Timing of plant immune responses by a central circadian regulator

Wang, Wei; Barnaby, Jinyoung Y.; Tada, Yutaka; Li, Hairi; Tör, Mahmut; Caldelari, Daniela; Lee, Dae-un; Fu, Xiang‐Dong; Dong, Xinnian

doi:10.1038/nature09766

Cited by 393 publications

(402 citation statements)

References 27 publications

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“…Genes peaking in expression 10 to 12 h after dawn were overrepresented for several defense-related terms, including "JA biosynthesis," "response to fungus," and "response to biotic stress" (see Supplemental Data Set 8 online). Hence, in contrast with the CCA1-controlled defense genes identified by Wang et al (2011), defense-related genes appear to peak in the early afternoon in our experiment. Over 60% of the 2404 rhythmic genes from the mock-inoculated leaves were differentially expressed in response to B. cinerea infection (1521 genes).…”

Section: B Cinerea Infection Dampens Clock Gene Oscillationsmentioning

confidence: 55%

Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis

et al. 2012

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Transcriptional reprogramming forms a major part of a plant's response to pathogen infection. Many individual components and pathways operating during plant defense have been identified, but our knowledge of how these different components interact is still rudimentary. We generated a high-resolution time series of gene expression profiles from a single Arabidopsis thaliana leaf during infection by the necrotrophic fungal pathogen Botrytis cinerea. Approximately one-third of the Arabidopsis genome is differentially expressed during the first 48 h after infection, with the majority of changes in gene expression occurring before significant lesion development. We used computational tools to obtain a detailed chronology of the defense response against B. cinerea, highlighting the times at which signaling and metabolic processes change, and identify transcription factor families operating at different times after infection. Motif enrichment and network inference predicted regulatory interactions, and testing of one such prediction identified a role for TGA3 in defense against necrotrophic pathogens. These data provide an unprecedented level of detail about transcriptional changes during a defense response and are suited to systems biology analyses to generate predictive models of the gene regulatory networks mediating the Arabidopsis response to B. cinerea.

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Section: B Cinerea Infection Dampens Clock Gene Oscillationsmentioning

confidence: 55%

Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis

et al. 2012

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“…4E). This cyclical accumulation of salicylates may underlie the enhanced resistance of Arabidopsis to biotrophic bacteria when infection occurs in the early morning as opposed to the evening (16).…”

Section: Clock Coentrainment Increases Plant Resistance and Decreasesmentioning

confidence: 99%

Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior

Goodspeed

Chehab

Min-Venditti

et al. 2012

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

281

317

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Diverse life forms have evolved internal clocks enabling them to monitor time and thereby anticipate the daily environmental changes caused by Earth's rotation. The plant circadian clock regulates expression of about one-third of the Arabidopsis genome, yet the physiological relevance of this regulation is not fully understood. Here we show that the circadian clock, acting with hormone signals, provides selective advantage to plants through anticipation of and enhanced defense against herbivory. We found that cabbage loopers (Trichoplusia ni) display rhythmic feeding behavior that is sustained under constant conditions, and plants entrained in light/dark cycles coincident with the entrainment of the T. ni suffer only moderate tissue loss due to herbivory. In contrast, plants entrained out-of-phase relative to the insects are significantly more susceptible to attack. The in-phase entrainment advantage is lost in plants with arrhythmic clocks or deficient in jasmonate hormone; thus, both the circadian clock and jasmonates are required. Circadian jasmonate accumulation occurs in a phase pattern consistent with preparation for the onset of peak circadian insect feeding behavior, providing evidence for the underlying mechanism of clock-enhanced herbivory resistance. Furthermore, we find that salicylate, a hormone involved in biotrophic defense that often acts antagonistically to jasmonates, accumulates in opposite phase to jasmonates. Our results demonstrate that the plant circadian clock provides a strong physiological advantage by performing a critical role in Arabidopsis defense.circadian rhythm | diurnal rhythm | plant-herbivore interaction | jasmonic acid | salicylic acid I n the battle between plant host and herbivore, plants appear to be disadvantaged due to their relative immobility because once herbivorous insects attack, plants cannot escape by relocating. However, it is well-documented that plants can detect attack by insect herbivores and, in response, activate defense responses (1). These defense responses include accumulation of proteins and compounds that are toxic to and/or act to deter feeding of herbivores, thereby reducing herbivore performance and increasing plant resistance. Jasmonate hormones are critical for plant herbivore defense (1-3) and for the regulation of both herbivore and wound-responsive gene expression (4).Remarkably, many genes regulated in expression by wounding also have strong circadian regulation. Over 40% of genes whose expression is induced by wounding have peak circadian expression at subjective dusk, and over 80% of genes down-regulated by wounding have peak expression at subjective dawn (5). However, it remained to be determined whether this circadian regulation of wound-inducible genes enables plants to anticipate herbivore attack through a cyclical activation of defense response. Here we demonstrate that Arabidopsis plants that are entrained such that their subjective day is in-phase with Trichoplusia ni subjective day have increased resistance to herbivory. In contrast,...

