OXR2 Increases Plant Defense against a Hemibiotrophic Pathogen via the Salicylic Acid Pathway

Mencia, Regina; Céccoli, Gabriel; Fabro, Georgina; Torti, Pablo; Colombatti, Francisco; Ludwig‐Müller, Jutta; Alvarez, María Elena; Welchen, Elina

doi:10.1104/pp.19.01351

Cited by 23 publications

(24 citation statements)

References 122 publications

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“…Plant mitochondria have even been observed to accumulate around the cellular site of pathogen infection (Fuchs et al, 2016), where they displayed pathogen-induced redox imbalances. Resistance to pathogen infection has been associated with several mitochondrial proteins, including SDH1 (Gleason et al, 2011), Pre-sequence translocase-associated protein import motor (PAM16) (Huang et al, 2013), Outer Membrane 66 (OM66) (Zhang et al, 2014) and Oxidation Resistance 2 (OXR2) (Mencia et al, 2020). Although the precise mechanisms are not well understood, in several cases the resistance has been associated with ROS production and the plant hormone salicylic acid.…”

Section: Pathogen Responsementioning

confidence: 99%

“…One hypothesis is that the plant ETC is inhibited by pathogen-induced salicylic acid for instance at Complex II (Norman et al, 2004) and that this results in increased ROS production (Belt et al, 2017). Conversely, many mutants with altered expression of mitochondrial proteins contain changed salicylic acid levels, indicating interplay between mitochondrial function, ROS and salicylic acid (Adamowicz-Skrzypkowska et al, 2020;Mencia et al, 2020;Zhang et al, 2014). The AOX pathway has been associated with pathogen defenses, for instance by repressing a mitochondrial ROS burst after infection with Pseudomonas syringae pv.…”

Section: Pathogen Responsementioning

confidence: 99%

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Plant mitochondria – past, present and future

2021

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The study of plant mitochondria started in earnest around 1950 with the first isolations of mitochondria from animal and plant tissues. The first 35 years were spent establishing the basic properties of plant mitochondria and plant respiration using biochemical and physiological approaches. A number of unique properties (compared to mammalian mitochondria) were observed: (i) the ability to oxidize malate, glycine and cytosolic NAD (P)H at high rates; (ii) the partial insensitivity to rotenone, which turned out to be due to the presence of a second NADH dehydrogenase on the inner surface of the inner mitochondrial membrane in addition to the classical Complex I NADH dehydrogenase; and (iii) the partial insensitivity to cyanide, which turned out to be due to an alternative oxidase, which is also located on the inner surface of the inner mitochondrial membrane, in addition to the classical Complex IV, cytochrome oxidase. With the appearance of molecular biology methods around 1985, followed by genomics, further unique properties were discovered: (iv) plant mitochondrial DNA (mtDNA) is 10-600 times larger than the mammalian mtDNA, yet it only contains approximately 50% more genes; (v) plant mtDNA has kept the standard genetic code, and it has a low divergence rate with respect to point mutations, but a high recombinatorial activity; (vi) mitochondrial mRNA maturation includes a uniquely complex set of activities for processing, splicing and editing (at hundreds of sites); (vii) recombination in mtDNA creates novel reading frames that can produce male sterility; and (viii) plant mitochondria have a large proteome with 2000-3000 different proteins containing many unique proteins such as 200-300 pentatricopeptide repeat proteins. We describe the present and fairly detailed picture of the structure and function of plant mitochondria and how the unique properties make their metabolism more flexible allowing them to be involved in many diverse processes in the plant cell, such as photosynthesis, photorespiration, CAM and C4 metabolism, heat production, temperature control, stress resistance mechanisms, programmed cell death and genomic evolution. However, it is still a challenge to understand how the regulation of metabolism and mtDNA expression works at the cellular level and how retrograde signaling from the mitochondria coordinates all those processes.

