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ANNUAL PLANT REVIEWS, VOLUME 50

Plant Mitochondria

SECOND EDITION



Edited by

David C. Logan

IRHS, Université d’Angers, INRA,
Agrocampus-Ouest, France












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Annual Plant Reviews

A series for researchers and postgraduates in the plant sciences. Each volume in this series focuses on a theme of topical importance and emphasis is placed on rapid publication.


Editorial Board:

Professor Jeremy A. Roberts (Editor‐in‐Chief), Plant Science Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK

Dr David Evans, School of Biological and Molecular Sciences, Oxford Brookes University, Headington, Oxford, OX3 0BP, UK

Professor Hidemasa Imaseki, Obata‐Minami 2419, Moriyama‐ku, Nagoya 463, Japan

Dr Jocelyn K.C. Rose, Department of Plant Biology, Cornell University, Ithaca, New York 14853, USA


Titles in the series:

  1. Arabidopsis

    Edited by M. Anderson and J.A. Roberts

  2. Biochemistry of Plant Secondary Metabolism

    Edited by M. Wink

  3. Functions of Plant Secondary Metabolites and Their Exploitation in Biotechnology

    Edited by M. Wink

  4. Molecular Plant Pathology

    Edited by M. Dickinson and J. Beynon

  5. Vacuolar Compartments

    Edited by D.G. Robinson and J.C. Rogers

  6. Plant Reproduction

    Edited by S.D. O’Neill and J.A. Roberts

  7. Protein–Protein Interactions in Plant Biology

    Edited by M.T. McManus, W.A. Laing and A.C. Allan

  8. The Plant Cell Wall

    Edited by J.K.C. Rose

  9. The Golgi Apparatus and the Plant Secretory Pathway

    Edited by D.G. Robinson

  10. The Plant Cytoskeleton in Cell Differentiation and Development

    Edited by P.J. Hussey

  11. Plant–Pathogen Interactions

    Edited by N.J. Talbot

  12. Polarity in Plants

    Edited by K. Lindsey

  13. Plastids

    Edited by S.G. Moller

  14. Plant Pigments and their Manipulation

    Edited by K.M. Davies

  15. Membrane Transport in Plants

    Edited by M.R. Blatt

  16. Intercellular Communication in Plants

    Edited by A.J. Fleming

  17. Plant Architecture and Its Manipulation

    Edited by C. Turnbull

  18. Plasmodeomata

    Edited by K.J. Oparka

  19. Plant Epigenetics

    Edited by P. Meyer

  20. Flowering and Its Manipulation

    Edited by C. Ainsworth

  21. Endogenous Plant Rhythms

    Edited by A.J.W. Hall and H.G. McWatters

  22. Control of Primary Metabolism in Plants

    Edited by W.C. Plaxton and M.T. McManus

  23. Biology of the Plant Cuticle

    Edited by M. Riederer and C. M¨uller

  24. Plant Hormone Signaling

    Edited by P. Hedden and S.G. Thomas

  25. Plant Cell Separation and Adhesion

    Edited by J.A. Roberts and Z. Gonzalez‐Carranza

  26. Senescence Processes in Plants

    Edited by S. Gan

  27. Seed Development, Dormancy and Germination

    Edited by K. Bradford and H. Nonogaki

  28. Plant Proteomics

    Edited by C. Finnie

  29. Regulation of Transcription in Plants

    Edited by K.D. Grasser

  30. Light and Plant Development

    Edited by G.C. Whitelam and K.J. Halliday

  31. Plant Mitochondria

    Edited by D.C. Logan

  32. Cell Cycle Control and Plant Development

    Edited by D. Inzé

  33. Intracellular Signaling in Plants

    Edited by Z. Yang

  34. Molecular Aspects of Plant Disease Resistance

    Edited by J. Parker

  35. Plant Systems Biology

    Edited by G.M. Coruzzi and R.A. Gutierrez

  36. TheMoss Physcomitrella patens

    Edited by C.D. Knight, P.‐F. Perroud and D.J. Cove

  37. Root Development

    Edited by T. Beeckman

  38. Fruit Development and Seed Dispersal

