Molecular Mechanisms of Gravity Perception and Signal Transduction

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Molecular Mechanisms of Gravity Perception and Signal Transduction Molecular mechanisms of gravity perception and signal transduction in plants Yaroslav Kolesnikov, Serhiy Kretynin, Igor Volotovsky, Elizabeth Kordyum, Eric Ruelland, Volodymyr Kravets To cite this version: Yaroslav Kolesnikov, Serhiy Kretynin, Igor Volotovsky, Elizabeth Kordyum, Eric Ruelland, et al.. Molecular mechanisms of gravity perception and signal transduction in plants. Protoplasma, Springer Verlag, 2016, 253 (4), pp.987-1004. 10.1007/s00709-015-0859-5. hal-02165055 HAL Id: hal-02165055 https://hal.archives-ouvertes.fr/hal-02165055 Submitted on 25 Jun 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Molecular mechanisms of gravity perception and signal transduction in plants Yaroslav Kolesnikov, Serhiy Kretynin, Igor Volotovsky, Elizabeth Kordyum, Eric Ruelland, Volodymyr Kravets To cite this version: Yaroslav Kolesnikov, Serhiy Kretynin, Igor Volotovsky, Elizabeth Kordyum, Eric Ruelland, et al.. Molecular mechanisms of gravity perception and signal transduction in plants. Protoplasma, Springer Verlag, 2016, 253 (4), pp.987-1004. 10.1007/s00709-015-0859-5. hal-02165055 HAL Id: hal-02165055 https://hal.archives-ouvertes.fr/hal-02165055 Submitted on 25 Jun 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW ARTICLE Molecular mechanisms of gravity perception and signal transduction in plants 1 & 1 & 2 & Yaroslav S. Kolesnikov Serhiy V. Kretynin Igor D. Volotovsky 3 4,5 1 Elizabeth L. Kordyum & Eric Ruelland & Volodymyr S. Kravets Received: 26 March 2015 /Accepted: 13 July 2015 Abstract Gravity is one of the environmental cues that direct changes, membrane transport, vacuolar biogenesis mechanisms, plant growth and development. Recent investigations of different or nuclear events. These events culminate in changes in gene gravity signalling pathways have added complexity to how we expression and auxin lateral redistribution in gravity response think gravity is perceived. Particular cells within specific organs sites. The possible integration of these signalling events with or tissues perceive gravity stimulus. Many downstream signal- amyloplast movements or with other perception mechanisms is ling events transmit the perceived information into subcellular, discussed. Further investigation is needed to understand how biochemical, and genomic responses. They are rapid, non-geno- plants coordinate mechanisms and signals to sense this important mic, regulatory, and cell-specific. The chain of events may pass physical factor. by signalling lipids, the cytoskeleton, intracellular calcium levels, protein phosphorylation-dependent pathways, proteome Keywords Gravity . Signalling . Phospholipase . Calcium . Cytoskeleton . Phosphorylation * Volodymyr S. Kravets Abbreviations [email protected] ADK1 Adenosine kinase 1 Igor D. Volotovsky PI-PLC Phosphoinositide-specific phospholipase C [email protected] IP3 Inositol-1,4,5-trisphosphate Elizabeth L. Kordyum PIP5К Phosphatidylinositol monophosphate 5-kinase [email protected] PI-4,5-P2 Phosphatidylinositol-4,5-bisphosphate Eric Ruelland AtInsP5tase Arabidopsis thaliana inositol polyphosphate 5- [email protected] phosphatase PI Phosphatidylinositol 1 Department of Molecular Mechanisms of Cell Metabolism TOC Translocon of outer envelope Regulation, Institute of Bioorganic Chemistry and Petrochemistry, PA Phosphatidic acid National Academy of Sciences of Ukraine, Murmanska St., 1, PLD Phospholipase D Kiev 02094, Ukraine 2 PP Protein phosphatase Institute of Biophysics and Cell Engineering, National Academy of PDK1 Phosphoinositide-dependent protein kinase Sciences of Belarus, Academycheskaya St., 27, Minsk 220072, Belarus ROS Reactive oxygen species 3 SGR Shoot gravitropic response Department of Cell Biology and Anatomy, Institute of Botany, National Academy of Sciences of Ukraine, Tereschenkivska St., 2, Kyiv 01004, Ukraine 4 Université Paris-Est Créteil, Institut d’Ecologie et des Sciences de Introduction l’Environnement, Paris, France 5 Institut d’Ecologie et des Sciences de l’Environnement, Centre The spatial orientation of immobile higher plants in the gravita- National de la Recherche Scientifique, Paris, France tional field is mainly determined by gravitropism and phototropism. This orientation mobilizes