The Permeability Transition in Plant Mitochondria: The Missing Link
Identifieur interne : 000253 ( Pmc/Corpus ); précédent : 000252; suivant : 000254The Permeability Transition in Plant Mitochondria: The Missing Link
Auteurs : Marco Zancani ; Valentino Casolo ; Elisa Petrussa ; Carlo Peresson ; Sonia Patui ; Alberto Bertolini ; Valentina De Col ; Enrico Braidot ; Francesco Boscutti ; Angelo VianelloSource :
- Frontiers in Plant Science [ 1664-462X ] ; 2015.
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 Ca2+ and leads to mitochondrial swelling and release of intramembrane space proteins (e.g., cytochrome
Url:
DOI: 10.3389/fpls.2015.01120
PubMed: 26697057
PubMed Central: 4678196
Links to Exploration step
PMC:4678196Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Permeability Transition in Plant Mitochondria: The Missing Link</title><author><name sortKey="Zancani, Marco" sort="Zancani, Marco" uniqKey="Zancani M" first="Marco" last="Zancani">Marco Zancani</name></author><author><name sortKey="Casolo, Valentino" sort="Casolo, Valentino" uniqKey="Casolo V" first="Valentino" last="Casolo">Valentino Casolo</name></author><author><name sortKey="Petrussa, Elisa" sort="Petrussa, Elisa" uniqKey="Petrussa E" first="Elisa" last="Petrussa">Elisa Petrussa</name></author><author><name sortKey="Peresson, Carlo" sort="Peresson, Carlo" uniqKey="Peresson C" first="Carlo" last="Peresson">Carlo Peresson</name></author><author><name sortKey="Patui, Sonia" sort="Patui, Sonia" uniqKey="Patui S" first="Sonia" last="Patui">Sonia Patui</name></author><author><name sortKey="Bertolini, Alberto" sort="Bertolini, Alberto" uniqKey="Bertolini A" first="Alberto" last="Bertolini">Alberto Bertolini</name></author><author><name sortKey="De Col, Valentina" sort="De Col, Valentina" uniqKey="De Col V" first="Valentina" last="De Col">Valentina De Col</name></author><author><name sortKey="Braidot, Enrico" sort="Braidot, Enrico" uniqKey="Braidot E" first="Enrico" last="Braidot">Enrico Braidot</name></author><author><name sortKey="Boscutti, Francesco" sort="Boscutti, Francesco" uniqKey="Boscutti F" first="Francesco" last="Boscutti">Francesco Boscutti</name></author><author><name sortKey="Vianello, Angelo" sort="Vianello, Angelo" uniqKey="Vianello A" first="Angelo" last="Vianello">Angelo Vianello</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26697057</idno><idno type="pmc">4678196</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4678196</idno><idno type="RBID">PMC:4678196</idno><idno type="doi">10.3389/fpls.2015.01120</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000253</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Permeability Transition in Plant Mitochondria: The Missing Link</title><author><name sortKey="Zancani, Marco" sort="Zancani, Marco" uniqKey="Zancani M" first="Marco" last="Zancani">Marco Zancani</name></author><author><name sortKey="Casolo, Valentino" sort="Casolo, Valentino" uniqKey="Casolo V" first="Valentino" last="Casolo">Valentino Casolo</name></author><author><name sortKey="Petrussa, Elisa" sort="Petrussa, Elisa" uniqKey="Petrussa E" first="Elisa" last="Petrussa">Elisa Petrussa</name></author><author><name sortKey="Peresson, Carlo" sort="Peresson, Carlo" uniqKey="Peresson C" first="Carlo" last="Peresson">Carlo Peresson</name></author><author><name sortKey="Patui, Sonia" sort="Patui, Sonia" uniqKey="Patui S" first="Sonia" last="Patui">Sonia Patui</name></author><author><name sortKey="Bertolini, Alberto" sort="Bertolini, Alberto" uniqKey="Bertolini A" first="Alberto" last="Bertolini">Alberto Bertolini</name></author><author><name sortKey="De Col, Valentina" sort="De Col, Valentina" uniqKey="De Col V" first="Valentina" last="De Col">Valentina De Col</name></author><author><name sortKey="Braidot, Enrico" sort="Braidot, Enrico" uniqKey="Braidot E" first="Enrico" last="Braidot">Enrico Braidot</name></author><author><name sortKey="Boscutti, Francesco" sort="Boscutti, Francesco" uniqKey="Boscutti F" first="Francesco" last="Boscutti">Francesco Boscutti</name></author><author><name sortKey="Vianello, Angelo" sort="Vianello, Angelo" uniqKey="Vianello A" first="Angelo" last="Vianello">Angelo Vianello</name></author></analytic><series><title level="j">Frontiers in Plant Science</title><idno type="eISSN">1664-462X</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>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<sup>2+</sup> and leads to mitochondrial swelling and release of intramembrane space proteins (e.g., cytochrome <italic>c</italic>). 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 <italic>Drosophila</italic> 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.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Akerman, K E" uniqKey="Akerman K">K. E. Akerman</name></author><author><name sortKey="Moore, A L" uniqKey="Moore A">A. L. Moore</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Alavian, K N" uniqKey="Alavian K">K. N. Alavian</name></author><author><name sortKey="Beutner, G" uniqKey="Beutner G">G. Beutner</name></author><author><name sortKey="Lazrove, E" uniqKey="Lazrove E">E. Lazrove</name></author><author><name sortKey="Sacchetti, S" uniqKey="Sacchetti S">S. Sacchetti</name></author><author><name sortKey="Park, H A" uniqKey="Park H">H.