Guanosine tetraphosphate modulates salicylic acid signalling and the resistance of <i>Arabidopsis thaliana</i> to <i>Turnip mosaic virus</i>

Abdelkefi, Hela; Sugliani, Matteo; Ke, Hang; Harchouni, Seddik; Soubigou‐Taconnat, Ludivine; Citerne, Sylvie; Mouille, Grégory; Fakhfakh, H.; Robaglia, Christophe; Field, Ben

doi:10.1111/mpp.12548

Cited by 42 publications

(57 citation statements)

References 57 publications

(81 reference statements)

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“…PtRSH4a had the greatest number of ESTs indicating higher expression levels, and PtRSH4a EST abundance increased in response to a number of stresses including high levels of 2E, 4E decadienal, a volatile oxylipin associated with diatom stress signalling (Vardi et al , 2006)(Table S2). This may suggest that diatom RSH genes are involved in defence responses, as previously observed for plant RSH (van der Biezen et al , 2000; Givens et al , 2004; Kim et al , 2009; Abdelkefi et al , 2018). Furthermore, recent transcriptome experiments show that PtRSHl and PtRSH4b are induced rapidly after the onset of nitrogen starvation and in response to incubation in darkness for eight hours (Matthijs et al , 2016; Matthijs et al , 2017).…”

Section: Resultssupporting

confidence: 68%

Golden magic: RSH enzymes for (p)ppGpp metabolism in the diatom Phaeodactylum tricornutum

Avilán

Puppo

Villain

et al. 2018

Preprint

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The nucleotides guanosine tetraphosphate and pentaphosphate (together known as (p)ppGpp or magic spot) are produced in plant plastids from GDP/GTP and ATP by RelA-SpoT homologue (RSH) enzymes. In the model plant Arabidopsis (p)ppGpp regulates chloroplast transcription and translation to affect growth, and is also implicated in acclimation to stress. However, little is known about (p)ppGpp metabolism or its evolution in other photosynthetic eukaryotes. Here we studied (p)ppGpp metabolism in the golden-coloured marine diatom Phaeodactylum tricornutum. We identified three expressed RSH genes in the P. tricornutum genome, and determined the enzymatic activity of the corresponding enzymes by heterologous expression in bacteria. We showed that two P. tricornutum RSH are (p)ppGpp synthetases, despite substitution of a residue within the active site believed critical for activity, and that the third RSH is a bifunctional (p)ppGpp synthetase and hydrolase, the first of its kind demonstrated in a photosynthetic eukaryote. A broad phylogenetic analysis then showed that diatom RSH belong to novel algal RSH clades. Together our work significantly expands the horizons of (p)ppGpp signalling in the photosynthetic eukaryotes by demonstrating an unexpected functional, structural and evolutionary diversity in RSH enzymes from organisms with plastids derived from red algae.HighlightWe discover RSH enzymes for (p)ppGpp metabolism in the diatom Phaeodactylum tricornutum and show that they have surprising functional and structural features, and belong to novel red-plastid lineage RSH clades.

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Section: Resultssupporting

confidence: 68%

Golden magic: RSH enzymes for (p)ppGpp metabolism in the diatom Phaeodactylum tricornutum

Avilán

Puppo

Villain

et al. 2018

Preprint

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“…Interestingly, HCPro, the RNA silencing suppressor of TuMV, interacts with AtCA1 (the homologue of SABP3 (SA‐binding protein 3)) to compromise the SA pathway and facilitate viral infection (Poque et al , ). Recently, it was reported that high levels of guanosine pentaphosphate or tetraphosphate ((p)ppGpp) accumulation increased susceptibility to TuMV and reduced SA content, whereas plants with lower (p)ppGpp levels were more resistant to TuMV and had increased SA content, indicating a role for the SA pathway in defence against TuMV (Abdelkefi et al , ). Our finding that transgenic NahG N. benthamiana was susceptible to TuMV, while exogenous SA enhanced N. benthamiana resistance to TuMV, demonstrates that SA participates in defence against TuMV in N. benthamiana (Fig.…”