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Section: Pathogen Responsementioning

confidence: 99%

Section: Pathogen Responsementioning

confidence: 99%

Plant mitochondria – past, present and future

2021

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“…This decrease in weight cannot only be observed after the SA treatments or elevated constitutive SA levels in plants, but also after the treatments with analogs for the SA-induced defense, such as benzothiadiazole (BTH) [37], since the SA and analogs are also in the crossroads between defense and growth [38]. Recently, a gene was identified from A. thaliana that encodes a mitochondrial protein with as yet an unknown function [39,40]. Overexpression of this OXR2 gene resulted in a phenotype with constitutively activated SA defense response in A. thaliana that caused the plant to be more resistant to Pseudomonas syringae infection [40].…”

Section: Introductionmentioning

confidence: 99%

A Novel Target (Oxidation Resistant 2) in Arabidopsis thaliana to Reduce Clubroot Disease Symptoms via the Salicylic Acid Pathway without Growth Penalties

et al. 2021

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The clubroot disease (Plasmodiophora brassicae) is one of the most damaging diseases worldwide among brassica crops. Its control often relies on resistant cultivars, since the manipulation of the disease hormones, such as salicylic acid (SA) alters plant growth negatively. Alternatively, the SA pathway can be increased by the addition of beneficial microorganisms for biocontrol. However, this potential has not been exhaustively used. In this study, a recently characterized protein Oxidation Resistant 2 (OXR2) from Arabidopsis thaliana is shown to increase the constitutive pathway of SA defense without decreasing plant growth. Plants overexpressing AtOXR2 (OXR2-OE) show strongly reduced clubroot symptoms with improved plant growth performance, in comparison to wild type plants during the course of infection. Consequently, oxr2 mutants are more susceptible to clubroot disease. P. brassicae itself was reduced in these galls as determined by quantitative real-time PCR. Furthermore, we provide evidence for the transcriptional downregulation of the gene encoding a SA-methyltransferase from the pathogen in OXR2-OE plants that could contribute to the phenotype.

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“…Many pieces of evidence also exist connecting mitochondrial proteins to resistance against pathogen infection and biotic stress, and on the role of mitochondria in modifying salicylic acid (SA) levels or responses (Colombatti et al ., 2014; Belt et al ., 2017; Mencia et al ., 2020). SA is a main player in the build‐up of the systemic acquired resistance observed in plants after infection with biotrophic pathogens.…”

Section: Long‐distance Signallingmentioning

confidence: 99%

Breaking boundaries: exploring short‐ and long‐distance mitochondrial signalling in plants

Welchen

González

2021

New Phytologist

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Communication of mitochondria with other cell compartments is essential for the coordination of cellular functions. Mitochondria send retrograde signals through metabolites, redox changes, direct organelle contacts and protein trafficking. Accumulating evidence indicates that, in animal systems, changes in mitochondrial function also trigger responses in other, either neighbouring or distantly located cells. Although not clearly established, there are indications that this type of communication may also be operative in plants. Grafting experiments suggested that the translocation of entire mitochondria or submitochondrial vesicles between neighbouring cells is possible in plants, as already documented in animals. Changes in mitochondrial function also regulate cell-to-cell communication via plasmodesmata and may be transmitted over long distances through plant hormones acting as mitokines to relay mitochondrial signals to distant tissues. Long-distance movement of transcripts encoding mitochondrial proteins involved in crucial aspects of metabolism and retrograde signalling was also described. Finally, changes in mitochondrial reactive species (ROS) production may affect the "ROS wave" that triggers systemic acquired acclimation throughout the plant. In this review, we summarize available evidence suggesting that mitochondria establish sophisticated communications not only within the cell but also with neighbouring cells and distant tissues to coordinate plant growth and stress responses in a cell non-autonomous manner.

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OXR2 Increases Plant Defense against a Hemibiotrophic Pathogen via the Salicylic Acid Pathway

Cited by 23 publications

References 122 publications

Plant mitochondria – past, present and future

Plant mitochondria – past, present and future

A Novel Target (Oxidation Resistant 2) in Arabidopsis thaliana to Reduce Clubroot Disease Symptoms via the Salicylic Acid Pathway without Growth Penalties

Breaking boundaries: exploring short‐ and long‐distance mitochondrial signalling in plants

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