-A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id><journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id><journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id><journal-title-group><journal-title>Frontiers in Plant Science</journal-title></journal-title-group><issn pub-type="epub">1664-462X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26697057</article-id><article-id pub-id-type="pmc">4678196</article-id><article-id pub-id-type="doi">10.3389/fpls.2015.01120</article-id><article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject><subj-group><subject>Mini Review</subject></subj-group></subj-group></article-categories><title-group><article-title>The Permeability Transition in Plant Mitochondria: The Missing Link</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zancani</surname><given-names>Marco</given-names></name><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/222602/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Casolo</surname><given-names>Valentino</given-names></name><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/298424/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Petrussa</surname><given-names>Elisa</given-names></name></contrib><contrib contrib-type="author"><name><surname>Peresson</surname><given-names>Carlo</given-names></name></contrib><contrib contrib-type="author"><name><surname>Patui</surname><given-names>Sonia</given-names></name></contrib><contrib contrib-type="author"><name><surname>Bertolini</surname><given-names>Alberto</given-names></name></contrib><contrib contrib-type="author"><name><surname>De Col</surname><given-names>Valentina</given-names></name></contrib><contrib contrib-type="author"><name><surname>Braidot</surname><given-names>Enrico</given-names></name><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/298730/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Boscutti</surname><given-names>Francesco</given-names></name></contrib><contrib contrib-type="author"><name><surname>Vianello</surname><given-names>Angelo</given-names></name></contrib></contrib-group><aff id="aff1"><institution>Plant Biology Unit, Department of Agricultural and Environmental Sciences, University of Udine</institution><country>Udine, Italy</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Ildikò Szabò, University of Padova, Italy</italic></p></fn><fn fn-type="edited-by"><p>Reviewed by: <italic>Hao Peng, Washington State University, USA; Paolo Pinton, University of Ferrara, Italy</italic></p></fn><corresp id="fn001">*Correspondence: <italic>Marco Zancani, <email xlink:type="simple">marco.zancani@uniud.it</email></italic></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science</p></fn></author-notes><pub-date pub-type="epub"><day>15</day><month>12</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>6</volume><elocation-id>1120</elocation-id><history><date date-type="received"><day>30</day><month>9</month><year>2015</year></date><date date-type="accepted"><day>26</day><month>11</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015 Zancani, Casolo, Petrussa, Peresson, Patui, Bertolini, De Col, Braidot, Boscutti and Vianello.</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>Zancani, Casolo, Petrussa, Peresson, Patui, Bertolini, De Col, Braidot, Boscutti and Vianello</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>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.</license-p></license></permissions><abstract><p>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<sup>2+</sup> and leads to mitochondrial swelling and release of intramembrane space proteins (e.g., cytochrome <italic>c</italic>). 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 <italic>Drosophila</italic> 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.</p></abstract><kwd-group><kwd>permeability transition</kwd><kwd>plant mitochondria</kwd><kwd>ATP synthase</kwd><kwd>exaptation</kwd><kwd>environmental stress</kwd></kwd-group><funding-group><award-group><funding-source id="cn001">Italian Ministry of Education</funding-source></award-group></funding-group><counts><fig-count count="1"></fig-count><table-count count="1"></table-count><equation-count count="0"></equation-count><ref-count count="100"></ref-count><page-count count="8"></page-count><word-count count="0"></word-count></counts></article-meta></front><body><sec><title>The Permeability Transition</title><p>ATP synthesis in mitochondria occurs by a chemiosmotic coupling of substrate oxidation and phosphorylation (<xref rid="B67" ref-type="bibr">Mitchell, 1961</xref>). This explanation is based on the highly selective permeability of the inner mitochondrial membrane (IMM) and on utilization of protonmotive force by the F<sub>1</sub>F<sub>O</sub> ATP synthase (F-ATPase) for the synthesis of ATP. Nevertheless, a sudden increase in permeability