    Edited by L. Østergaard

  39. Function and Biotechnology of Plant Secondary Metabolites

    Edited by M. Wink

  40. Biochemistry of Plant Secondary Metabolism

    Edited by M. Wink

  41. Plant Polysaccharides

    Edited by P. Ulvskov

  42. NitrogenMetabolism in Plants in the Post‐genomic Era

    Edited by C. Foyer and H. Zhang

  43. Biology of Plant Metabolomics

    Edited by R.D. Hall

  44. The Plant Hormone Ethylene

    Edited by M.T. McManus

  45. The Evolution of Plant Form

    Edited by B.A. Ambrose and M.D. Purugganan

  46. Plant Nuclear Structure, Genome Architecture and Gene Regulation

    Edited by D.E. Evans, K. Graumann and J.A. Bryant

  47. Insect‐Plant Interactions

    Edited by C. Voelckel and G. Jander

  48. PhosphorusMetabolism in Plants

    Edited by W.C. Plaxton and H. Lambers

  49. The Gibberellins

    Edited by P. Hedden and S.G. Thomas

LIST OF CONTRIBUTORS

Hermann Bauwe
Department of Plant Physiology, University of Rostock, Rostock, Germany

Françoise Budar
Institut Jean‐Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris‐Saclay, 78000 Versailles, Versailles, France

Alan C. Christensen
School of Biological Sciences, University of Nebraska–Lincoln, Lincoln, USA

Néstor Fernández Del‐Saz
Grup de Recerca en Biologia de les Plantes en Condicions Mediterrànies, Departament de Biologia, Universitat de les Illes Balears, Palma de Mallorca, Spain

Iris Finkemeier
Plant Proteomics Group, Max Planck Institute for Plant Breeding Research, Cologne, Germany & Institute of Plant Biology and Biotechnology, University of Münster, Münster, Germany

Marc Hanikenne
InBioS – PhytoSYSTEMS, Functional Genomics and Plant Molecular Imaging, University of Liège, Liège, Belgium

Richard P. Jacoby
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, Bayliss Building M316, University of Western Australia, Crawley, Australia

David C. Logan
IRHS, Université d’Angers, INRA, Agrocampus-Ouest, France

A. Harvey Millar
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, Bayliss Building M316, University of Western Australia, Crawley, Australia

Hakim Mireau
Institut Jean‐Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris‐Saclay, 78000 Versailles, Versailles, France

Oren Ostersetzer‐Biran
Department of Plant and Environmental Sciences, Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel

Gaël Paszkiewicz
IIRHS UMR1345, INRA/Agrocampus‐ouest, Université d’ngers, France

Miquel Ribas‐Carbo
Grup de Recerca en Biologia de les Plantes en Condicions Mediterrànies, Departament de Biologia, Universitat de les Illes Balears, Palma de Mallorca, Spain

Markus Schwarzländer
Plant Energy Biology Laboratory, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany;Institute of Plant Biology and Biotechnology, University of Münster, Münster, Germany

Iain Scott
Vascular Medicine Institute, Division of Cardiology, Department of Medicine, University of Pittsburgh, Pittsburgh, USA

Nicolas L. Taylor
ARC Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, Bayliss Building M316, University of Western Australia, Crawley, Australia;Institute of Agriculture, University of Western Australia, Crawley, Australia

Olivier Van Aken
ARC Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, Australia;
Department of Biology, Lund University, 35 Sölvegatan, Lund, Sweden

Gianpiero Vigani
Dipartimenti di Scienze Agrarie e Ambientali – Produzione, Territorio, Agroenergia, Università degli studi di Milano, Milano, Italy

Michal Zmudjak
Department of Plant and Environmental Sciences, Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel