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“…Over evolutionary time, organisms have adapted to environmental fluctuations by an internal rep- 35 resentation of time-endogenous biological clocks-that perpetuate biological rhythms even when en-36 vironmental conditions are kept constant. These rhythms are characteristically innate, evidenced by 37 particularly tricky.…”

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confidence: 99%

“…Although rhythms in immunity are observed across a broad array of taxa, including plants [35,36] which is highlighted by the local circadian clock of macrophages [46], and the feedback between immu-138 nity and molecular, cellular, and behavioral rhythms. The emerging picture is that the immune system 139 is an active component of integrated whole-body circadian rhythms in animals [50] and plants [35,36] Interspecific influence of parasites on one another's rhythm, to our knowledge, has only been described it has already been documented for other systems (e.g., in bioluminescent squid light organ symbionts 234 and in mammalian gut microbiota) [4,91].…”

mentioning

confidence: 99%

“…The emerging picture is that the immune system 139 is an active component of integrated whole-body circadian rhythms in animals [50] and plants [35,36] Interspecific influence of parasites on one another's rhythm, to our knowledge, has only been described it has already been documented for other systems (e.g., in bioluminescent squid light organ symbionts 234 and in mammalian gut microbiota) [4,91].…”

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confidence: 99%

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The influence of biological rhythms on host–parasite interactions

Martinez

Helm

2015

Trends in Ecology & Evolution

108

101

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6Biological rhythms-from circadian control of cellular processes to annual cycles in life history-are 7 a main structural element of biology. Biological rhythms are considered adaptive because they allow 8 organisms to partition activities to cope with, and take advantage of, predictable fluctuations in 9 environmental conditions. A flourishing area of immunology is uncovering rhythms in the immune 10 system of animals, including humans. Given the temporal structure of immunity, and rhythms in 11 parasite activity and disease incidence, we propose that the intersection of Chronobiology, Disease 12Ecology and Evolutionary Biology holds the key to understanding host-parasite interactions. We 13 review host-parasite interactions while explicitly considering biological rhythms, and propose that 14(1) rhythms influence within-host infection dynamics and transmission between hosts, (2) rhythms 15 might account for diel and annual periodicity in host-parasite systems, and (3) rhythms can lead to 16 a host-parasite arms race in the temporal domain. Interactions between hosts and parasites (i.e., microparasites and macroparasites) are embedded within 77 environmental rhythms ( Figure 1A). In addition to the environment, host immunity imposes selective 78 pressure on parasites, whilst parasite-driven morbidity and mortality reduces host fitness. These multiple 79 selective forces make optimal timing of allocation of limited resources to survival and reproduction 80

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Timing of plant immune responses by a central circadian regulator

Cited by 393 publications

References 27 publications

Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis

Arabidopsis Defense against Botrytis cinerea: Chronology and Regulation Deciphered by High-Resolution Temporal Transcriptomic Analysis

Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior

The influence of biological rhythms on host–parasite interactions

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