of the IMM has been described in the 1950s (<xref rid="B73" ref-type="bibr">Raaflaub, 1953a</xref>,<xref rid="B74" ref-type="bibr">b</xref>) and characterized in the late 1970s (<xref rid="B40" ref-type="bibr">Haworth and Hunter, 1979</xref>; <xref rid="B43" ref-type="bibr">Hunter and Haworth, 1979a</xref>,<xref rid="B44" ref-type="bibr">b</xref>). Initially considered an artifact, later it has been named Permeability Transition (PT) and associated to a pore, the Permeability Transition Pore (PTP). The appreciation of its relevance has increased since it has been related to many diseases in mammals, including reperfusion injury of the heart and muscular dystrophy (<xref rid="B7" ref-type="bibr">Bernardi, 2013a</xref>). This mitochondrial PT requires matrix Ca<sup>2+</sup> and is favored by matrix P<sub>i</sub>, as well as benzodiazepine Bz-423 and thiol oxidants, while it can be inhibited by Mg<sup>2+</sup>, thiol reductants, ADP and ATP (<xref rid="B8" ref-type="bibr">Bernardi, 2013b</xref>). Cyclosporin A (CsA) acts as inhibitor of PT (<xref rid="B16" ref-type="bibr">Crompton et al., 1988</xref>) by binding with the peptidyl-prolyl isomerase Cyclophilin D (CyPD) (<xref rid="B37" ref-type="bibr">Halestrap and Davidson, 1990</xref>). The features of PTP (e.g., pore diameter of ∼2.8 nm and size exclusion of about 1500 Da) are consistent with those described for the Mitochondrial Mega-Channel (MMC), a high-conductance channel, which is considered to be its electrophysiological equivalent (<xref rid="B86" ref-type="bibr">Szabó and Zoratti, 1992</xref>).</p></sec><sec><title>The PT in Plants</title><p>The first evidence of a Ca<sup>2+</sup>-induced and CsA-delayed collapse of transmembrane electrical potential difference (ΔΨ) in pea stem mitochondria dates back to 1995 (<xref rid="B91" ref-type="bibr">Vianello et al., 1995</xref>). PT has been then observed in different plant species, although the features of this phenomenon cannot be summarized in a straightforward model (<bold>Table <xref ref-type="table" rid="T1">1</xref></bold>). Potato tuber mitochondria exhibit a typical Ca<sup>2+</sup>/P<sub>i</sub>-induced PT, inhibited (<xref rid="B4" ref-type="bibr">Arpagaus et al., 2002</xref>) or not (<xref rid="B30" ref-type="bibr">Fortes et al., 2001</xref>) by CsA. These mitochondria do not show any Ca<sup>2+</sup> uptake, suggesting an external effect of Ca<sup>2+</sup> on PT (<xref rid="B30" ref-type="bibr">Fortes et al., 2001</xref>), which is not consistent with the observations in mammals (<xref rid="B9" ref-type="bibr">Bernardi et al., 2015</xref>). The PT described in oat leaves (<xref rid="B17" ref-type="bibr">Curtis and Wolpert, 2002</xref>) and wheat roots (<xref rid="B93" ref-type="bibr">Virolainen et al., 2002</xref>) shows a Ca<sup>2+</sup>/P<sub>i</sub> -induced ΔΨ collapse and matrix swelling, which are CsA-insensitive. Calcium uptake by isolated plant mitochondria occurs spontaneously in wheat, but requires the addition of the Ca<sup>2+</sup>/H<sup>+</sup> ionophore A23187 in oat.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p>Characteristics of permeability transition (PT) in plant mitochondria.</p></caption><table frame="hsides" rules="groups" cellspacing="5" cellpadding="5"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Plant material</th><th valign="top" align="center" rowspan="1" colspan="1">Ca<sup>2+</sup> stimulation</th><th valign="top" align="center" rowspan="1" colspan="1">CsA inhibition</th><th valign="top" align="center" rowspan="1" colspan="1">Sucrose swelling</th><th valign="top" align="center" rowspan="1" colspan="1">Cytochrome <italic>c</italic> release</th><th valign="top" align="left" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Etiolated pea stem</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Not detected</td><td valign="top" align="left" rowspan="1" colspan="1"><xref rid="B91" ref-type="bibr">Vianello et al., 1995</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Potato tuber</td><td valign="top" align="left" rowspan="1" colspan="1">Yes (external)</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1"><xref rid="B30" ref-type="bibr">Fortes et al., 2001</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Potato tuber</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1"><xref rid="B4" ref-type="bibr">Arpagaus et al., 2002</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oat leaves</td><td valign="top" align="left" rowspan="1" colspan="1">Yes (with A23187)</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1"><xref rid="B17" ref-type="bibr">Curtis and Wolpert, 2002</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Wheat roots</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1"><xref rid="B93" ref-type="bibr">Virolainen et al., 2002</xref></td></tr></tbody></table></table-wrap><p>Indirect evidence of PT in plants has been also based on the CsA-induced inhibition of programmed cell death (PCD), reviewed by <xref rid="B92" ref-type="bibr">Vianello et al. (2007</xref>, <xref rid="B90" ref-type="bibr">2012</xref>). However, the prevention of PCD might depend on CsA binding to cytosolic Cyclophilin A (a ubiquitous enzyme) that drives enzymatic cascades (<xref rid="B61" ref-type="bibr">Lu et al., 2007</xref>), linked to oxidative stress (<xref rid="B69" ref-type="bibr">Nigro et al., 2013</xref>).