Section: Discussionmentioning

confidence: 99%

NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana

Wang

Han

Peng

et al. 2019

Molecular Plant Pathology

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Summary AGD2‐LIKE DEFENCE RESPONSE PROTEIN 1 (ALD1) triggers plant defence against bacterial and fungal pathogens by regulating the salicylic acid (SA) pathway and an unknown SA‐independent pathway. We now show that Nicotiana benthamiana ALD1 is involved in defence against a virus and that the ethylene pathway also participates in ALD1 ‐mediated resistance. NbALD1 was up‐regulated in plants infected with turnip mosaic virus (TuMV). Silencing of NbALD1 facilitated TuMV infection, while overexpression of NbALD1 or exogenous application of pipecolic acid (Pip), the downstream product of ALD1 , enhanced resistance to TuMV. The SA content was lower in NbALD1 ‐silenced plants and higher where NbALD1 was overexpressed or following Pip treatments. SA mediated resistance to TuMV and was required for NbALD1 ‐mediated resistance. However, on NahG plants (in which SA cannot accumulate), Pip treatment still alleviated susceptibility to TuMV, further demonstrating the presence of an SA‐independent resistance pathway. The ethylene precursor, 1‐aminocyclopropanecarboxylic acid (ACC), accumulated in NbALD1 ‐silenced plants but was reduced in plants overexpressing NbALD1 or treated with Pip. Silencing of ACS1 , a key gene in the ethylene pathway, alleviated the susceptibility of NbALD1 ‐silenced plants to TuMV, while exogenous application of ACC compromised the resistance of Pip‐treated or NbALD1 transgenic plants. The results indicate that NbALD1 mediates resistance to TuMV by positively regulating the resistant SA pathway and negatively regulating the susceptible ethylene pathway.

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“…Clearly, chloroplast infection by TuMV leads to physiological changes in infected plants, which may interfere with important processes such as photosynthesis. In this context, Abdelkefi et al (2018) determinate that (p)ppGpp was involved in modulation of plant immunity against TuMV using transcriptomics tools (microarray analysis). Study demonstrated that (p)ppGpp accumulation was associated with increased susceptibility to TuMV and reduced levels of the defence hormone SA.…”

Section: Potyvirus Genusmentioning

confidence: 99%

Transcriptomics of plant–virus interactions: a review

Zanardo

Souza

Alves

2019

Theor. Exp. Plant Physiol.

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Posing as one of the major threats for a wide range of plant species, viruses are responsible for huge losses in crop production around the world. The design of new efficient molecular strategies aiming plant resistance requires a holistic view of the complex mechanisms underlying the plant-virus interactions, as well as the discovery of all virus-associated functional components involved in disease. Most of plant viruses present RNA genomes, which aspects of structural diversity and function are frequently difficult to be described using classical molecular biology approaches. As a promising alternative, the advancing field of transcriptomics has shaded light on the understanding of a plethora of plant-virus interactions, in model and crop plants. The advent of RNA sequencing (RNA-seq) and its several variants, such as sRNA-seq and Degradome-seq, has brought the study of plant-virus interactions in a new age. Previously unknown players acting during virus infections are now structurally and functionally described. In this review, we focus on the advances of plant-virus interactions study promoted by the expanding field of transcriptomics. We present an overview of state-ofart of the plant-virus interactions study, regarding important aspects of plant physiology and virology, following by a succinct description of the main transcriptomic approaches used in this field. A detailed description of the use of transcriptomic approaches for some of main plant virus genres during host-interactions is also presented. Finally, we bring concluding remarks discussing the importance of transcriptomics in the study of plant viral diseases, and the future prospects of new approaches in transcriptomics with potential of use in plant-virus interaction studies. Keywords Functional genomics Á Plant physiology Á Plant virology Á Gene expression Á RNA-seq Larissa Goulart Zanardo and Gilza Barcelos de Souza have contributed equally to this manuscript.

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Guanosine tetraphosphate modulates salicylic acid signalling and the resistance of Arabidopsis thaliana to Turnip mosaic virus

Cited by 42 publications

References 57 publications

Golden magic: RSH enzymes for (p)ppGpp metabolism in the diatom Phaeodactylum tricornutum

Golden magic: RSH enzymes for (p)ppGpp metabolism in the diatom Phaeodactylum tricornutum

NbALD1 mediates resistance to turnip mosaic virus by regulating the accumulation of salicylic acid and the ethylene pathway in Nicotiana benthamiana

Transcriptomics of plant–virus interactions: a review

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