OEP40, a Regulated Glucose-permeable β-Barrel Solute Channel in the Chloroplast Outer Envelope Membrane

Abstract

Chloroplasts and mitochondria are unique endosymbiotic cellular organelles surrounded by two membranes. Essential metabolic networking between these compartments and their hosting cells requires the exchange of a large number of biochemical pathway intermediates in a directed and coordinated fashion across their inner and outer envelope membranes. Here, we describe the identification and functional characterization of a highly specific, regulated solute channel in the outer envelope of chloroplasts, named OEP40. Loss of OEP40 function in Arabidopsis thaliana results in early flowering under cold temperature. The reconstituted recombinant OEP40 protein forms a high conductance ␤-barrel ion channel with subconductant states in planar lipid bilayers. The OEP40 channel is slightly cation-selective P K؉ /P Cl؊ ≈ 4:1 and rectifying (ı ᠬ/ı ᠭ Х 2) with a slope conductance of Ḡ max Х 690 picosiemens. The OEP40 channel has a restriction zone diameter of Х1.4 nm and is permeable for glucose, glucose 1-phosphate and glucose 6-phosphate, but not for maltose. Moreover, channel properties are regulated by trehalose 6-phosphate, which cannot permeate. Altogether, our results indicate that OEP40 is a "glucose-gate" in the outer envelope membrane of chloroplasts, facilitating selective metabolite exchange between chloroplasts and the surrounding cell.The plant cell is highly compartmentalized, containing at least seven different types of organelles that are involved in metabolism and cellular maintenance. In many cases, metabolic pathways and other cellular processes are not confined to one organelle but require the cooperation of several of them, e.g. in protein secretion or photorespiration. Metabolic networking between compartments thus requires directed and coordinated exchange of biochemical pathway intermediates across organellar membranes (1). Chloroplasts and mitochondria are unique endosymbiotic cellular organelles, which like their prokaryotic ancestors are surrounded by two membranes. The inner membrane of both organelles is derived from the bacterial plasma membrane. Surprisingly, also the outer membrane largely originated from and still resembles the outer membrane of the Gram-negative-like bacterial endosymbiont (2). In the inner chloroplast envelope membrane (IE), 5 numerous metabolite transporter proteins were identified and characterized to large detail with respect to their physiological impact and molecular mechanisms (3). These transporters are hydrophobic, polytopic, and mainly ␣-helical membrane proteins facilitating the exchange of metabolic precursors, intermediates, and final products between plastids and the cytoplasm. In contrast, the characteristic channels of the outer membranes in bacteria, chloroplasts as well as mitochondria, span the membrane in the form of ␤-strands that are organized to form a barrel-like pore structure (4). Proteins sharing this three-dimensional arrangement were implied in a variety of functions, including protein import (5). In addition, solute pores like the voltage-dependen...

Mitochondrial Outer Membrane Channels: Emerging Diversity in Transport Processes

“…Supporting this view, a similar complexity of transport processes has been observed in the outer envelope membrane of plants plastids that are the other cell organelles of endosymbiotic origin. Members of the Omp85 family mediate protein transport and so far five solute channels with distinct substrate specificities have been identified in the plastid envelope membrane …”

“…Members of the Omp85 family mediate protein transport and so far five solute channels with distinct substrate specificities have been identified in the plastid envelope membrane. [45,102,103] Abbreviations Ayr1, acyl dihydroxyacetone phosphate reductase; ERMES, ER mitochondria encounter structure; Mdm10, mitochondrial distribution and morphology protein 10; MIA, mitochondrial intermembrane space import and assembly; MIM complex, mitochondrial import; MPP, mitochondrial processing peptidase; SAM complex, sorting and assembly machinery; TIM23 complex, presequence translocase; TIM22 complex, carrier translocase; TOM complex, translocase of the outer mitochondrial membrane; OMC, outer membrane channel; OXA, oxidase assembly; VDAC, voltage-dependent anion channel.…”

BANFF:bending of bilayer membranes byamphiphilic α-helices isnecessary forform andfunction of organelles

“…Proteins sharing this 3-D arrangement were implied in a variety of functions, including protein import (Bredemeier et al 2007). In addition, solute pores like the voltage dependent anion channel (VDAC) in mitochondria (Checchetto and Szabo 2018;Colombini 2012) or the outer envelope proteins OEP21, OEP24, OEP37 and OEP40 (Bölter et al 1999;Goetze et al 2006;Harsman et al 2016;Pohlmeyer et al 1998) in chloroplasts are essential parts of the outer membrane permeom of these organelles (Breuers et al 2011;Duy et al 2007).…”

Targeting carbon for crop yield and drought resilience

“…However, this mechanism is different in sink and source tissues, potentially because of differences in the make‐up of SnRK1 complex in source and sink tissues, developmental regulation of trehalose pathway gene expression with a far stronger expression in sink tissues, and likely additional targets of T6P. Interestingly, in this latter regard, T6P regulates a glucose‐permeable solute channel in the chloroplast outer envelope membrane . Effects on flowering could also involve other receptors; however, SnRK1 has been shown to affect flowering …”

“…Interestingly, in this latter regard, T6P regulates a glucose-permeable solute channel in the chloroplast outer envelope membrane. 104 Effects on flowering could also involve wileyonlinelibrary.com/jsfa other receptors 105 ; however, SnRK1 has been shown to affect flowering. 102,106 There is considerable evidence therefore that T6P regulates metabolic homeostasis in the light of sucrose supply and that this also regulates sucrose homeostasis itself.…”