</p></sec><sec><title>The Mitochondrial Ca<sup>2+</sup> Accumulation in Plants</title><p>The PT requires Ca<sup>2+</sup> accumulation into the mitochondrial matrix (i.e., matrix Ca<sup>2+</sup> is a permissive factor, although it may not be sufficient <italic>per se</italic>). Calcium transport in isolated plant mitochondria exhibits distinct features. The uptake could be mediated by a low-affinity electrophoretic P<sub>i</sub>-dependent symport, with low or no sensitivity to ruthenium red and lanthanides (<xref rid="B24" ref-type="bibr">Dieter and Marme, 1980</xref>; <xref rid="B1" ref-type="bibr">Akerman and Moore, 1983</xref>; <xref rid="B82" ref-type="bibr">Silva et al., 1992</xref>), but also by a uniport mechanism (<xref rid="B100" ref-type="bibr">Zottini and Zannoni, 1993</xref>). CsA inhibits mitochondrial Ca<sup>2+</sup> transport in <italic>Citrus</italic> (<xref rid="B23" ref-type="bibr">de Oliveira et al., 2007</xref>), suggesting its synergic effect with PT. A low concentration of matrix free Ca<sup>2+</sup> (∼100 nM) is maintained under steady state, where influx is balanced by an efflux through a yet speculative Na<sup>+</sup>-independent Ca<sup>2+</sup>/H<sup>+</sup> antiport mechanism (<xref rid="B70" ref-type="bibr">Nomura and Shiina, 2014</xref>). The influx of Ca<sup>2+</sup> in plant mitochondria is highly variable, depending on species and tissues, or might be even completely absent (<xref rid="B65" ref-type="bibr">Martins and Vercesi, 1985</xref>). <italic>In vivo</italic> Ca<sup>2+</sup> dynamics have been monitored by fluorescent probes targeted to plant mitochondria (<xref rid="B63" ref-type="bibr">Manzoor et al., 2012</xref>; <xref rid="B60" ref-type="bibr">Loro and Costa, 2013</xref>). Matrix Ca<sup>2+</sup> uptake can be induced by abiotic stresses such as heat, oxidative stress, or anoxia, and follows the cytosolic Ca<sup>2+</sup> pattern (<xref rid="B85" ref-type="bibr">Subbaiah et al., 1998</xref>; <xref rid="B58" ref-type="bibr">Logan and Knight, 2003</xref>; <xref rid="B78" ref-type="bibr">Schwarzländer et al., 2012</xref>; <xref rid="B76" ref-type="bibr">Rikhvanov et al., 2014</xref>).</p><p>Homologue genes of mammalian mitochondrial Ca<sup>2+</sup> uniporter (MCU) and its regulatory protein MICU1 have been found in plants (<xref rid="B10" ref-type="bibr">Bick et al., 2012</xref>; <xref rid="B84" ref-type="bibr">Stael et al., 2012</xref>; <xref rid="B76" ref-type="bibr">Rikhvanov et al., 2014</xref>). The MICU1 homologue in <italic>Arabidopsis</italic> (AtMICU) is a negative regulator of mitochondrial Ca<sup>2+</sup> uptake in root tips, providing strong evidence for the operation of a mitochondrial Ca<sup>2+</sup> uniporter in plants (<xref rid="B95" ref-type="bibr">Wagner et al., 2015</xref>).</p></sec><sec><title>The Involvement of PT/PCD in Plant Development and Stress Responses</title><p>The physiological role of mitochondrial PT in plants is often related to developmental processes (<xref rid="B75" ref-type="bibr">Reape et al., 2015</xref>) and mild environmental stresses, which involve also PCD in many cases. However, the mechanistic link between PT and PCD remains still speculative.</p><p>Permeability transition/programmed cell death are fundamental in the selection of damaged cells and in sculpturing new anatomical and morphological structures (<xref rid="B87" ref-type="bibr">Van Hautegem et al., 2015</xref>). Morphological modifications are also needed for adaptive responses to environment (e.g., climate changes) and, more in general, for fitness increase. In particular, <italic>Aponogeton madagascariensis</italic> forms lacunae on its leaves by executing PCD, which is inhibited by CsA, suggesting the involvement of PT (<xref rid="B59" ref-type="bibr">Lord et al., 2013</xref>). In aerenchyma formation, lack of oxygen induces stress characterized by mitochondrial PT, ATP depletion, and PCD induction (<xref rid="B96" ref-type="bibr">Yamauchi et al., 2013</xref>). Consistently, stressed pea plants show cytochrome <italic>c</italic> release, followed by DNA fragmentation (<xref rid="B77" ref-type="bibr">Sarkar and Gladish, 2012</xref>).