Plant Mitochondria

Abstract

Plant mitochondria, like the mitochondria of other eukaryotes, originated from an endosymbiotic event and have retained their own genome. Over a billion years of evolution, most mitochondrial genes are laterally transferred to the nucleus. Consequently, most proteins required for mitochondrial biogenesis and activity are synthesised in the cytosol and imported via specific protein import machineries. Mitochondria are energy‐generating organelles that via electron transfer chain (ETC), create a proton gradient and generate adenosine triphosphate (ATP), the energy chemical used by the cell for numerous biochemical reactions. Energy production can come at a cost as reactive oxygen species (ROS) are generated as by‐product. Plant mitochondria have alternative ETC pathways to regulate mitochondrial ROS (mtROS) through modulating the rate of redox reactions, proton gradient and ATP production. Although excessive ROS can damage cellular components and lead to programmed cell death, mtROS also play an important role as signalling molecules. mtROS are involved in nucleus–mitochondria communications (anterograde–retrograde signalling), mitochondrial autophagy (mitophagy) and play a role in the plant response to various environmental stimuli. Considering the pivotal roles of mitochondria in energy generation and cellular signalling, perturbation of mitochondrial biogenesis and activity renders plants to be more susceptible to various stresses and ultimately compromises plant growth, development and reproduction.

Key Concepts

  • Plant mitochondria are small (1–2 μm long) rod‐shaped organelle that undergo frequent fusion and fission events.
  • The plant mitochondrial inner membrane houses protein complexes involved in the electron transfer chain (ETC) that creates a proton‐motive gradient across the intermembrane space to drive the production of adenosine triphosphate (ATP) through ATP synthase.
  • The majority of plant mitochondrial proteins (approximately 2000) are encoded in the nuclear genome, whereas the plant mitochondrial genome contains around 50 genes encoding for ETC subunits, mitoribosomal translation machinery and transfer ribonucleic acids (tRNAs).
  • The abundance of mtROS produced by the ETC is proportionally linked with the efficiency and rate of electron transfer and ATP production.
  • Plant mitochondria have alternative ETC pathways to modulate ROS homeostasis, proton gradient and ATP production.
  • mtROS can damage mitochondrial macromolecules and ultimately organelle function but are also important signalling molecules in various pathways, including stress response and anterograde–retrograde signalling.
  • The nucleus controls mitochondrial gene expression through anterograde signalling, yet the mitochondria can also influence nuclear gene expression through retrograde signalling.
  • Disrupted plant mitochondrial function often causes enhanced sensitivity to a number of stresses, disrupted pollen development in cytoplasmic male sterility and affects normal plant growth and development.

Keywords: anterograde and retrograde signalling; cytoplasmic male sterility; electron transfer chain; mitochondrial biogenesis; mitochondrial genome; mitochondrial homeostasis; mitochondrial import; mitophagy; plant mitochondria; reactive oxygen species; stress response

