Linking mitochondrial and chloroplast retrograde signalling in plants

Wang, Yan; Selinski, Jennifer; Mao, Chunli; Zhu, Yanqiao; Berkowitz, Oliver; Whelan, James

doi:10.1098/rstb.2019.0410

Cited by 69 publications

(71 citation statements)

References 129 publications

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“…ROS are produced in several plant subcellular compartments such as mitochondria, peroxisomes and chloroplasts as well as in the ER and nuclei (Wang et al, 2020; Waszczak et al, 2018). ROS accumulation in mitochondria and in chloroplasts can occur both during basal metabolism, including respiration and photosynthesis respectively, and in response to stress stimuli (Gollan, Tikkanen, & Aro, 2015; Wang et al, 2020; Waszczak et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

The intracellular ROS accumulation in elicitor‐induced immunity requires the multiple organelle‐targeted Arabidopsis NPK1‐related protein kinases

Marti¹,

Savatin²,

Gigli-Bisceglia³

et al. 2021

Plant Cell & Environment

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Recognition at the plasma membrane of danger signals (elicitors) belonging to the classes of the microbe/pathogen‐ and damage‐associated molecular patterns is a key event in pathogen sensing by plants and is associated with a rapid activation of immune responses. Different cellular compartments, including plasma membrane, chloroplasts, nuclei and mitochondria, are involved in the immune cellular program. However, how pathogen sensing is transmitted throughout the cell remains largely to be uncovered. Arabidopsis NPK1‐related Proteins (ANPs) are mitogen‐activated protein kinase kinase kinases previously shown to have a role in immunity. In this article, we studied the in vivo intracellular dynamics of ANP1‐ and ANP3‐GFP fusions and found that under basal physiological conditions both proteins are present in the cytosol, while ANP3 is also localized in mitochondria. After elicitor perception, both proteins are present also in the plastids and nuclei, revealing a localization pattern that is so far unique. The N‐terminal region of the protein kinases is responsible for their localization in mitochondria and plastids. Moreover, we found that the localization of ANPs coincides with the sites of elicitor‐induced ROS accumulation and that plants lacking ANP function do not accumulate intracellular ROS.

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Section: Discussionmentioning

confidence: 99%

The intracellular ROS accumulation in elicitor‐induced immunity requires the multiple organelle‐targeted Arabidopsis NPK1‐related protein kinases

Marti¹,

Savatin²,

Gigli-Bisceglia³

et al. 2021

Plant Cell & Environment

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“…ROS are also involved in retrograde signalling from mitochondria (see below). Since both organelles operate simultaneously within the same cell, one needs to ask how specificity in this signalling is achieved [100]. In energy metabolism, a royalsocietypublishing.org/journal/rstb Phil.…”

Section: (B) Operational Signalling From Plastidsmentioning

confidence: 99%

“…In fact, many regulators of plant MRR have been implicated in chloroplast retrograde signalling, including ABI4, WRKY40 and CDKE1 [47,[157][158][159], although recent evidence has ruled out a role for ABI4 in chloroplast biogenic signalling [160]. This interaction between plant mitochondrial and chloroplast retrograde signalling has been explored in detail in a review in this issue [100]. The ANAC017-induced genes are thought to help plants cope with oxidative stresses originating from the chloroplast, for instance during inhibition with methyl viologen [148,151].…”