</p><p>Programmed cell death is a common response in plants subjected to abiotic and biotic stresses, which may be linked to the sessile lifestyle, providing a survival strategy for the whole organism. Excess of UV-C stimulates reactive oxygen species (ROS) formation and collapse of ΔΨ in <italic>Arabidopsis</italic> mitochondria (<xref rid="B31" ref-type="bibr">Gao et al., 2008</xref>). The role of PT has also been described in case of extreme temperatures. In <italic>Arabidopsis</italic> protoplasts, heat stress induces mitochondrial swelling, and ΔΨ loss, but these damages are counteracted by a heat shock transcription factor (<xref rid="B99" ref-type="bibr">Zhang et al., 2009</xref>). Similarly, ROS and mild heat shock induce mitochondrial PT and the subsequent induction of cell death in <italic>Arabidopsis</italic> protoplasts, which are prevented by the superoxide dismutase analog TEMPOL, by the Ca<sup>2+</sup> channel-blocker lanthanum chloride, and by CsA (<xref rid="B79" ref-type="bibr">Scott and Logan, 2008</xref>). The role of mitochondria in PCD is confirmed in heat-stressed rice protoplasts, where mHSP70 overexpression maintains mitochondrial ΔΨ, partially inhibits cytochrome <italic>c</italic> release and suppresses PCD by lowering ROS formation (<xref rid="B72" ref-type="bibr">Qi et al., 2011</xref>). In wheat cells subjected to freezing, ROS-dependent PCD is associated to ΔΨ collapse and cytochrome <italic>c</italic> release (<xref rid="B62" ref-type="bibr">Lyubushkina et al., 2014</xref>). In salt-stressed tobacco protoplasts, PCD is triggered by ROS produced by mitochondria, through a process controlled by a CsA-sensitive PT (<xref rid="B56" ref-type="bibr">Lin et al., 2006</xref>).</p><p>The response to heavy metals requires the participation of mitochondrial PT. In particular, aluminum triggers a high ROS production in peanut, by plasmalemma NADPH oxidases, which induce mitochondrial mediated-PCD (<xref rid="B42" ref-type="bibr">Huang et al., 2014</xref>). Consistently, metal phytotoxicity appears to be also mediated by PT in aluminum- treated <italic>Arabidopsis</italic> protoplasts (<xref rid="B55" ref-type="bibr">Li and Xing, 2011</xref>) and in cadmium-treated rice roots (<xref rid="B98" ref-type="bibr">Yeh et al., 2007</xref>).</p><p>Biotic stress, such as pathogen attack, may lead to protoplast shrinkage, mitochondria swelling and cytochrome <italic>c</italic> release. These responses appear to be associated to PCD involvement during the hypersensitive response, a strategy to counteract biotrophic pathogens. The generation of a defensive layer, promoted by PT-induced PCD, has been shown in <italic>Arabidopsis.</italic> In particular, PCD is mediated by a rapid decrease in mitochondrial ΔΨ, which is partially counteracted by CsA (<xref rid="B97" ref-type="bibr">Yao et al., 2004</xref>). Finally, there is evidence on the release of cytochrome <italic>c</italic> induced by elicitors such as harpin or victorin (<xref rid="B17" ref-type="bibr">Curtis and Wolpert, 2002</xref>; <xref rid="B51" ref-type="bibr">Krause and Durner, 2004</xref>).</p></sec><sec><title>The Molecular Structure of PTP</title><p>The components involved in PTP formation initially included the voltage-dependent anion channel, the benzodiazepine receptor, the adenine nucleotide translocase and the phosphate carrier. This model has been questioned, since isolated mitochondria from organisms where the expression of each of these proteins has been suppressed still exhibit a PT (<xref rid="B49" ref-type="bibr">Kokoszka et al., 2004</xref>; <xref rid="B52" ref-type="bibr">Krauskopf et al., 2006</xref>; <xref rid="B5" ref-type="bibr">Baines et al., 2007</xref>; <xref rid="B36" ref-type="bibr">Gutiérrez-Aguilar et al., 2014</xref>; <xref rid="B81" ref-type="bibr">Šileikytė et al., 2014</xref>).</p><p>Recent evidence shows that F-ATPase is involved in PTP formation in different species and <italic>taxa</italic> (<xref rid="B8" ref-type="bibr">Bernardi, 2013b</xref>; <xref rid="B11" ref-type="bibr">Bonora et al., 2013</xref>; <xref rid="B2" ref-type="bibr">Alavian et al., 2014</xref>). This enzyme is highly conserved in both prokaryotes and eukaryotes (<xref rid="B39" ref-type="bibr">Hamasur and Glaser, 1992</xref>; <xref rid="B41" ref-type="bibr">Heazlewood et al., 2003</xref>), consisting in the hydrophilic F<sub>1</sub> and the hydrophobic F<sub>O</sub> sectors, which operate in concert to carry out distinct functions (<xref rid="B3" ref-type="bibr">Antoniel et al., 2014</xref>).</p><p>The F<sub>1</sub> contains five subunits: α and β forming the catalytic region, while γ, δ, and ε are organized in the central stalk. In all eukaryotes these subunits show a high degree of similarity in the sequences (<xref rid="B39" ref-type="bibr">Hamasur and Glaser, 1992</xref>; <xref rid="B3" ref-type="bibr">Antoniel et al., 2014</xref>; <xref rid="B46" ref-type="bibr">Jiko et al., 2015</xref>), while the subunit composition of the F<sub>O</sub> varies among different <italic>taxa</italic> and species (<xref rid="B39" ref-type="bibr">Hamasur and Glaser, 1992</xref>). For details about F-ATPase components in mammals, fungi and algae, see <xref rid="B89" ref-type="bibr">Vázquez-Acevedo et al. (2006)</xref>, <xref rid="B88" ref-type="bibr">van Lis et al. (2007)</xref>, <xref rid="B18" ref-type="bibr">Dabbeni-Sala et al. (2012)</xref>, <xref rid="B3" ref-type="bibr">Antoniel et al. (2014)</xref>, <xref rid="B53" ref-type="bibr">Lee et al. (2015)</xref> and <xref rid="B57" ref-type="bibr">Liu et al. (2015)</xref>. Specific subunits have been characterized in plants such as sweet potato (<xref rid="B68" ref-type="bibr">Morikami et al., 1992</xref>), potato (<xref rid="B22" ref-type="bibr">Dell’Orto et al., 1993</xref>; <xref rid="B71" ref-type="bibr">Polgreen et al., 1995</xref>) and soybean (<xref rid="B83" ref-type="bibr">Smith et al., 1994</xref>).