Figure 1. Structural organisation of mitochondria that mainly divided into six compartments: outer membrane, inner membrane, matrix, cristae, intermembrane space and intercristal space.
Figure 2. Plant mitochondrial electron transfer chain (ETC) in the inner membrane (IM). Complexes actively involved in the redox reactions and electron transfer are indicated in blue (Complex I–IV). ATP synthase (Complex V) consists of Fo and F1 units are shown in cyan. Plant‐specific alternative ETC pathways are shown in grey, which comprise of alternative oxidase (AOX) and NAD(P)H dehydrogenases (NDs). Electron (e) transfer is depicted as dashed lines and protons are pumped from the matrix (M) to the intermembrane (IMS) and intercristal spaces. Cyt c, cytochrome c; PUMP, plant uncoupling mitochondrial protein; TCA, tricarboxylic acid; UQ, ubiquinone.
Figure 3. Protein import pathways into plant mitochondria. Four major protein import pathways (dashed lines) for different types of protein from the cytosol (C) that all cross the translocase of outer membrane (TOM) complex. The general pathway (blue) describes the import of protein containing N‐terminal targeting peptide that uses the translocase of inner membrane (TIM17:23) complex and associated presequence‐assisted motor (PAM) complex into the matrix (M). The carrier import pathway (red) depicts the import of protein with internal targeting signal, mostly carrier proteins to the inner membrane via TIM22 gate. The sorting and assembly machinery (SAM) pathway is specifically for β‐barrel proteins targeted to the outer membrane (OM). Both carrier pathway and SAM pathway use small TIMs in assisting the translocation. The mitochondrial intermembrane space (IMS) assembly (MIA) pathway is used for translocating twin‐cysteine proteins into the IMS.
Figure 4. Intracellular communications within plant cell. The nucleus controls nuclear‐encoded mitochondrial gene expression (anterograde signalling), but mitochondria and chloroplasts influence nuclear gene expression through retrograde signalling, primarily by reactive oxygen species (ROS) and calcium ion (Ca2+). These signalling molecules may directly alter nuclear gene expression (red solid lines) or indirectly (blue dashed lines) through activation of redox sensors and post‐translational modifications by kinases (K) and phosphatases (P).
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References

Barkan A and Small I (2014) Pentatricopeptide repeat proteins in plants. Annual Review of Plant Biology 65: 415–442.

Broda M, Millar AH and Van Aken O (2018) Mitophagy: a mechanism for plant growth and survival. Trends in Plant Science 23: 434–450.

Carraretto L, Checchetto V, De Bortoli S, et al. (2016) Calcium flux across plant mitochondrial membranes: possible molecular players. Frontiers in Plant Science 7: 1–8.

Carrie C, Murcha MW, Giraud E, et al. (2013) How do plants make mitochondria? Planta 237: 429–439.

Chehab EW, Eich E and Braam J (2009) Thigmomorphogenesis: a complex plant response to mechano‐stimulation. Journal of Experimental Botany 60: 43–56.

Chehab EW, Yao C, Henderson Z, Kim S and Braam J (2012) Arabidopsis touch‐induced morphogenesis is jasmonate mediated and protects against pests. Current Biology 22: 701–706.

Dojcinovic D, Krosting J, Harris AJ, Wagner DJ and Rhoads DM (2005) Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression. Plant Molecular Biology 58: 159–175.

Dudkina NV, Eubel H, Keegstra W, Boekema EJ and Braun HP (2005) Structure of a mitochondrial supercomplex formed by respiratory‐chain complexes I and III. Proceedings of the National Academy of Sciences of the United States of America 102: 3225–3229.

Dudkina NV, Heinemeyer J, Sunderhaus S, Boekema EJ and Braun HP (2006) Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends in Plant Science 11: 232–240.

Dudkina NV, Kouřil R, Peters K, Braun HP and Boekema EJ (2010) Structure and function of mitochondrial supercomplexes. Biochimica et Biophysica Acta ‐ Bioenergetics 1797: 664–670.

Duncan O, Taylor NL, Carrie C, et al. (2011) Multiple lines of evidence localize signaling, morphology, and lipid biosynthesis machinery to the mitochondrial outer membrane of Arabidopsis. Plant Physiology 157: 1093–1113.

Duncan O, Murcha MW and Whelan J (2013) Unique components of the plant mitochondrial protein import apparatus. Biochimica et Biophysica Acta – Molecular Cell Research 1833: 304–313.

Ghifari AS, Gill‐Hille M and Murcha MW (2018) Plant mitochondrial protein import: the ins and outs. Biochemical Journal 475: 2191–2208.

Ghifari AS, Huang S and Murcha MW (2019) The peptidases involved in plant mitochondrial protein import. Journal of Experimental Botany 70: 6005–6018.

Gomes LC and Scorrano L (2013) Mitochondrial morphology in mitophagy and macroautophagy. Biochimica et Biophysica Acta – Molecular Cell Research 1833: 205–212.

