Unravelling the plant signalling machinery: an update on the cellular and genetic basis of plant signal transduction
Vadim Demidchik A B D , Frans Maathuis C D and Olga Voitsekhovskaja B DA Department of Plant Cell Biology and Bioengineering, Biological Faculty, Belarusian State University, 4 Independence Avenue, Minsk, 220030, Belarus.
B Laboratory of Molecular and Ecological Physiology, Komarov Botanical Institute, Russian Academy of Sciences, 2 Professora Popova Street, 197376 St Petersburg, Russia.
C Department of Biology, University of York, York YO10 5DD, UK.
D Corresponding authors. Emails: dzemidchyk@bsu.by; fjm3@york.ac.uk; ovoitse@binran.ru
This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 19–23 June 2016.
Functional Plant Biology 45(2) 1-8 https://doi.org/10.1071/FP17085
Submitted: 28 March 2017 Accepted: 27 May 2017 Published: 10 July 2017
Abstract
Plant signalling is a set of phenomena that serves the transduction of external and internal signals into physiological responses such as modification of enzyme activity, cytoskeleton structure or gene expression. It operates at the level of cell compartments, whole cells, tissues, organs or even plant communities. To achieve this, plants have evolved a network of signalling proteins including plasma membrane receptors and ion transporters, cascades of kinases and other enzymes as well as several second messengers such as cytosolic calcium (Ca2+), reactive oxygen/nitrogen species (ROS/RNS), cyclic nucleotides (cAMP and cGMP) and others. Overall, these systems recognise and decode environmental signals and co-ordinate ontogeny programs. This paper summarises recent progress in the field of plant signalling, which was a major theme of the 4th International Symposium on Plant Signalling and Behaviour, 2016, in Saint Petersburg, Russia. Several novel hypotheses and concepts were proposed during this meeting. First, the concept of ROS-Ca2+ hubs has found further evidence and acceptance. This concept is based on reciprocal activation of NADPH oxidases by cytosolic Ca2+ on the one hand, and Ca2+-permeable channels that are activated by NADPH-produced ROS. ROS-Ca2+ hubs enhance the intensity and duration of originally weak Ca2+ and ROS signals. Hubs are directly involved in ROS- and Ca2+-mediated physiological reactions, such as stress response, growth, programmed cell death, autophagy and long-distance signalling. Second, recent findings have widened the list of cyclic nucleotide-regulated processes and strengthened the biochemical basis of cyclic nucleotide biochemistry by exploring cyclase activities of new receptors such as the Phytosulfokine Receptor 1, the pathogen peptide 1 receptor (atPepR1), the brassinosteroid BRI1 receptor and the cell wall-associated kinase like 10. cGMP and cAMP signalling has demonstrated strong link to Ca2+ signalling, via cyclic nucleotide-gated Ca2+-permeable ion channels (CNGCs), and to ROS and RNS via their nitrosylated forms. Third, a novel role for cytosolic K+ as a regulator of plant autophagy and programmed cell death has emerged. The cell death-associated proteases and endonucleases were demonstrated to be activated by a decrease of cytosolic K+ via ROS-induced stimulation of the plasma membrane K+ efflux channel GORK. Importantly, the origin of ROS for induction of autophagy and cell death varies in different tissues and comprises several pools, including NADPH oxidases, peroxidases, photosynthetic and respiratory electron-transporting chains and peroxisomal enzymes. The peroxisome pool is the ‘latest’ addition to established cellular ROS-producing machineries and is dependent on the state and abundance of catalase in this compartment. Finally, new aspects of phytohormone signalling, such as regulation of root hydraulic pressure by abscisic acid and rate of mitosis by cytokinins, as well as localising cytokinin receptors in endoplasmic reticulum, are reported. Other observations suggest that melatonin is a hormone-like substance in plants, because it targets Ca2+, ROS and RNS.
Additional keywords: abscisic acid, Arabidopsis thaliana, autophagy, calcium signalling, cyclic nucleotide-gated channels, ion channels, melatonin, photosynthesis, programmed cell death, reactive nitrogen species, reactive oxygen species, ROS-calcium hub.
References
Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541–550.| Heat stress: an overview of molecular responses in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOgt7bF&md5=6ec334cbccda4dc96390c894fa94b19bCAS |
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141, 391–396.
| Production and scavenging of reactive oxygen species in chloroplasts and their functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksbY%3D&md5=7a3a6822275bb38148260965cbcbe873CAS |
Ashton AR (2011) Guanylyl cyclase activity in plants? Proceedings of the National Academy of Sciences of the United States of America 108, E96
| Guanylyl cyclase activity in plants?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtlKrs7k%3D&md5=c24ce847b03e0546a3d5404538d73475CAS |
Bäurle I (2016) Plant heat adaptation: priming in response to heat stress. F1000Research 5, 694
| Plant heat adaptation: priming in response to heat stress.Crossref | GoogleScholarGoogle Scholar |
Bhawana , Miller JL, Cahoon AB (2014) 3D Plant cell architecture of Arabidopsis thaliana (Brassicaceae) using focused ion beam-scanning electron microscopy. Applications in Plant Sciences 2, 1300090
| 3D Plant cell architecture of Arabidopsis thaliana (Brassicaceae) using focused ion beam-scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Bushby AJ, P’ng KM, Young RD, Pinali C, Knupp C, Quantock AJ (2011) Imaging three-dimensional tissue architectures by focused ion beam scanning electron microscopy. Nature Protocols 6, 845–858.
