50
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      The Permeability Transition in Plant Mitochondria: The Missing Link

      review-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The synthesis of ATP in mitochondria is dependent on a low permeability of the inner membrane. Nevertheless, mitochondria can undergo an increased permeability to solutes, named permeability transition (PT) that is mediated by a permeability transition pore (PTP). PTP opening requires matrix Ca 2+ and leads to mitochondrial swelling and release of intramembrane space proteins (e.g., cytochrome c). This feature has been initially observed in mammalian mitochondria and tentatively attributed to some components present either in the outer or inner membrane. Recent works on mammalian mitochondria point to mitochondrial ATP synthase dimers as physical basis for PT, a finding that has been substantiated in yeast and Drosophila mitochondria. In plant mitochondria, swelling and release of proteins have been linked to programmed cell death, but in isolated mitochondria PT has been observed in only a few cases and in plant cell cultures only indirect evidence is available. The possibility that mitochondrial ATP synthase dimers could function as PTP also in plants is discussed here on the basis of the current evidence. Finally, a hypothetical explanation for the origin of PTP is provided in the framework of molecular exaptation.

          Related collections

          Most cited references82

          • Record: found
          • Abstract: found
          • Article: not found

          The hydrogen hypothesis for the first eukaryote.

          A new hypothesis for the origin of eukaryotic cells is proposed, based on the comparative biochemistry of energy metabolism. Eukaryotes are suggested to have arisen through symbiotic association of an anaerobic, strictly hydrogen-dependent, strictly autotrophic archaebacterium (the host) with a eubacterium (the symbiont) that was able to respire, but generated molecular hydrogen as a waste product of anaerobic heterotrophic metabolism. The host's dependence upon molecular hydrogen produced by the symbiont is put forward as the selective principle that forged the common ancestor of eukaryotic cells.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae.

            We used electron cryotomography of mitochondrial membranes from wild-type and mutant Saccharomyces cerevisiae to investigate the structure and organization of ATP synthase dimers in situ. Subtomogram averaging of the dimers to 3.7 nm resolution revealed a V-shaped structure of twofold symmetry, with an angle of 86° between monomers. The central and peripheral stalks are well resolved. The monomers interact within the membrane at the base of the peripheral stalks. In wild-type mitochondria ATP synthase dimers are found in rows along the highly curved cristae ridges, and appear to be crucial for membrane morphology. Strains deficient in the dimer-specific subunits e and g or the first transmembrane helix of subunit 4 lack both dimers and lamellar cristae. Instead, cristae are either absent or balloon-shaped, with ATP synthase monomers distributed randomly in the membrane. Computer simulations indicate that isolated dimers induce a plastic deformation in the lipid bilayer, which is partially relieved by their side-by-side association. We propose that the assembly of ATP synthase dimer rows is driven by the reduction in the membrane elastic energy, rather than by direct protein contacts, and that the dimer rows enable the formation of highly curved ridges in mitochondrial cristae.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Macromolecular organization of ATP synthase and complex I in whole mitochondria.

              We used electron cryotomography to study the molecular arrangement of large respiratory chain complexes in mitochondria from bovine heart, potato, and three types of fungi. Long rows of ATP synthase dimers were observed in intact mitochondria and cristae membrane fragments of all species that were examined. The dimer rows were found exclusively on tightly curved cristae edges. The distance between dimers along the rows varied, but within the dimer the distance between F(1) heads was constant. The angle between monomers in the dimer was 70° or above. Complex I appeared as L-shaped densities in tomograms of reconstituted proteoliposomes. Similar densities were observed in flat membrane regions of mitochondrial membranes from all species except Saccharomyces cerevisiae and identified as complex I by quantum-dot labeling. The arrangement of respiratory chain proton pumps on flat cristae membranes and ATP synthase dimer rows along cristae edges was conserved in all species investigated. We propose that the supramolecular organization of respiratory chain complexes as proton sources and ATP synthase rows as proton sinks in the mitochondrial cristae ensures optimal conditions for efficient ATP synthesis.
                Bookmark

                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                15 December 2015
                2015
                : 6
                : 1120
                Affiliations
                [1]Plant Biology Unit, Department of Agricultural and Environmental Sciences, University of Udine Udine, Italy
                Author notes

                Edited by: Ildikò Szabò, University of Padova, Italy

                Reviewed by: Hao Peng, Washington State University, USA; Paolo Pinton, University of Ferrara, Italy

                *Correspondence: Marco Zancani, marco.zancani@ 123456uniud.it

                This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2015.01120
                4678196
                26697057
                cb5c9d00-cb43-4485-9397-0c92b6d21db7
                Copyright © 2015 Zancani, Casolo, Petrussa, Peresson, Patui, Bertolini, De Col, Braidot, Boscutti and Vianello.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 30 September 2015
                : 26 November 2015
                Page count
                Figures: 1, Tables: 1, Equations: 0, References: 100, Pages: 8, Words: 0
                Funding
                Funded by: Italian Ministry of Education
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                permeability transition,plant mitochondria,atp synthase,exaptation,environmental stress

                Comments

                Comment on this article