Gualberto JM, Mileshina D, Wallet C, et al. (2014) The plant mitochondrial genome: dynamics and maintenance. Biochimie 100: 107–120.

Gualberto JM and Newton KJ (2017) Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annual Review of Plant Biology 68: 225–252.

Haïli N, Planchard N, Arnal N, et al. (2016) The MTL1 pentatricopeptide repeat protein is required for both translation and splicing of the mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in arabidopsis1. Plant Physiology 170: 354–366.

Hamasaki H, Yoshizumi T, Takahashi N, et al. (2012) SD3, an Arabidopsis thaliana homolog of TIM21, affects intracellular ATP levels and seedling development. Mol Plant 5: 461–471.

Hartl M and Finkemeier I (2012) Plant mitochondrial retrograde signaling: post‐translational modifications enter the stage. Frontiers in Plant Science 3: 1–7.

Heazlewood JL, Howell KA and Millar AH (2003) Mitochondrial complex I from Arabidopsis and rice: orthologs of mammalian and fungal components coupled with plant‐specific subunits. Biochimica et Biophysica Acta – Bioenergetics 1604: 159–169.

Howell KA, Millar AH and Whelan J (2006) Ordered assembly of mitochondria during rice germination begins with pro‐mitochondrial structures rich in components of the protein import apparatus. Plant Molecular Biology 60: 201–223.

Howell KA, Cheng K, Murcha MW, et al. (2007) Oxygen initiation of respiration and mitochondrial biogenesis in rice. Journal of Biological Chemistry 282: 15619–15631.

Hu Y, Zou W, Wang Z, et al. (2019) Translocase of the outer mitochondrial membrane 40 is required for mitochondrial biogenesis and embryo development in arabidopsis. Frontiers in Plant Science 10: 1–17.

Huang S, Van Aken O, Schwarzländer M, Belt K and Millar AH (2016) The roles of mitochondrial reactive oxygen species in cellular signaling and stress response in plants. Plant Physiology 171: 1551–1559.

Huang S, Braun H‐P, Gawryluk RMR and Millar AH (2019) Mitochondrial complex II of plants: subunit composition, assembly and function in respiration and signaling. The Plant Journal: 1–13.

Klodmann J, Sunderhaus S, Nimtz M, Jänsch L and Braun HP (2010) Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell 22: 797–810.

Klodmann J, Senkler M, Rode C and Braun HP (2011) Defining the protein complex proteome of plant mitochondria. Plant Physiology 157: 587–598.

Kmiec B, Teixeira PF, Berntsson RP‐A, et al. (2013) Organellar oligopeptidase (OOP) provides a complementary pathway for targeting peptide degradation in mitochondria and chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 110: E3761–E3769.

Kmiec B, Teixeira PF and Glaser E (2014) Shredding the signal: targeting peptide degradation in mitochondria and chloroplasts. Trends in Plant Science 19: 771–778.

Kmiec B, Branca RMM, Murcha MW, et al. (2018) A common peptidolytic mechanism for targeting peptide degradation in mitochondria and chloroplasts. Molecular Plant 11: 342–345.

Koulintchenko M, Konstantinov Y and Dietrich A (2008) Plant mitochondria actively import DNA via the permeability transition pore complex. The EMBO Journal 22: 1245–1254.

Lange MJP and Lange T (2015) Touch‐induced changes in Arabidopsis morphology dependent on gibberellin breakdown. Nature Plants 1: 2–6.

Law SR, Narsai R, Taylor NL, et al. (2012) Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiology 158: 1610–1627.

Lee CP and Millar AH (2016) The plant mitochondrial transportome: balancing metabolic demands with energetic constraints. Trends in Plant Science 21: 662–676.

Li F, Chung T and Vierstra RD (2014) AUTOPHAGY‐RELATED11 plays a critical role in general autophagy‐ and senescence‐induced mitophagy in Arabidopsis. Plant Cell 26: 788–807.

Liberatore KL, Dukowic‐Schulze S, Miller ME, Chen C and Kianian SF (2016) The role of mitochondria in plant development and stress tolerance. Free Radical Biology and Medicine 100: 238–256.

