defense responses in Arabidopsis revealed by microarray analysis

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

Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping

Plant J.

Expression profile matrices of Arabidopsis transcription factor genes predict their putative functions in response to environmental stresses

Plant Cell

Bacterial disease resistance in Arabidopsis through flagellin perception

Nature

MAP kinase signalling cascade in Arabidopsis innate immunity

Nature

Activation of a mitogen-activated protein kinase pathway in Arabidopsis by chitin

Mol. Plant Pathol.

Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response

Plant Mol. Biol.

Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways

Mol. Plant– Microbe Interact.

Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor

Plant Physiol.

The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense

Plant Cell

Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors

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Genes Dev.

Plant pathogens and integrated defence responses to infection

Transcriptional networks in plants
Regulation of the Arabidopsis defense transcriptome