Gene expression evolution in pattern-triggered immunity within<i>Arabidopsis thaliana</i>and across Brassicaceae species

Winkelmüller, Thomas M.; Entila, Frederickson; Anver, Shajahan; Piasecka, Anna; Song, Baoxing; Dahms, Eik; Sakakibara, Hitoshi; Gan, Xiangchao; Kułak, Karolina; Sawikowska, Aneta; Krajewski, Paweł; Tsiantis, Miltos; Garrido‐Oter, Ruben; Fukushima, Kenji; Schulze‐Lefert, Paul; Laurent, Stefan; Bednarek, Paweł; Tsuda, Kazuhiko

doi:10.1093/plcell/koab073

Cited by 37 publications

(28 citation statements)

References 102 publications

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“…Photoperiod stress is a relatively new form of abiotic stress and not much is known about similarities with other stresses. We therefore compared the transcriptomic profile of plants in response to photoperiod stress with those in response to other biotic ( Truman et al, 2007 ; Winkelmüller et al, 2021 ) and abiotic stresses, including a shift to blue light (BL), drought stress, heat stress, cold stress, salt stress, ozone treatment, fluctuating light and high light stress ( Lee et al, 2005 ; Tosti et al, 2006 ; Kleine et al, 2007 ; Truman et al, 2007 ; Huang et al, 2008 , 2019 ; Larkindale and Vierling, 2008 ; Ding et al, 2014 ; Schneider et al, 2019 ; Figure 5 and Supplementary Data 7 ). In addition, we compared our dataset with the transcriptomic profile of circadian clock-regulated genes ( Covington et al, 2008 ) as a previous study found a link between photoperiod stress and the circadian clock ( Nitschke et al, 2016 ).…”

Section: Resultsmentioning

confidence: 99%

Photoperiod Stress in Arabidopsis thaliana Induces a Transcriptional Response Resembling That of Pathogen Infection

et al. 2022

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Plants are exposed to regular diurnal rhythms of light and dark. Changes in the photoperiod by the prolongation of the light period cause photoperiod stress in short day-adapted Arabidopsis thaliana. Here, we report on the transcriptional response to photoperiod stress of wild-type A. thaliana and photoperiod stress-sensitive cytokinin signaling and clock mutants and identify a core set of photoperiod stress-responsive genes. Photoperiod stress caused altered expression of numerous reactive oxygen species (ROS)-related genes. Photoperiod stress-sensitive mutants displayed similar, but stronger transcriptomic changes than wild-type plants. The alterations showed a strong overlap with those occurring in response to ozone stress, pathogen attack and flagellin peptide (flg22)-induced PAMP triggered immunity (PTI), which have in common the induction of an apoplastic oxidative burst. Interestingly, photoperiod stress triggers transcriptional changes in jasmonic acid (JA) and salicylic acid (SA) biosynthesis and signaling and results in increased JA, SA and camalexin levels. These responses are typically observed after pathogen infections. Consequently, photoperiod stress increased the resistance of Arabidopsis plants to a subsequent infection by Pseudomonas syringae pv. tomato DC3000. In summary, we show that photoperiod stress causes transcriptional reprogramming resembling plant pathogen defense responses and induces systemic acquired resistance (SAR) in the absence of a pathogen.

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Section: Resultsmentioning

confidence: 99%

Photoperiod Stress in Arabidopsis thaliana Induces a Transcriptional Response Resembling That of Pathogen Infection

et al. 2022

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“…Previous studies have applied single or dual omics to uncover the molecular mechanisms involved in plant–pathogen interactions (Bassal et al ., 2020 ; Bjornson et al ., 2021 ; Chen et al ., 2018 ; Jeon et al ., 2020 ; Lovelace et al ., 2018 ; Nobori et al ., 2018 , 2020 ; Winkelmüller et al ., 2021 ). In this study, we performed a multi‐omics analysis consisting of five omics datasets including metabolome, transcriptome, proteome, ubiquitome and acetylome to systematically elucidate PTI triggered by two different PAMPs in rice.…”

Section: Discussionmentioning

confidence: 99%

“…Like in Arabidopsis , similar PTI‐mediated defence occurs in rice against fungal and bacterial infection, such as ROS production, callose deposition, MAPK signalling cascade activation and the hormone signalling pathways activation (Liu et al ., 2013 , 2014 ; Yang et al ., 2013 ). Up to now, some single or combined omics studies, including transcriptomic, proteomics and metabolomics, have been reported to investigate the effects of plant responses to invading pathogens or challenged by different PAMPs (Bassal et al ., 2020 ; Bjornson et al ., 2021 ; Chen et al ., 2018 ; Jeon et al ., 2020 ; Lovelace et al ., 2018 ; Nobori et al ., 2018 ; Winkelmüller et al ., 2021 ). However, an integrative study of multi‐omics data is still lacking.…”