Lister R, Carrie C, Duncan O, et al. (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell 19: 3739–3759.

Michaud M, Cognat V, Duchêne AM and Maréchal‐Drouard L (2011) A global picture of tRNA genes in plant genomes. Plant Journal 66: 80–93.

Millar AH, Eubel H, Jänsch L, et al. (2004) Mitochondrial cytochrome c oxidase and succinate dehydrogenase complexes contain plant specific subunits. Plant Molecular Biology 56: 77–90.

Minibayeva F, Dmitrieva S, Ponomareva A and Ryabovol V (2012) Oxidative stress‐induced autophagy in plants: the role of mitochondria. Plant Physiology and Biochemistry 59: 11–19.

Minina EA, Filonova LH, Fukada K, et al. (2013) Autophagy and metacaspase determine the mode of cell death in plants. Journal of Cell Biology 203: 917–927.

van Moerkercke A, Duncan O, Zander M, et al. (2019) A MYC2/MYC3/MYC4‐dependent transcription factor network regulates water spray‐responsive gene expression and jasmonate levels. Proceedings of the National Academy of Sciences of the United States of America 116: 23345–23356.

Murcha MW, Wang Y, Narsai R and Whelan J (2014) The plant mitochondrial protein import apparatus – the differences make it interesting. Biochimica et Biophysica Acta – General Subjects 1840: 1233–1245.

Murcha MW, Kubiszewski‐Jakubiak S, Teixeira PF, et al. (2016) Plant‐specific preprotein and amino acid transporter proteins are required for tRNA import into mitochondria. Plant Physiology 172: 2471–2490.

Narsai R, Law SR, Carrie C, Xu L and Whelan J (2011) In‐depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiology 157: 1342–1362.

Ng S, Ivanova A, Duncan O, et al. (2013) A membrane‐bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell 25: 3450–3471.

Ng S, De Clercq I, Van Aken O, et al. (2014) Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Molecular Plant 7: 1075–1093.

Rhoads DM and Subbaiah CC (2007) Mitochondrial retrograde regulation in plants. Mitochondrion 7: 177–194.

Rose RJ and McCurdy DW (2017) New Beginnings: Mitochondrial Renewal by Massive Mitochondrial Fusion. Trends in Plant Science 22: 641–643.

Salinas T, Duchêne AM, Delage L, et al. (2006) The voltage‐dependent anion channel, a major component of the tRNA import machinery in plant mitochondria. Proceedings of the National Academy of Sciences of the United States of America 103: 18362–18367.

Schertl P and Braun HP (2014) Respiratory electron transfer pathways in plant mitochondria. Frontiers in Plant Science 5: 163.

Schimmeyer J, Bock R and Meyer EH (2016) l‐Galactono‐1,4‐lactone dehydrogenase is an assembly factor of the membrane arm of mitochondrial complex I in Arabidopsis. Plant Molecular Biology 90: 117–126.

Schmidtmann E, König AC, Orwat A, et al. (2014) Redox regulation of Arabidopsis mitochondrial citrate synthase. Molecular Plant 7: 156–169.

Sloan DB, Alverson AJ, Chuckalovcak JP, et al. (2012) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biology 10.

Subrahmanian N, Remacle C and Hamel PP (2016) Plant mitochondrial Complex I composition and assembly: a review. Biochimica et Biophysica Acta – Bioenergetics 1857: 1001–1014.

Sweetman C, Waterman CD, Rainbird BM, et al. (2019) AtNDB2 is the main external NADH dehydrogenase in mitochondria and is important for tolerance to environmental stress. Plant Physiology 181: 774–788.

Touzet P and Budar F (2004) Unveiling the molecular arms race between two conflicting genomes in cytoplasmic male sterility? Trends in Plant Science 9: 568–570.

Uyttewaal M, Mireau H, Rurek M, et al. (2008) PPR336 is associated with polysomes in plant mitochondria. Journal of Molecular Biology 375: 626–636.