physiological activity with secondary growth, cambium may be suggested to be a that results in differential growth. There are three main phases in gravisensing site (Coutand et al. 2014). Stamens, plumules, the gravitropic response: perception of a gravitational stimulus, fruits, and leaves are also sensitive to gravity, but their transduction of a signal, and the resulting differential growth that statocytes are less studied (Philosoph-Hadas et al. 2015). causes bending. Roots show positive gravitropism, growing in Statocytes thus transform a physical signal, gravity, into bio- the direction of a gravitational vector, and stems show negative chemical and physiological ones. The physiological signal is a gravitropism, growing in the direction opposite to the gravitation- change in auxin concentration that is first initiated in root cap al vector. cells by the rapid downward movement of the PIN3/PIN7 To begin this reflection on gravitropism, it is useful to get auxin transporter. The differences in auxin level are further an anatomical and cellular overview of the whole response. transmitted by other auxin transporters (PIN2) to the respon- Gravitropism starts with gravity susception. Amyloplasts ap- sive elongation zones (Feraru et al. 2015; Friml et al. 2002; pear to act as gravity sensors in statocytes, the specialized Kleine-Vehn et al. 2010; Rahman et al. 2010)(Fig.1). This graviperceptive cells, to fulfill a statolithic function by leads to differential growth on opposite sides of the root that sedimenting in the direction of the gravitational vector to the causes its bending. lower part of a cell. The gravitropically responsive apical parts Gravity perception and signal transduction have been ex- of alga Chara globularis rhizoids contain statoliths, compart- tensively studied for a long time. Different models of gravity ments filled with crystallites of barium sulphate (Sievers et al. signal perception have been proposed and tested: the starch 1991). In mosses, gravity perception and gravitropic bending statolith, the ligand-receptor, and the hydrostatic pressure are both carried out in the same cell, an apical cell of the models. Possible roles of the cytoskeleton, the plasmalemma chloronema. Amylochloroplasts containing large starch grains control center, calcium ions and other messengers, and the in this cell are believed to play the role of statoliths (Demkiv related gene activity were considered from the outset (Sack et al. 1998; Walker and Sack 1990). In higher plants, the sites 1997; Sievers et al. 1991). The field has seen many break- of gravity perception and reaction are spatially separated. In throughs and developments in recent years. The specific roles roots, statocytes are cells of the central zone of the root cap of signalling lipids and phospholipases, cytoskeleton, calci- columella. In stems, statocytes are localized in the endoder- um, protein phosphorylation, and transcription factors in grav- mis, particularly in hypocotyls, epicotyls, inflorescences, ity action and signalling can now be discussed. flower stalks, peduncles, gynophores, and in leaf petioles in dicots. In pistil, they are located in cells along the inner cortex layers below the epidermis. In monocot stems, they are also Models of gravity perception observed in bundle sheath of internodal pulvini, coleoptiles, and in stem leaf sheath (Blancaflor and Masson 2003; There are many hypotheses to explain the mechanisms of Kitazawa et al. 2005;Lietal.2013;Manoetal.2006; gravity perception by higher plants (Fig. 2). The conventional Philosoph-Hadas et al. 2015; Shimizu et al. 2005). In organs concept of gravity perception with statoliths, the starch- Fig. 1 Sites of gravity perception and response in different organs: a gravity perception in roots; b gravity perception and response in stems Molecular mechanisms of gravity perception and signalling Fig. 2 Integrated model of known gravity signalling pathways in plant cells. DAG diacylglycerol, IP3 inositol trisphosphate, IP6 inositol hexacisphosphate, L ligand, ECM extracellular matrix, PA phosphatidic acid, PA-PLA1 phosphatidic acid-specific phos- pholipase A1, PIP2 phos- phatidylinositol bisphosphate, PIPK phosphatidylinositol phos- phate kinase, PK protein kinase, PLC phospholipase C, PLD phospholipase D, PP protein phosphatase, PDK1 phosphoinositide-dependent
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