PREFACE

Welcome to the second edition of Plant Mitochondria. The first edition was published in 2007, which, perhaps depending on your age, was either a long time ago or almost as if it were yesterday. While we can accept differences in human perception of the passage of time, it becomes more conceptually difficult to understand that time is not an absolute: two people moving through time at different speeds will experience events in that timeline at different relative times. The publication of Albert Einstein’s 1905 paper ‘On the electrodynamics of moving bodies’, which became known as his special relativity paper, was a seminal moment for physics, and science in general (Einstein, 1905). However, at the same time, the organelles fuelling Einstein’s extraordinary thinking did not have an agreed name (Cowdry, 1918), nor, indeed, did we know that the fuelling was even performed by organelles, of whatever name: identification of mitochondria as the site of oxidative metabolism took another 40+ years. Research in physics operates at a pace and scale different to that of biology!

As biologists, we use time, in our experiments, all the time. We are interested in the rate of change of an activity or behaviour. And central to all biology is evolution, which is change over time. As Theodosius Dobzhansky famously wrote in his essay of the same title, ‘Nothing in biology makes sense except in the light of evolution’ (Dobzhansky, 1973). A true statement cannot be more true, just as a falsehood is a lie, but in the case of mitochondria, we can say the statement is particularly apt; indeed, perhaps the corollary is valid, and nothing in the evolution of life on earth makes sense without considering mitochondria?

The world at the time of publication of the first edition of this book was very different from the world of 2017. The first iPhone was released in 2007, cloud computing took off in 2007 (for example, Dropbox was started in 2007), Google introduced Android, and Amazon introduced the Kindle. These advances changed the way many of us interact with the world around us, with parallel developments in social media: Facebook had only opened up to individuals with private email addresses in September 2006, and Twitter, launched in July 2006, was showing traffic of 400 000 tweets per quarter in 2007, rising to 50 million per day in February 2010, and now stands at 500 million tweets per day! Social media has revolutionized the way many people communicate science. However, 2007 also marked the end of a period of economic growth and optimism that culminated in a massive loss of optimism and a global financial crash from which the world still reels. This led to ‘austerity’, budget cuts and drastic reductions in the funding of basic scientific research, as the reduced funds available are earmarked to support research some believe is more likely to lead to economic recovery.

Despite years of austerity for fundamental plant biology research funding, we have seen major breakthroughs in our understanding of plant mitochondria, and thus a new edition of this book was timely. The evolving story of the mitochondrion, the story of the evolving mitochondrion, is the longest in the history of the eukaryotic cell. To paraphrase Roy Batty, the mitochondrion has seen things other organelles wouldn’t believe. But, in what ways has our understanding of plant mitochondria advanced in 10 years?

We have seen dramatic advances in next‐generation sequencing since 2007, and use of this technology has had a profound influence on our understanding of the evolution of mitochondrial genomes. The availability of sequence data and bioinformatic advances were also critical to the discovery of PPR proteins as editing factors, and subsequently, the amino acid code they use for RNA recognition (Barkan et al., 2012). And, more recently, advances in genome sequencing led to the discovery of the first mitochondriate eukaryote, amongst over 300 mitogenomes analysed, to lack complex I (Skippington et al., 2015).

We have seen fresh views on the photorespiratory pathway, which enables continued operation of the Calvin–Benson cycle, rather than being a wasteful process. And interactions between the two processes apparently include regulatory feedback between glycine decarboxylation in the mitochondrion and CO2 fixation in the chloroplast (Hagemann & Bauwe, 2016).

Our understanding of other signalling processes between mitochondria and other cell components, and how these signals regulate mitochondrial activity, has increased apace in the past 10 years. We have also seen advances in our understanding of retrograde signalling, for example via NAC transcription factors (de Clercq et al., 2013; Ng et al., 2013), and there is growing evidence for retrograde signalling as a means to regulate nutrition, with a potential role for mitochondria as nutrient sensors (Vigani and Briat, 2015).

Signals induce changes in activity and one means to alter protein activity is by protein modification, but until recently we knew little about modification to mitochondrial proteins. However, lysine acetylation has now been identified as a common modification of mitochondrial proteins, and Arabidopsis sirtuin 2 was identified as the first plant mitochondrial lysine deacytylase (Finkemeier et al., 2011; König et al., 2014).