</p><p>Plant F<sub>1</sub> includes the classical five-subunit structure (<xref rid="B38" ref-type="bibr">Hamasur and Glaser, 1990</xref>, <xref rid="B39" ref-type="bibr">1992</xref>), and also a 24 kDa protein (<xref rid="B54" ref-type="bibr">Li et al., 2012</xref>), but the picture of F<sub>O</sub> components remains still incomplete. Several proteins belonging to F<sub>O</sub> have been identified in spinach (<xref rid="B39" ref-type="bibr">Hamasur and Glaser, 1992</xref>), potato (<xref rid="B45" ref-type="bibr">Jänsch et al., 1996</xref>), rice (<xref rid="B41" ref-type="bibr">Heazlewood et al., 2003</xref>), and <italic>Arabidopsis</italic> (<xref rid="B41" ref-type="bibr">Heazlewood et al., 2003</xref>; <xref rid="B66" ref-type="bibr">Meyer et al., 2008</xref>; <xref rid="B48" ref-type="bibr">Klodmann et al., 2011</xref>). As shown by <xref rid="B48" ref-type="bibr">Klodmann et al. (2011)</xref> and by <xref rid="B54" ref-type="bibr">Li et al. (2012)</xref>, F<sub>O</sub> includes subunits a, c, d, 4 (corresponding to subunit b or orf25, <xref rid="B41" ref-type="bibr">Heazlewood et al., 2003</xref>), a 6 kDa protein (plant specific), subunit 8 (also called AL6 or orfB, <xref rid="B41" ref-type="bibr">Heazlewood et al., 2003</xref>), ATP17 (plant specific) and Oligomycin Sensitivity-Conferring Protein (OSCP), sometimes referred to as δ’ in plants (<xref rid="B68" ref-type="bibr">Morikami et al., 1992</xref>), for some authors belonging to F<sub>1</sub> (<xref rid="B45" ref-type="bibr">Jänsch et al., 1996</xref>). Subunit g was found detached from F-ATPase monomer, suggesting that it could represent a dimer-specific protein (<xref rid="B66" ref-type="bibr">Meyer et al., 2008</xref>; <xref rid="B48" ref-type="bibr">Klodmann et al., 2011</xref>). Plant subunit e sequences have been identified so far only in protein databases for few species (e.g., rice and <italic>Medicago truncatula</italic>).</p><p>Multimeric structures of F-ATPase are present in animal, fungi (<xref rid="B21" ref-type="bibr">Davies et al., 2011</xref>; <xref rid="B80" ref-type="bibr">Seelert and Dencher, 2011</xref>; <xref rid="B57" ref-type="bibr">Liu et al., 2015</xref>) and plant mitochondria (<xref rid="B28" ref-type="bibr">Eubel et al., 2003</xref>, <xref rid="B27" ref-type="bibr">2004</xref>; <xref rid="B50" ref-type="bibr">Krause et al., 2004</xref>; <xref rid="B12" ref-type="bibr">Bultema et al., 2009</xref>). <xref rid="B28" ref-type="bibr">Eubel et al. (2003)</xref> highlighted the presence of F-ATPase dimers in <italic>Arabidopsis</italic>, potato, bean, and barley. The relative abundance of dimers in plants is low, with respect to the total F-ATPase, and even lower when comparing different organisms (<xref rid="B28" ref-type="bibr">Eubel et al., 2003</xref>, <xref rid="B27" ref-type="bibr">2004</xref>).</p><p>Rows of F-ATPase dimers in <italic>cristae</italic> seem to be a universal feature of all mitochondria (<xref rid="B21" ref-type="bibr">Davies et al., 2011</xref>) that enable the formation of highly curved ridges in <italic>cristae</italic> (<xref rid="B20" ref-type="bibr">Davies et al., 2012</xref>). The Inhibitory factor 1 (IF<sub>1</sub>) that binds F-ATPase at low pH (<xref rid="B13" ref-type="bibr">Campanella et al., 2008</xref>) could favor dimer formation even if it is not clear how it improves dimer stability. The arrangement of F-ATPase in mammals and fungi is different from that of potato, being the angle between monomers in the latter larger (∼115°) than in the former (∼80°) (<xref rid="B21" ref-type="bibr">Davies et al., 2011</xref>). Interestingly, this correlates with <italic>cristae</italic> morphology observed for many plant mitochondria, where irregular saccular structures with a less convex curvature appear particularly prevalent (<xref rid="B25" ref-type="bibr">Douce, 1985</xref>). In aging <italic>Podospora anserina</italic> (<italic>Ascomycetes</italic>) mitochondria, the IMM is progressively vesiculated, the <italic>cristae</italic> collapse and the F-ATPase dimers are disassembled (<xref rid="B19" ref-type="bibr">Daum et al., 2013</xref>). The impairment of ATP synthesis, and the outer membrane rupture by swelling, lead to the release of pro-apoptotic factors and, finally, to cell death.</p><p>Animal mitochondria F-ATPase dimers have been shown to act as pores with properties of the PTP (<xref rid="B33" ref-type="bibr">Giorgio et al., 2013</xref>). CyPD modulates F-ATPase activity by binding OSCP (<xref rid="B32" ref-type="bibr">Giorgio et al., 2009</xref>) and this interaction is favored by P<sub>i</sub>, while CsA displaces CyPD from the enzyme. F-ATPase is inhibited by Bz-423, which binds to OSCP (<xref rid="B15" ref-type="bibr">Cleary et al., 2007</xref>). These features are consistent with those observed for PT regulation. Magnesium, Ca<sup>2+</sup>, adenine nucleotides, membrane potential and matrix pH are also key modulators of both F-ATPase activity and PTP. Electrophysiological experiments, after isolation and insertion of F-ATPase dimers in artificial phospholipid bilayers, showed that the pore activity matches that of PTP-MMC (<xref rid="B33" ref-type="bibr">Giorgio et al., 2013</xref>).