Section: Introductionmentioning

confidence: 99%

Multilayer regulatory landscape during pattern‐triggered immunity in rice

Tang

Liu

et al. 2021

Plant Biotechnology Journal

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Upon fungal and bacterial pathogen attack, plants launch pattern-triggered immunity (PTI) by recognizing pathogen-associated molecular patterns (PAMPs) to defend against pathogens. Although PTI-mediated response has been widely studied, a systematic understanding of the reprogrammed cellular processes during PTI by multi-omics analysis is lacking. In this study, we generated metabolome, transcriptome, proteome, ubiquitome and acetylome data to investigate rice (Oryza sativa) PTI responses to two PAMPs, the fungi-derived chitin and the bacteriaderived flg22. Integrative multi-omics analysis uncovered convergence and divergence of rice responses to these PAMPs at multiple regulatory layers. Rice responded to chitin and flg22 in a similar manner at the transcriptome and proteome levels, but distinct at the metabolome level. We found that this was probably due to post-translational regulation including ubiquitination and acetylation, which reshaped gene expression by modulating enzymatic activities, and possibly led to distinct metabolite profiles. We constructed regulatory atlas of metabolic pathways, including the defence-related phenylpropanoid and flavonoid biosynthesis and linoleic acid derivative metabolism. The multi-level regulatory network generated in this study sets the foundation for in-depth mechanistic dissection of PTI in rice and potentially in other related poaceous crop species.

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“…Fortunately, the available genome information can be used to identify the starch metabolism genes in Brassica crops ( http://brassicadb.cn/ ). The relevant genomic distribution, structure, and duplication of these core genes as well as the syntenic analysis of B. rapa (AA genome), Brassica nigra (BB genome), and Brassica oleracea (CC genome) are important to reveal the commonalities of Brassica crops susceptible to P. brassicae [ 32 ].…”

Section: Introductionmentioning

confidence: 99%

Starch content changes and metabolism-related gene regulation of Chinese cabbage synergistically induced by Plasmodiophora brassicae infection

Choi

Wang

et al. 2022

Horticulture Research

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Clubroot is one of the major diseases adversely affecting Chinese cabbage (Brassica rapa) yield and quality. To precisely characterize the Plasmodiophora brassicae infection on Chinese cabbage, we developed a dual fluorescent staining method for simultaneously examining the pathogen, cell structures, and starch grains. The number of starch (amylopectin) grains increased in B. rapa roots infected by P. brassicae, especially from 14 to 21 days after inoculation. Therefore, the expression levels of 38 core starch metabolism genes were investigated by quantitative real-time PCR. Most genes related to starch synthesis were up-regulated at seven days after the P. brassicae inoculation, whereas the expression levels of the starch degradation-related genes increased at 14 days after the inoculation. Then genes encoding the core enzymes involved in starch metabolism were investigated by assessing their chromosomal distributions, structures, duplication events, and synteny among Brassica species. Genome comparisons indicated that 38 non-redundant genes belonging to six core gene families related to starch metabolism are highly conserved among Arabidopsis thaliana, B. rapa, Brassica nigra, and Brassica oleracea. Genome sequencing projects have revealed that P. brassicae obtained host nutrients by manipulating plant metabolism. Starch may serve as a carbon source for P. brassicae colonization as indicated by the histological observation and transcriptomic analysis. Results of this study may elucidate the evolution and expression of core starch metabolism genes and provide researchers with novel insights into the pathogenesis of clubroot in B. rapa.

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Gene expression evolution in pattern-triggered immunity withinArabidopsis thalianaand across Brassicaceae species

Cited by 37 publications

References 102 publications

Photoperiod Stress in Arabidopsis thaliana Induces a Transcriptional Response Resembling That of Pathogen Infection

Photoperiod Stress in Arabidopsis thaliana Induces a Transcriptional Response Resembling That of Pathogen Infection

Multilayer regulatory landscape during pattern‐triggered immunity in rice

Starch content changes and metabolism-related gene regulation of Chinese cabbage synergistically induced by Plasmodiophora brassicae infection

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