It Started With a Kiss: Monitoring Organelle Interactions and Identifying Membrane Contact Site Components in Plants

Baillie, Alice L.; Falz, Anna-Lena; Müller-Schüssele, Stefanie J; Sparkes, Imogen

doi:10.3389/fpls.2020.00517

Cited by 21 publications

(23 citation statements)

References 77 publications

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“…A tentative hypothesis is that the attenuation of lipid transfer from the ER to plastids caused by TGD5 mutation alters the frequency and/or duration of membrane contact between both organelles, resulting in perturbed membrane remodeling of the plastid envelope and, ultimately, in uncontrolled stromule formation. This hypothesis should be tested experimentally using MCS‐monitoring techniques (Baillie, 2020) in tgd5 / suba1 in the future.…”

Section: Discussionmentioning

confidence: 99%

TGD5 is required for normal morphogenesis of non‐mesophyll plastids, but not mesophyll chloroplasts, in Arabidopsis

et al. 2021

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Stromules are dynamic membrane-bound tubular structures that emanate from plastids. Stromule formation is triggered in response to various stresses and during plant development, suggesting that stromules may have physiological and developmental roles in these processes. Despite the possible biological importance of stromules and their prevalence in green plants, their exact roles and formation mechanisms remain unclear. To explore these issues, we obtained Arabidopsis thaliana mutants with excess stromule formation in the leaf epidermis by microscopy-based screening. Here, we characterized one of these mutants, stromule biogenesis altered 1 (suba1). suba1 forms plastids with severely altered morphology in a variety of nonmesophyll tissues, such as leaf epidermis, hypocotyl epidermis, floral tissues, and pollen grains, but apparently normal leaf mesophyll chloroplasts. The suba1 mutation causes impaired chloroplast pigmentation and altered chloroplast ultrastructure in stomatal guard cells, as well as the aberrant accumulation of lipid droplets and their autophagic engulfment by the vacuole. The causal defective gene in suba1 is TRIGALAC-TOSYLDIACYLGLYCEROL5 (TGD5), which encodes a protein putatively involved in the endoplasmic reticulum (ER)-to-plastid lipid trafficking required for the ER pathway of thylakoid lipid assembly. These findings suggest that a non-mesophyll-specific mechanism maintains plastid morphology. The distinct mechanisms maintaining plastid morphology in mesophyll versus non-mesophyll plastids might be attributable, at least in part, to the differential contributions of the plastidial and ER pathways of lipid metabolism between mesophyll and non-mesophyll plastids.

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Section: Discussionmentioning

confidence: 99%

TGD5 is required for normal morphogenesis of non‐mesophyll plastids, but not mesophyll chloroplasts, in Arabidopsis

et al. 2021

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“…50 nm wide perinuclear space between the inner and outer nuclear membrane is contiguous with the ER lumen [36]. Chloroplasts, like many other organelles that form physical interactions with the ER, are tethered to the outer ER/nuclear membrane typically at 10-30 nm distance [37][38][39][40]. The ER outer membrane is thus frequently in very close association with the outer chloroplast envelope membrane [11,[41][42][43].…”

Section: Nature Of the Linkages-the Nuclear Envelopementioning

confidence: 99%

“…Notably, transorganellar complementation experiments elegantly demonstrated the existence of metabolic continuity in biosynthetic pathways, which span both organelles [44,45]. These tethers between chloroplasts and the ER are such that a 400 pN force applied with optical tweezers could not separate them [39,46,47]. Various biophysical, genetic, biochemical and microscopy methodologies have begun to provide a picture of the complexity of these interactions and the reader is referred to the comprehensive review on this subject by Baillie et al [39].…”

Section: Nature Of the Linkages-the Nuclear Envelopementioning

confidence: 99%

The Passage of H2O2 from Chloroplasts to Their Associated Nucleus during Retrograde Signalling: Reflections on the Role of the Nuclear Envelope