Vercesi AE, Borecký J and Maia I de G, Arruda P, Cuccovia IM, Chaimovich H. (2006) Plant uncoupling mitochondrial proteins. Annual Review of Plant Biology 57: 383–404.

Vincent T, Vingadassalon A, Ubrig E, et al. (2017) A genome‐scale analysis of mRNAs targeting to plant mitochondria: upstream AUGs in 5′ untranslated regions reduce mitochondrial association. Plant Journal 92: 1132–1142.

Wagner AM, Krab K, Wagner MJ and Moore AL (2008) Regulation of thermogenesis in flowering Araceae: the role of the alternative oxidase. Biochimica et Biophysica Acta ‐ Bioenergetics 1777: 993–1000.

Waltz F, Nguyen TT, Arrivé M, et al. (2019) Small is big in Arabidopsis mitochondrial ribosome. Nature Plants 5: 106–117.

Wang Y, Carrie C, Giraud E, et al. (2012) Dual location of the mitochondrial preprotein transporters B14.7 and Tim23‐2 in complex I and the TIM17:23 complex in Arabidopsis links mitochondrial activity and biogenesis. The Plant Cell 24: 2675–2695.

Xu Y, Berkowitz O, Narsai R, et al. (2019) Mitochondrial function modulates touch signalling in Arabidopsis thaliana. Plant Journal 97: 623–645.

Yoshida K, Noguchi K, Motohashi K and Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant and Cell Physiology 54: 875–892.

Yoshida K and Hisabori T (2014) Mitochondrial isocitrate dehydrogenase is inactivated upon oxidation and reactivated by thioredoxin‐dependent reduction in Arabidopsis. Frontiers in Environmental Science 2: 1–7.

Zhu Y, Lu J, Wang J, et al. (2011) Regulation of thermogenesis in plants: the interaction of alternative oxidase and plant uncoupling mitochondrial protein. Journal of Integrative Plant Biology 53: 7–13.

Further Reading

Bergthorsson U, Adams KL, Thomason B and Palmer JD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197–201.

Gualberto JM and Newton KJ (2017) Plant mitochondrial genomes: dynamics and mechanisms of mutation. Annual Review of Plant Biology 68: 225–252.

Liere K, Weihe A and Börner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function and regulation. Journal of Plant Physiology 168: 1345–1360.

Logan DC (ed.) (2018) Plant mitochondria. In: Annual Plant Reviews, vol. 50. Wiley.

Millar AH, Whelan J, Soole KL and Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annual Review of Plant Biology 62: 79–104.

Møller IM (2016) What is hot in plant mitochondria? Physiologia Plantarum 157: 256–263.

Murcha MW, Kmiec B, Kubiszewski‐Jakubiak S, et al. (2014) Protein import into plant mitochondria: signals, machinery, processing, and regulation. Journal of Experimental Botany 65: 6301–6335.

Noctor G, De Paepe R and Foyer CH (2007) Mitochondria redox biology and homeostasis in plants. Trends in Plant Science 12: 125–134.

Rose RJ (ed.) (2016) Molecular Cell Biology of the Growth and Differentiation of Plant Cells. Taylor & Francis Group: LLC.

Rose RJ (2019) Sustaining life: maintaining chloroplasts and mitochondria and their genomes in plants. Yale Journal of Biology and Medicine 92: 499–510.

Sweetlove LJ, Fait A, Nunes‐Nesi A, Williams T and Fernie AR (2007) The mitochondrion: an integration point of cellular metabolism and signalling. Critical Reviews in Plant Sciences 26: 17–43.

Wang Y, Selinski J, Mao C, et al. (2020) Linking mitochondrial and chloroplast signalling in plants. Philosophical Transactions of the Royal Society B 375: 20190410.

Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nature Review Molecular Cell Biology 11: 872–884.

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Ghifari, Abi S, and Murcha, Monika W(Oct 2020) Plant Mitochondria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029217]