Spatial chloroplast-to-nucleus signalling involving plastid–nuclear complexes and stromules

Mullineaux, Phil; Expósito-Rodríguez, Marino; Laissue, Pierre Philippe; Smirnoff, Nicholas; Park, Eunsook

doi:10.1098/rstb.2019.0405

Cited by 62 publications

(50 citation statements)

References 64 publications

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“…In conjunction with the tomato nuclear and plastid genome sequences [ 56 , 71 ], evaluation of changes to the tomato chloroplast proteome, and its sub-organellar fractions, in response to cues during development, as well as abiotic and biotic stress are now possible. Future confirmation of CIP localization using fluorescent reporter fusion proteins will determine if these proteins are imported and localized in more than one organelle or if their co-isolation with chloroplasts solely reflects the known tight apposition of ER, peroxisomes, mitochondria, and nuclei with chloroplasts [ 103 , 111 , 112 , 117 ].…”

Section: Discussionmentioning

confidence: 99%

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Methodology: an optimized, high-yield tomato leaf chloroplast isolation and stroma extraction protocol for proteomics analyses and identification of chloroplast co-localizing proteins

2020

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Background Chloroplasts are critical organelles that perceive and convey metabolic and stress signals to different cellular components, while remaining the seat of photosynthesis and a metabolic factory. The proteomes of intact leaves, chloroplasts, and suborganellar fractions of plastids have been evaluated in the model plant Arabidopsis, however fewer studies have characterized the proteomes of plastids in crops. Tomato (Solanum lycopersicum) is an important world-wide crop and a model system for the study of wounding, herbivory and fruit ripening. While significant advances have been made in understanding proteome and metabolome changes in fruit ripening, far less is known about the tomato chloroplast proteome or its subcompartments. Results With the long-term goal of understanding chloroplast proteome dynamics in response to stress, we describe a high-yielding method to isolate intact tomato chloroplasts and stromal proteins for proteomic studies. The parameters that limit tomato chloroplast yields were identified and revised to increase yields. Compared to published data, our optimized method increased chloroplast yields by 6.7- and 4.3-fold relative to published spinach and Arabidopsis leaf protocols, respectively; furthermore, tomato stromal protein yields were up to 79-fold higher than Arabidopsis stromal proteins yields. We provide immunoblot evidence for the purity of the stromal proteome isolated using our enhanced methods. In addition, we leverage our nanoliquid chromatography tandem mass spectrometry (nanoLC–MS/MS) data to assess the quality of our stromal proteome. Using strict criteria, proteins detected by 1 peptide spectral match, by one peptide, or were sporadically detected were designated as low-level contaminating proteins. A set of 254 proteins that reproducibly co-isolated with the tomato chloroplast stroma were identified. The subcellular localization, frequency of detection, normalized spectral abundance, and functions of the co-isolating proteins are discussed. Conclusions Our optimized method for chloroplast isolation increased the yields of tomato chloroplasts eightfold enabling the proteomics analysis of the chloroplast stromal proteome. The set of 254 proteins that co-isolate with the chloroplast stroma provides opportunities for developing a better understanding of the extensive and dynamic interactions of chloroplasts with other organelles. These co-isolating proteins also have the potential for expanding our knowledge of proteins that are co-localized in multiple subcellular organelles.

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Section: Discussionmentioning

confidence: 99%

“…There is substantial evidence that nuclei and plastids interact [ 117 ]. Chloroplasts can be found directly appressed to nuclear envelopes and connected to nuclei via stromules.…”

Section: Methodsmentioning

confidence: 99%

Methodology: an optimized, high-yield tomato leaf chloroplast isolation and stroma extraction protocol for proteomics analyses and identification of chloroplast co-localizing proteins

2020

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“…Thus, organization of chloroplasts during infection is typified by perinuclear chloroplast localization and the CHUP1-dependent extension of stromules toward the nucleus, each of which provide a physical basis for retrograde signalling (Erickson et al, 2018;Mullineaux et al, 2020). Indeed, perinuclear positioning of chloroplasts in immunity appears generic, being reported during viral infections (Fig.…”

Section: Cellular Reorganization During Infection Stromules Andmentioning

confidence: 91%

“…For example, HR in Arabidopsis inoculated with PstavrRpm1 is enhanced by increased light intensity and associated with disruption of the PSII light harvesting complex, decreased F v / F m (Fig. 1f) and accumulation of the Chl catabolite phaeophorbide, a potent photosensitizer that generates 1 O 2 (Mur et al ., 2010). Indeed, F v / F m provides a powerful readout to accurately capture and quantify the timing of specific R protein activation, before visible symptoms, as illustrated for the RPM1–AvrRpm1 and RPS4–AvrRPS4 interactions (Fig.…”

Section: Cros In Immunity and Insights From Disruption Of Chloroplastmentioning

confidence: 99%

Chloroplast immunity illuminated

Littlejohn¹,

Breen

Smirnoff

et al. 2020

New Phytologist

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Summary The chloroplast has recently emerged as pivotal to co‐ordinating plant defence responses and as a target of plant pathogens. Beyond its central position in oxygenic photosynthesis and primary metabolism – key targets in the complex virulence strategies of diverse pathogens – the chloroplast integrates, decodes and responds to environmental signals. The capacity of chloroplasts to synthesize phytohormones and a diverse range of secondary metabolites, combined with retrograde and reactive oxygen signalling, provides exquisite flexibility to both perceive and respond to biotic stresses. These processes also represent a plethora of opportunities for pathogens to evolve strategies to directly or indirectly target ‘chloroplast immunity’. This review covers the contribution of the chloroplast to pathogen associated molecular pattern and effector triggered immunity as well as systemic acquired immunity. We address phytohormone modulation of immunity and surmise how chloroplast‐derived reactive oxygen species underpin chloroplast immunity through indirect evidence inferred from genetic modification of core chloroplast components and direct pathogen targeting of the chloroplast. We assess the impact of transcriptional reprogramming of nuclear‐encoded chloroplast genes during disease and defence and look at future research challenges.

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“…This close proximity provides the opportunity for direct transfer of ROS into the nucleus without passage through the cytosol. Details of this novel pathway are discussed in this issue [99].…”

Section: (B) Operational Signalling From Plastidsmentioning

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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Spatial chloroplast-to-nucleus signalling involving plastid–nuclear complexes and stromules

Cited by 62 publications

References 64 publications

Methodology: an optimized, high-yield tomato leaf chloroplast isolation and stroma extraction protocol for proteomics analyses and identification of chloroplast co-localizing proteins

Methodology: an optimized, high-yield tomato leaf chloroplast isolation and stroma extraction protocol for proteomics analyses and identification of chloroplast co-localizing proteins

Chloroplast immunity illuminated

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

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