Breeze

Mullineaux

2022

Plants

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The response of chloroplasts to adverse environmental cues, principally increases in light intensity, stimulates chloroplast-to-nucleus retrograde signalling, which leads to the induction of immediate protective responses and longer-term acclimation. Hydrogen peroxide (H2O2), generated during photosynthesis, is proposed to both initiate and transduce a retrograde signal in response to photoinhibitory light intensities. Signalling specificity achieved by chloroplast-sourced H2O2 for signal transduction may be dependent upon the oft-observed close association of a proportion of these organelles with the nucleus. In this review, we consider more precisely the nature of the close association between a chloroplast appressed to the nucleus and the requirement for H2O2 to cross both the double membranes of the chloroplast and nuclear envelopes. Of particular relevance is that the endoplasmic reticulum (ER) has close physical contact with chloroplasts and is contiguous with the nuclear envelope. Therefore, the perinuclear space, which transducing H2O2 molecules would have to cross, may have an oxidising environment the same as the ER lumen. Based on studies in animal cells, the ER lumen may be a significant source of H2O2 in plant cells arising from the oxidative folding of proteins. If this is the case, then there is potential for the ER lumen/perinuclear space to be an important location to modify chloroplast-to-nucleus H2O2 signal transduction and thereby introduce modulation of it by additional different environmental cues. These would include for example, heat stress and pathogen infection, which induce the unfolded protein response characterised by an increased H2O2 level in the ER lumen.

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“…MCS foster physical interactions and the exchange of molecules between organelles without the need of membrane fusion events. The transient connections are established through tethering proteins, connecting the membranes of interacting organelles and allowing for direct exchange of lipids, cellular signals (e.g., Ca 2+ , reactive oxygen species [ROS], etc) and/or other molecules (Baillie et al, 2020;Prinz et al, 2020;Rossini et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

“…It is well recognised that MCS can form between nearly all organelles (Eisenberg-Bord et al, 2016;Valm et al, 2017;Shai et al, 2018;Baillie et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

SLDP and LIPA mediate lipid droplet-plasma membrane tethering in Arabidopsis thaliana

Krawczyk

Sun

Doner

et al. 2022

Preprint

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Membrane contact sites (MCS) are inter-organellar connections that allow for the direct exchange of molecules, such as lipids or Ca2+ between organelles, but can also serve to tether organelles at specific locations within cells. Here we identified and characterised three proteins that form a lipid droplet (LD)-plasma membrane (PM) tethering complex in plant cells, namely LD-localised SEED LD PROTEIN (SLDP) 1 and 2 and PM-localised LD-PLASMA MEMBRANE ADAPTOR (LIPA). Using proteomics and different protein-protein interaction assays, we show that both SLDPs associate with LIPA. Disruption of either SLDP1 and 2 expression, or that of LIPA, leads to an aberrant clustering of LDs in Arabidopsis seedlings. Ectopic co-expression of one of the SLDPs with LIPA on the other hand is sufficient to reconstitute LD-PM tethering in Nicotiana tabacum pollen tubes, a cell type characterised by dynamically moving LDs in the cytosolic streaming. Further, confocal laser scanning microscopy revealed both SLDP2.1 and LIPA to be enriched at LD-PM contact sites in seedlings. These and other results suggest that SLDP and LIPA interact to form a tethering complex that anchors a subset of LDs to the PM during post-germinative seedling growth in Arabidopsis thaliana.

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It Started With a Kiss: Monitoring Organelle Interactions and Identifying Membrane Contact Site Components in Plants

Cited by 21 publications

References 77 publications

TGD5 is required for normal morphogenesis of non‐mesophyll plastids, but not mesophyll chloroplasts, in Arabidopsis

TGD5 is required for normal morphogenesis of non‐mesophyll plastids, but not mesophyll chloroplasts, in Arabidopsis

The Passage of H2O2 from Chloroplasts to Their Associated Nucleus during Retrograde Signalling: Reflections on the Role of the Nuclear Envelope

SLDP and LIPA mediate lipid droplet-plasma membrane tethering in Arabidopsis thaliana

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