IntEResting structures: formation and applications of organized smooth endoplasmic reticulum in plant cells

Sandor, Andras; Fricker, Mark D.; Kriechbaumer, Verena

doi:10.1104/pp.20.00719

Cited by 8 publications

(19 citation statements)

References 107 publications

(152 reference statements)

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“…In canonical secretory pathways, secretory proteins are believed to be translocated from the ER, followed by vesicle trafficking to the Golgi apparatus and ultimately transported to the PM or the extracellular matrix (Nagashima et al., 2020; Sun et al., 2021). Thus, ER plays an essential role in secretory protein biosynthesis and post‐translational modifications (Chen et al., 2020; Sandor et al., 2021). Generally, the nascent LTPs possess an ER‐targeting SP and tend to be secreted into the apoplastic space for function (Boutrot et al., 2008; Cai et al., 2011; Edstam et al., 2011).…”

Section: Discussionmentioning

confidence: 99%

Secretory lipid transfer protein OsLTPL94 acts as a target of EAT1 and is required for rice pollen wall development

et al. 2021

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SUMMARY The plant pollen wall protects the male gametophyte from various biotic and abiotic stresses. The formation of a unique pollen wall structure and elaborate exine pattern is a well‐organized process, which needs coordination between reproductive cells and the neighboring somatic cells. However, molecular mechanisms underlying this process remain largely unknown. Here, we report a rice male‐sterile mutant (l94) that exhibits defective pollen exine patterning and abnormal tapetal cell development. MutMap and knockout analyses demonstrated that the causal gene encodes a type‐G non‐specific lipid transfer protein (OsLTPL94). Histological and cellular analyses established that OsLTPL94 is strongly expressed in the developing microspores and tapetal cells, and its protein is secreted to the plasma membrane. The l94 mutation impeded the secretory ability of OsLTPL94 protein. Further in vivo and in vitro investigations supported the hypothesis that ETERNAL TAPETUM 1 (EAT1), a basic helix‐loop‐helix transcription factor (bHLH TF), activated OsLTPL94 expression through direct binding to the E‐box motif of the OsLTPL94 promoter, which was supported by the positive correlation between the expression of EAT1 and OsLTPL94 in two independent eat1 mutants. Our findings suggest that the secretory OsLTPL94 plays a key role in the coordinated development of tapetum and microspores with the regulation of EAT1.

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Section: Discussionmentioning

confidence: 99%

Secretory lipid transfer protein OsLTPL94 acts as a target of EAT1 and is required for rice pollen wall development

et al. 2021

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“…Morphologically, the C22Y compartments are also similar to some of the larger OSER structures (Ferrero et al ., 2015; Sandor et al ., 2021), and the fibrous 22Y structures resemble elongated lamellae, another typical OSER phenotype (Sandor et al ., 2021). Notably, 22Y compartments are morphologically identical to the OSER structures described induced by the nuc mutation of the MVP1 protein in A. thaliana (Jancowski et al ., 2014).…”

Section: Discussionmentioning

confidence: 99%

Characterisation of organised smooth endoplasmic reticulum suggests a route towards synthetic compartmentalisation

Sandor

Samalova

Brandizzí

et al. 2022

Preprint

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Engineering of subcellular compartmentalisation is one of synthetic biology's key challenges. Among different approaches, de novo construction of a synthetic compartment is the most coveted but also most difficult option. Restructuring the endoplasmic reticulum (ER), via the introduction of recombinant oligomerising ER-membrane resident proteins, is an alternative starting point for building a new compartment. The presence of such proteins leads to a massive expansion of the ER and the formation of organised smooth endoplasmic reticulum (OSER), a large membranous compartment. However, OSER is poorly characterised and our understanding of its effect on the underlying biology of the plant is limited. Here we characterise a range of OSER compartments and show how the structure of the inducing polyprotein constructs affect the final compartment morphology, with the cytosolic-facing antiparallel oligomerisation domain demonstrated to be an essential component to trigger OSER formation. We show that while OSER retains a connection to the ER, a diffusional barrier exists to both the ER and the cytosol. Using high-resolution quantitative image analysis, we also show that the presence of this large compartment does not disrupt the rest of the ER network. Moreover, transgenic Arabidopsis constitutively expressing the compartment-forming polyproteins grew and developed normally. These properties collectively suggest that OSER could be developed as a plant synthetic biology tool for compartmentalisation, combining the benefits of several existing strategies. Only a single protein construct is necessary to induce its formation, and the compartment retains a delimiting membrane and a diffusional barrier to the rest of the cell.