</p><p>The involvement of F-ATPase dimers in PTP formation has been extended and confirmed in yeast and <italic>Drosophila</italic>, even if these organisms show specific differences. In yeast mitochondria the ionophore ETH129 is needed for Ca<sup>2+</sup> uptake in the matrix and the PT displays a low conductance (around 300 pS). Phosphate acts as an inhibitor of PT, while CsA does not interfere with PTP. Yeast mutants lacking of subunits e and g, which are involved in dimerization, display a striking resistance to PTP opening (<xref rid="B14" ref-type="bibr">Carraro et al., 2014</xref>). In <italic>Drosophila</italic> (<xref rid="B94" ref-type="bibr">von Stockum et al., 2015</xref>), PTP has been initially identified as mitochondrial Ca<sup>2+</sup>-induced Ca<sup>2+</sup> release channel (mCrC). The main differences between mCrC and mammalian PTP are: (i) absence of swelling; (ii) absence of CsA effect, since no CyPD is present in this species; (iii) sensitivity to rotenone, an inhibitor of Complex I; (iv) inhibition of mCrC by P<sub>i</sub>; (v) low conductance (around 53 pS) of the F-ATPase dimers in artificial bilayer.</p><p>Other research groups have also suggested that F-ATPase is involved in pore formation by the channel activity within the c-ring formed by c subunits of F<sub>O</sub> (<xref rid="B11" ref-type="bibr">Bonora et al., 2013</xref>; <xref rid="B2" ref-type="bibr">Alavian et al., 2014</xref>). Nevertheless, this hypothesis is still under debate, since it does not justify the different pore size observed in bovine, yeast, and <italic>Drosophila</italic>, where similar c-rings are present (<xref rid="B9" ref-type="bibr">Bernardi et al., 2015</xref>). Finally, the possible involvement of IF<sub>1</sub> in modulation of PTP through F-ATPase dimerization needs further investigations (<xref rid="B29" ref-type="bibr">Faccenda et al., 2013</xref>; <xref rid="B9" ref-type="bibr">Bernardi et al., 2015</xref>).</p><p>The presence in plants of many common components and features of F-ATPase lead us to speculate that, similarly to mammals, yeast, and <italic>Drosophila</italic>, PT function could be exerted by F-ATPase dimers also in such organisms.</p></sec><sec><title>The Emergence of PT During Evolution</title><p>Evolution does not always proceed by adaptations. It may also develop a non-adaptive exaptation/cooptation (pre-adaptation), where the term exaptation/cooptation means a trait evolved to accomplish a specific function (or even no function), which may be then exapted/coopted to perform a novel function (or to acquire a function) (<xref rid="B34" ref-type="bibr">Gould and Vrba, 1982</xref>).</p><p>It has been suggested that the structure of PTP (as a multicomponent complex, <xref rid="B7" ref-type="bibr">Bernardi, 2013a</xref>) may have arisen by a mechanism of molecular exaptation, a phenomenon largely recognized at different levels of complexity (genes, proteins, organs), during evolution (<xref rid="B90" ref-type="bibr">Vianello et al., 2012</xref>; <xref rid="B6" ref-type="bibr">Barve and Wagner, 2013</xref>). The new model, involving F-ATPase dimer in PTP formation, does not contradict our previous interpretation on its origin, but rather appears to support it further. The dimer appears to be the result of a molecular exaptation/cooptation, where two monomers are assembled to perform an additional function (<bold>Figure <xref ref-type="fig" rid="F1">1A</xref></bold>). In other words, F-ATPase seems to have a “Janus double face”, catalyzing the synthesis of ATP, but in some circumstances preventing such a synthesis (<xref rid="B9" ref-type="bibr">Bernardi et al., 2015</xref>). This dimer could even possess a “triple face”, because the dimerization induces also the curvature of the IMM.</p><fig id="F1" position="float"><label>FIGURE 1</label><caption><p><bold>(A)</bold> Hypothetical model of PTP in plants, based on F-ATPase dimer formation, as proposed by <xref rid="B8" ref-type="bibr">Bernardi (2013b)</xref>, <xref rid="B11" ref-type="bibr">Bonora et al. (2013)</xref>, and <xref rid="B2" ref-type="bibr">Alavian et al. (2014)</xref>. Plant F-ATPase subunits are organized on the basis of their putative correspondence to the mammalian ones. <bold>(B)</bold> Circular phylogenetic tree of peptide sequences of homologous subunit g of mitochondrial ATP synthase in four representative <italic>taxa</italic> (i.e., <italic>Bos taurus</italic>, <italic>Drosophila melanogaster</italic>, <italic>Saccharomyces cerevisiae</italic>, and <italic>Arabidopsis thaliana</italic>). Alignments of multiple amino acid sequences were performed using MUSCLE software (<xref rid="B26" ref-type="bibr">Edgar, 2004</xref>). Phylogenetic trees were obtained using phyML version 3.0 with the maximum-likelihood (ML) method (<xref rid="B35" ref-type="bibr">Guindon et al., 2010</xref>). The NCBI Reference Sequence accession codes for the g subunit are: <italic>B. taurus</italic> = NP_001019721; <italic>D. melanogaster</italic> = NP_609142; <italic>S. cerevisiae</italic> = NP_015345; <italic>A. thaliana</italic> = NP_179558. Where more isoforms were found in NCBI databases, we randomly selected only one of these sequences.