Finally, I end this preface with microscopy, the scientific tool first used to investigate mitochondria in the late 19th century. Our knowledge of mitochondrial cell biology has advanced dramatically since 2007, aided by the development of better imaging systems and the relatively massive computing power at our disposal to drive image analysis. These have allowed precise quantitative analysis of changes in the dynamics and, even more excitingly, the physiology of each individual mitochondrion, in real time. These advances have underpinned work identifying energy transients in individual mitochondria within living plant cells, in situ, and components of mitochondrial calcium regulation (Schwarzländer and Finkemeier, 2013; Schwarzländer et al., 2012a, b, 2014; Wagner et al., 2015).

Advances in our understanding of plant mitochondria are made through the actions of research scientists, and communicating those advances is a vital part of their job. The purpose of this book is to communicate to you some of the most important aspects of plant mitochondrial biology, and who better to serve as the conduit for that communication than the researchers responsible for those very advances? The chapter authors are experts in their field – many of the advances in plant mitochondrial biology over the past 10 years arise from the primary research output of these authors or members of their teams. I would like to thank them all for their excellent contributions to plant mitochondrial biology, for staying with this project through its long gestation and, in many cases, for being great friends to have within the community.

David C. Logan
June 2017
Tusson, France

References

  1. Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, Small I (2012) A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet 8: e1002910
  2. Cowdry EV (1918) The mitochondrial constituents of protoplasm. Contrib Embryol Carnegie Inst 25: 39–160
  3. De Clercq I, Vermeirssen V, van Aken O, et al. (2013) The membrane‐bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell 25: 3472–3490
  4. Dobzhansky T (1973) Nothing in biology makes sense except in the light of evolution. Am Biol Teach 35: 125–129
  5. Einstein A (1905) On the electrodynamics of moving bodies. Ann der Phys 17: 891–921 www.fourmilab.ch/etexts/einstein/specrel/www/
  6. Finkemeier I, Laxa M, Miguet L, Howden AJM, Sweetlove LJ (2011) Proteins of diverse function and subcellular location are lysine acetylated in Arabidopsis. Plant Physiol 155: 1779–1790
  7. Hagemann M, Bauwe H (2016) Photorespiration and the potential to improve photosynthesis. Curr Opin Chem Biol 35: 109–116
  8. König AC, Hartl M, Pham PA, et al. (2014) The Arabidopsis class II sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism. Plant Physiol 164: 1401–1414
  9. 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
  10. Schwarzländer M, Finkemeier I (2013) Mitochondrial energy and redox signaling in plants. Antioxidants Redox Signal 18: 2122–2144
  11. Schwarzländer M, Logan DC, Johnston IG, Jones NS, Meyer AJ, Fricker MD, Sweetlove LJ (2012a) Pulsing of membrane potential in individual mitochondria: a stress‐induced mechanism to regulate respiratory bioenergetics in Arabidopsis. Plant Cell 24: 1188–1201
  12. Schwarzländer M, Murphy MP, Duchen MR, et al. (2012b) Mitochondrial 'flashes': a radical concept repHined. Trends Cell Biol 22: 503–508
  13. Schwarzländer M, Wagner S, Ermakova YG, et al. (2014) The ‘mitoflash’ probe cpYFP does not respond to superoxide. Nature 514: E12–E14
  14. Skippington E, Barkman TJ, Rice DW, Palmer JD (2015) Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes. Proc Natl Acad Sci USA 112: E3515–3524
  15. Vigani G, Briat JF (2015) Impairment of respiratory chain under nutrient deficiency in plants: does it play a role in the regulation of iron and sulfur responsive genes? Front Plant Sci 6: 1185
  16. Wagner S, Behera S, de Bortoli S, et al. (2015) The EF‐hand Ca2+ binding protein MICU choreographs mitochondrial Ca2+ dynamics in Arabidopsis. Plant Cell 27: 3190–3212