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“…Initially analyzed in plant cells (termed "membrane zippering"; Mullen et al, 2001), and later coined OSER (for "organized smooth endoplasmic reticulum") based on the studies in yeast and animal cells (Snapp et al, 2003), the formation of ER subdomains is a dynamic event, mainly governed by the principles of self-organization (Borgese et al, 2006). While recognition of the phenomenon dates back to EM studies in the 1980s, the formation of OSER structures applies to all eukaryotes (reviewed in Sandor et al, 2021). One open question still is whether specific ER proteins are needed for creating/maintaining (native) OSER structures.…”

Section: Figurementioning

confidence: 99%

“…structures are formed (Sandor et al, 2021). Thus, the spatial organization of the membrane-bound G6PD5 proteoforms at the ER seems to be governed by features of both, the transmembrane regions and the globular catalytic domains.…”

Section: Figurementioning

confidence: 99%

Alternative splicing of Arabidopsis G6PD5 recruits NADPH-producing OPPP reactions to the endoplasmic reticulum

et al. 2022

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Glucose-6-phosphate dehydrogenase is the rate-limiting enzyme of the oxidative pentose-phosphate pathway (OPPP). The OPPP mainly provides NADPH and sugar-phosphate building blocks for anabolic pathways and is present in all eukaryotes. In plant cells, the irreversible part of the OPPP is found in several compartments. Among the isoforms catalyzing the first OPPP step in Arabidopsis, G6PD1 to G6PD4 target plastids (with G6PD1 being also directed to peroxisomes), whereas G6PD5 and G6PD6 operate in the cytosol. We noticed that alternative splice forms G6PD5.4 and G6PD5.5 encode N-terminally extended proteoforms. Compared to G6PD5.1, RT-PCR signals differed and fluorescent reporter fusions expressed in Arabidopsis protoplasts accumulated in distinct intracellular sites. Co-expression with organelle-specific markers revealed that the G6PD5.4 and G6PD5.5 proteoforms label different subdomains of the endoplasmic reticulum (ER), and analysis of C-terminal roGFP fusions showed that their catalytic domains face the cytosol. In g6pd5-1 g6pd6-2 mutant protoplasts lacking cytosolic G6PDH activity, the ER-bound proteoforms were both active and thus able to form homomers. Among the Arabidopsis 6-phosphogluconolactonases (catalyzing the second OPPP step), we noticed that isoform PGL2 carries a C-terminal CaaX motif that may be prenylated for membrane attachment. Reporter-PGL2 fusions co-localized with G6PD5.4 in ER subdomains, which was abolished by Cys-to-Ser exchange in the 256CSIL motif. Among the Arabidopsis 6-phosphogluconate dehydrogenases (catalyzing the third OPPP step), S-acylated peptides were detected for all three isoforms in a recent palmitoylome, with dual cytosolic/peroxisomal PGD2 displaying three sites. Co-expression of GFP-PGD2 diminished crowding of OFP-G6PD5.4 at the ER, independent of PGL2's presence. Upon pull-down of GFP-G6PD5.4, not only unlabeled PGD2 and PGL2 were enriched, but also enzymes that depend on NADPH provision at the ER, indicative of physical interaction with the OPPP enzymes. When membrane-bound G6PD5.5 and 5.4 variants were co-expressed with KCR1 (ketoacyl-CoA reductase, involved in fatty acid elongation), ATR1 (NADPH:cytochrome-P450 oxidoreductase), or pulled C4H/CYP73A5 (cinnamate 4-hydroxylase) as indirectly (via ATR) NADPH-dependent cytochrome P450 enzyme, co-localization in ER subdomains was observed. Thus, alternative splicing of G6PD5 can direct the NADPH-producing OPPP reactions to the cytosolic face of the ER, where they may operate as membrane-bound metabolon to support several important biosynthetic pathways of plant cells.

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IntEResting structures: formation and applications of organized smooth endoplasmic reticulum in plant cells

Abstract: Novel findings in organised smooth endoplasmic reticulum uncover mechanisms of formation and potential applications for this structure.

Cited by 8 publications

References 107 publications

Secretory lipid transfer protein OsLTPL94 acts as a target of EAT1 and is required for rice pollen wall development

Secretory lipid transfer protein OsLTPL94 acts as a target of EAT1 and is required for rice pollen wall development

Characterisation of organised smooth endoplasmic reticulum suggests a route towards synthetic compartmentalisation

Alternative splicing of Arabidopsis G6PD5 recruits NADPH-producing OPPP reactions to the endoplasmic reticulum

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