</p></caption><graphic xlink:href="fpls-06-01120-g001"></graphic></fig><p>The F-ATPase dimer is present in eukaryotes, but not in prokaryotes, because the F-ATPase of the latter is lacking of some crucial subunits (e and g) involved in dimer formation (<xref rid="B3" ref-type="bibr">Antoniel et al., 2014</xref>). It is thus reasonable to assume that the dimer/PTP may be arisen after the endosymbiosis between an alpha-proteobacterium and an archaeon (<xref rid="B64" ref-type="bibr">Martin and Müller, 1998</xref>). At the beginning, these dimers could have transferred ATP from the endosymbiont to the cytoplasm of the host cell, because the former presumably did not have ATP/ADP transporters. PTP was then maintained to dissipate the protonmotive force, thus regulating both ATP synthesis and exchanges of solutes between the cytoplasm and the mitochondrial matrix.</p><p>The presence of F-ATPase dimer has been assessed in different evolutionary divergent eukaryotes, some of which exhibit mitochondrial PT, such as ‘<italic>Unikonts’</italic> (<italic>Opisthokonts</italic>) and <italic>Plantae</italic> (<xref rid="B4" ref-type="bibr">Arpagaus et al., 2002</xref>; <xref rid="B33" ref-type="bibr">Giorgio et al., 2013</xref>; <xref rid="B14" ref-type="bibr">Carraro et al., 2014</xref>; <xref rid="B94" ref-type="bibr">von Stockum et al., 2015</xref>). To understand the phylogenesis of this structure/function, a cladogram has been generated by comparing the ancestral sequences of F<sub>O</sub> subunit g from bovine and <italic>Drosophila</italic> (animals), yeast (fungi, <italic>Ascomycetes</italic>), and <italic>Arabidopsis</italic> (<italic>Plantae</italic>) (<bold>Figure <xref ref-type="fig" rid="F1">1B</xref></bold>). The tree suggests an early differentiation at higher taxonomical levels (supergroups): <italic>Plantae</italic> show the highest phylogenetic distance and within the <italic>Opisthokonts</italic>, mammals, and insects exhibit similar distances, whereas yeast shows a higher distance. These phylogenetic patterns are consistent with the main evolutionary life tree (e.g., <xref rid="B47" ref-type="bibr">Keeling et al., 2005</xref>).</p><p>It has been suggested that F-ATPase shows a progressive differentiation along the main steps of evolution. In turn, some features of PTP seem to be occurred independently from changes in ATP synthase. As an example, swelling of mitochondria occurs only in bovine (<xref rid="B9" ref-type="bibr">Bernardi et al., 2015</xref>) and in some plants (see <bold>Table <xref ref-type="table" rid="T1">1</xref></bold>), suggesting that PTP has been differently shaped by exaptation during the evolution. Hence, exaptation leading to PT seems to have occurred in diverse contexts during life history, depending on the molecular characteristics of F-ATPase structure and the specific requirements of the respective <italic>taxa</italic>.</p></sec><sec><title>Future Directions</title><p>The molecular nature of PTP in plants is still elusive. Further structural and functional studies are required to verify if F-ATPase dimers represent the channel associated to PT also in plants. This is needed to understand better the relationship between mitochondrial PT and PCD in plants.</p></sec><sec><title>Author Contributions</title><p>MZ and AV co-supervised the manuscript and co-wrote the article. VC, EP, CP, SP, AB, and EB co-wrote the article. VDC and FB performed the phylogenetic analyses and co-wrote the article.</p></sec><sec><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><fn-group><fn fn-type="financial-disclosure"><p><bold>Funding</bold>. This work was supported by the Italian Ministry of Education, University and Research (National Research Program PRIN2010CSJX4F) and the European Social Fund (Program 2007/2013).</p></fn></fn-group><ack><p>We thank Paolo Bernardi (University of Padova), Markus Schwarzländer (University of Bonn), and Giovanna Lippe (University of Udine) for their critical reading of the manuscript and Manuela Antoniel (University of Padova) for help in drawing F-ATPase.</p></ack><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Akerman</surname><given-names>K. E.</given-names></name><name><surname>Moore</surname><given-names>A. L.</given-names></name></person-group> (<year>1983</year>). <article-title>Phosphate dependent, ruthenium red insensitive Ca<sup>2+</sup> uptake in mung bean mitochondria.</article-title><source><italic>Biochem. Biophys. Res. 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