Section: Retrograde Signalling From Mitochondria In Autotrophsmentioning

confidence: 99%

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

Pfannschmidt

Terry

Aken

et al. 2020

Phil. Trans. R. Soc. B

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Endosymbiotic organelles of eukaryotic cells, the plastids, including chloroplasts and mitochondria, are highly integrated into cellular signalling networks. In both heterotrophic and autotrophic organisms, plastids and/or mitochondria require extensive organelle-to-nucleus communication in order to establish a coordinated expression of their own genomes with the nuclear genome, which encodes the majority of the components of these organelles. This goal is achieved by the use of a variety of signals that inform the cell nucleus about the number and developmental status of the organelles and their reaction to changing external environments. Such signals have been identified in both photosynthetic and non-photosynthetic eukaryotes (known as retrograde signalling and retrograde response, respectively) and, therefore, appear to be universal mechanisms acting in eukaryotes of all kingdoms. In particular, chloroplasts and mitochondria both harbour crucial redox reactions that are the basis of eukaryotic life and are, therefore, especially susceptible to stress from the environment, which they signal to the rest of the cell. These signals are crucial for cell survival, lifespan and environmental adjustment, and regulate quality control and targeted degradation of dysfunctional organelles, metabolic adjustments, and developmental signalling, as well as induction of apoptosis. The functional similarities between retrograde signalling pathways in autotrophic and non-autotrophic organisms are striking, suggesting the existence of common principles in signalling mechanisms or similarities in their evolution. Here, we provide a survey for the newcomers to this field of research and discuss the importance of retrograde signalling in the context of eukaryotic evolution. Furthermore, we discuss commonalities and differences in retrograde signalling mechanisms and propose retrograde signalling as a general signalling mechanism in eukaryotic cells that will be also of interest for the specialist. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

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“…Numerous other signal transducers have been proposed including the calcium-sensing (CaS) protein, mitogen-activated protein kinase (MAPK) cascades, ROS, tetrapyrroles, intermediate products of the isoprenoid biosynthesis, and carotenoid derivatives ( Leister, 2017 ; Teardo et al, 2019 ; Wu et al, 2019 ; Jiang et al, 2020 ; Wang et al, 2020a ). Finally, this retrograde signaling modulates the expression of (a)biotic stress- and photosynthesis-related genes to adapt the photosynthetic machinery ( Wang et al, 2020b ). It is indeed generally thought that the activation of plant immune response induces plant growth reduction and a decrease in photosynthesis ( Bilgin et al, 2010 ; Baccelli et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Chloroplast Electron Chain, ROS Production, and Redox Homeostasis Are Modulated by COS-OGA Elicitation in Tomato (Solanum lycopersicum) Leaves

et al. 2020

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The stimulation of plant innate immunity by elicitors is an emerging technique in agriculture that contributes more and more to residue-free crop protection. Here, we used RNA-sequencing to study gene transcription in tomato leaves treated three times with the chitooligosaccharides–oligogalacturonides (COS-OGA) elicitor FytoSave® that induces plants to fend off against biotrophic pathogens. Results showed a clear upregulation of sequences that code for chloroplast proteins of the electron transport chain, especially Photosystem I (PSI) and ferredoxin. Concomitantly, stomatal conductance decreased by half, reduced nicotinamide adenine dinucleotide phosphate [NAD(P)H] content and reactive oxygen species production doubled, but fresh and dry weights were unaffected. Chlorophyll, β-carotene, violaxanthin, and neoxanthin contents decreased consistently upon repeated elicitations. Fluorescence measurements indicated a transient decrease of the effective PSII quantum yield and a non-photochemical quenching increase but only after the first spraying. Taken together, this suggests that plant defense induction by COS-OGA induces a long-term acclimation mechanism and increases the role of the electron transport chain of the chloroplast to supply electrons needed to mount defenses targeted to the apoplast without compromising biomass accumulation.

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Linking mitochondrial and chloroplast retrograde signalling in plants

Cited by 69 publications

References 129 publications

The intracellular ROS accumulation in elicitor‐induced immunity requires the multiple organelle‐targeted Arabidopsis NPK1‐related protein kinases

The intracellular ROS accumulation in elicitor‐induced immunity requires the multiple organelle‐targeted Arabidopsis NPK1‐related protein kinases

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

Chloroplast Electron Chain, ROS Production, and Redox Homeostasis Are Modulated by COS-OGA Elicitation in Tomato (Solanum lycopersicum) Leaves

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