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1. Loss of inner-envelope K+/H+ exchangers impairs plastid rRNA maturation and gene expression

   https://doi.org/10.1093/plcell/koab123  

   DeTar, Rachael Ann ; Barahimipour, Rouhollah ; Manavski, Nikolay ; Schwenkert, Serena ; Höhner, Ricarda ; Bölter, Bettina ; Inaba, Takehito ; Meurer, Jörg ; Zoschke, Reimo ; Kunz, Hans-Henning ( May 2021 , The Plant Cell)

   Abstract The inner-envelope K+ EFFLUX ANTIPORTERS (KEA) 1 and 2 are critical for chloroplast development, ion homeostasis, and photosynthesis. However, the mechanisms by which changes in ion flux across the envelope affect organelle biogenesis remained elusive. Chloroplast development requires intricate coordination between the nuclear genome and the plastome. Many mutants compromised in plastid gene expression (PGE) display a virescent phenotype, that is delayed greening. The phenotypic appearance of Arabidopsis thaliana kea1 kea2 double mutants fulfills this criterion, yet a link to PGE has not been explored. Here, we show that a simultaneous loss of KEA1 and KEA2 results in maturation defects of the plastid ribosomal RNAs. This may be caused by secondary structure changes of rRNA transcripts and concomitant reduced binding of RNA-processing proteins, which we documented in the presence of skewed ion homeostasis in kea1 kea2. Consequently, protein synthesis and steady-state levels of plastome-encoded proteins remain low in mutants. Disturbance in PGE and other signs of plastid malfunction activate GENOMES UNCOUPLED 1-dependent retrograde signaling in kea1 kea2, resulting in a dramatic downregulation of GOLDEN2-LIKE transcription factors to halt expression of photosynthesis-associated nuclear-encoded genes (PhANGs). PhANG suppression delays the development of fully photosynthesizing kea1 kea2 chloroplasts, probably to avoid progressingmore »photo-oxidative damage. Overall, our results reveal that KEA1/KEA2 function impacts plastid development via effects on RNA-metabolism and PGE.« less
2. Maize defective kernel5 is a bacterial TamB homologue required for chloroplast envelope biogenesis

   https://doi.org/10.1083/jcb.201807166  

   Zhang, Junya ; Wu, Shan ; Boehlein, Susan K. ; McCarty, Donald R. ; Song, Gaoyuan ; Walley, Justin W. ; Myers, Alan ; Settles, A. Mark ( August 2019 , Journal of Cell Biology)

   Chloroplasts are of prokaryotic origin with a double-membrane envelope separating plastid metabolism from the cytosol. Envelope membrane proteins integrate chloroplasts with the cell, but envelope biogenesis mechanisms remain elusive. We show that maize defective kernel5 (dek5) is critical for envelope biogenesis. Amyloplasts and chloroplasts are larger and reduced in number in dek5 with multiple ultrastructural defects. The DEK5 protein is homologous to rice SSG4, Arabidopsis thaliana EMB2410/TIC236, and Escherichia coli tamB. TamB functions in bacterial outer membrane biogenesis. DEK5 is localized to the envelope with a topology analogous to TamB. Increased levels of soluble sugars in dek5 developing endosperm and elevated osmotic pressure in mutant leaf cells suggest defective intracellular solute transport. Proteomics and antibody-based analyses show dek5 reduces levels of Toc75 and chloroplast envelope transporters. Moreover, dek5 chloroplasts reduce inorganic phosphate uptake with at least an 80% reduction relative to normal chloroplasts. These data suggest that DEK5 functions in plastid envelope biogenesis to enable transport of metabolites and proteins.
3. Sulfolipid density dictates the extent of carbon nanodot interaction with chloroplast membranes

   https://doi.org/10.1039/D2EN00158F  

   Kim, Kyoungtea ; Jeon, Su-Ji ; Hu, Peiguang ; Anastasia, Caroline M. ; Beimers, William F. ; Giraldo, Juan Pablo ; Pedersen, Joel A. ( January 2022 , Environmental Science: Nano)

   Mechanisms of nanomaterial delivery to plant chloroplasts have been explored to improve plant stress tolerance, promote photosynthesis, facilitate genetic engineering, and manufacture self-repairing biomaterials, fuels, and biopharmaceuticals. However, the molecular interactions of nanomaterials with chloroplast membranes are not well understood. In this study, we examine the interactions of an important set of chloroplast membrane lipids including sulfoquinovosyl diacylglycerols with carbon nanodots varying in functional group charge. To accomplish this objective, we constructed a novel model chloroplast membrane and interrogated the influence of carbon nanodot functional group charge, model chloroplast membrane composition, and ionic strength on the carbon nanodot-chloroplast membrane interactions using quartz crystal microbalance with dissipation monitoring. We further examined the interaction of carbon nanodots with native chloroplasts isolated from Arabidopsis thaliana using confocal laser-scanning microscopy. Our results indicate that carbon nanodot–chloroplast membrane interactions are dictated primarily by electrostatics. Despite being the least abundant lipids in chloroplast membranes, we find that the relative abundance of sulfoquinovosyl diacylglycerol in model membranes is a critical factor governing both the affinity and capacity of the membrane for positively charged carbon nanodots. Rates of carbon nanodot attachment to model chloroplast membranes varied with ionic strength in a manner consistent with electrical double layer compressionmore »on carbon nanodots. Our findings elucidate chemical interactions between nanomaterials and plant biosurfaces at the molecular level and potentially contribute to establishing structure–property–interaction relationships of sustainable nanomaterials with plant organelle membranes.« less
4. Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms

   https://doi.org/10.1093/plcell/koab021  

   Forsythe, Evan S ; Williams, Alissa M ; Sloan, Daniel B ( January 2021 , The Plant Cell)

   Abstract Nuclear and plastid (chloroplast) genomes experience different mutation rates, levels of selection, and transmission modes, yet key cellular functions depend on their coordinated interactions. Functionally related proteins often show correlated changes in rates of sequence evolution across a phylogeny (evolutionary rate covariation or ERC), offering a means to detect previously unidentified suites of coevolving and cofunctional genes. We performed phylogenomic analyses across angiosperm diversity, scanning the nuclear genome for genes that exhibit ERC with plastid genes. As expected, the strongest hits were highly enriched for genes encoding plastid-targeted proteins, providing evidence that cytonuclear interactions affect rates of molecular evolution at genome-wide scales. Many identified nuclear genes functioned in post-transcriptional regulation and the maintenance of protein homeostasis (proteostasis), including protein translation (in both the plastid and cytosol), import, quality control and turnover. We also identified nuclear genes that exhibit strong signatures of coevolution with the plastid genome, but their encoded proteins lack organellar-targeting annotations, making them candidates for having previously undescribed roles in plastids. In sum, our genome-wide analyses reveal that plastid-nuclear coevolution extends beyond the intimate molecular interactions within chloroplast enzyme complexes and may be driven by frequent rewiring of the machinery responsible for maintenance of plastid proteostasis inmore »angiosperms.« less
5. Light-induced displacement of PLASTID MOVEMENT IMPAIRED1 precedes light-dependent chloroplast movements

   https://doi.org/10.1093/plphys/kiac193  

   Dwyer, Matthew E. ; Hangarter, Roger P. ( April 2022 , Plant Physiology)

   Light-dependent chloroplast movements are an actin-dependent cellular response to changes in the light environment that help plants maximize photosynthetic potential and reduce photodamage. Over a dozen proteins are known to be required for normal chloroplast movements, but the molecular mechanisms regulating the transformation of light perception into chloroplast motility are not fully understood. Here, we show that in Arabidopsis (Arabidopsis thaliana) the actin-bundling plasma membrane-associated proteins THRUMIN1, PLASTID MOVEMENT IMPAIRED1 (PMI1), and KINESIN-LIKE PROTEIN FOR ACTIN-BASED CHLOROPLAST MOVEMENT1 (KAC1) interact through the 14-3-3 proteins KAPPA and OMEGA. We also show that the interaction of PMI1 with 14-3-3 KAPPA and OMEGA is regulated by blue light activation of the Phototropin2 photoreceptor. Live-cell confocal microscopy revealed light-induced dynamic changes in the cellular localizations of PMI1 and KAC1. In particular, PMI1 was relocated away from irradiated areas of the plasma membrane in less than a minute after blue light exposure, consistent with PMI1 playing a critical role in initiating light-dependent chloroplast movements. We present a modified conceptual model for high light-dependent chloroplast movements in which PMI1 acts as the mobile signal that initiates a coordinated sequence of changes in protein–protein and protein–plasma membrane interactions that initiate the chloroplast movement response and determinemore »where in the cell chloroplasts are able to anchor to the plasma membrane.

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