| Imaging three-dimensional tissue architectures by focused ion beam scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFyqtLo%3D&md5=838db8fd85daea8b721c0550ea6040f0CAS |
Caesar K, Thamm AM, Witthöft J, Elgass K, Huppenberger P, Grefen C, Horak J, Harter K (2011) Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. Journal of Experimental Botany 62, 5571–5580.
| Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFCitrfE&md5=7a2d966c9a18047a76f8af94694ad078CAS |
Chichkova NV, Galiullina RA, Mochalova LV, Trusova SV, Sobri ZM, Gallois P, Vartapetian AB (2017) Arabidopsis thaliana phytaspase: identification and peculiar properties. Functional Plant Biology
| Arabidopsis thaliana phytaspase: identification and peculiar properties.Crossref | GoogleScholarGoogle Scholar |
Corpas FJ, Barroso JB (2013) Nitro‐oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytologist 199, 633–635.
| Nitro‐oxidative stress vs oxidative or nitrosative stress in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSrurfJ&md5=37aa6483db022d36edaf3b05a46c3486CAS |
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environmental and Experimental Botany 109, 212–228.
| Mechanisms of oxidative stress in plants: from classical chemistry to cell biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaiur%2FM&md5=f8db8a141307c54edb23849b86ec517bCAS |
Demidchik V, Shabala S (2017) Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’. Functional Plant Biology
| Mechanisms of cytosolic calcium elevation in plants: the role of ion channels, calcium extrusion systems and NADPH oxidase-mediated ‘ROS-Ca2+ Hub’.Crossref | GoogleScholarGoogle Scholar |
Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM (2003) Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells. Journal of Cell Science 116, 81–88.
| Free oxygen radicals regulate plasma membrane Ca2+- and K+-permeable channels in plant root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtF2lsA%3D%3D&md5=eede4b7865478d7d00a7ac9b79d5f2d2CAS |
Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. Journal of Cell Science 123, 1468–1479.
| Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1KmtL0%3D&md5=1ea5171aa64a36e614598240e5e6d344CAS |
Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014) Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. Journal of Experimental Botany 65, 1259–1270.
| Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htb4%3D&md5=bf101b7b23972cc5786358931a472e29CAS |
Demidchik V, Voitsekhovskaja O, Tyutereva E, Pozhvanov G (2016) ‘Proceeding of fourth international symposium on plant signaling and behavior.’ (SINEL Co. Ltd: Saint Petersburg Russia)
Demidchik V, Tyutereva EV, Voitsekhovskaja OV (2017) The role of ion disequilibrium in induction of programmed cell death and autophagy by environmental stresses in roots. Functional Plant Biology
| The role of ion disequilibrium in induction of programmed cell death and autophagy by environmental stresses in roots.Crossref | GoogleScholarGoogle Scholar |
Erland LAE, Saxena PK, Murch SJ (2017) Melatonin in plant signalling and behaviour. Functional Plant Biology
| Melatonin in plant signalling and behaviour.Crossref | GoogleScholarGoogle Scholar |
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiology 171, 1606–1615.
| ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVGlsbvF&md5=3554a9536f036809202c146d38e53cf4CAS |
Gorshkov O, Mokshina N, Ibragimova N, Ageeva M, Gogoleva N, Gorshkova T (2017) Phloem fibers as motors of gravitropic behaviour of flax plants: level of transcriptome. Functional Plant Biology
| Phloem fibers as motors of gravitropic behaviour of flax plants: level of transcriptome.Crossref | GoogleScholarGoogle Scholar |
Hackenberg T, Juul T, Auzina A, Gwiżdż S, Małolepszy A, Van Der Kelen K, Dam S, Bressendorff S, Lorentzen A, Roepstorff P, Nielsen KL, Jørgensen J-E, Hofius D, Van Breusegem F, Petersen M, Andersen SU (2013) Catalase and NO CATALASE ACTIVITY1 promote autophagy-dependent cell death in Arabidopsis. The Plant Cell 25, 4616–4626.
| Catalase and NO CATALASE ACTIVITY1 promote autophagy-dependent cell death in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVOqsrw%3D&md5=995f0228916a0b5ca8014d6fec5612acCAS |
Ishioka N, Tanimoto S (1990) Involvement of cyclic AMP in adventitious bud initiation of Torenia stem segments. Plant & Cell Physiology 31, 91–97.
Isner JC, Maathuis FJM (2011) Measurement of cellular cGMP in plant cells and tissues using the endogenous fluorescent reporter FlincG. The Plant Journal 65, 329–334.
| Measurement of cellular cGMP in plant cells and tissues using the endogenous fluorescent reporter FlincG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsl2mt70%3D&md5=02aed215c07b726b1750c9e1f866bd00CAS |
Isner JC, Maathuis FJM (2017) cGMP signalling in plants: from enigma to main stream. Functional Plant Biology
Ivanov VB, Filin AN (2017) Cytokinins regulate root growth through its action on meristematic cells proliferation but not on the transition to differentiation. Functional Plant Biology
| Cytokinins regulate root growth through its action on meristematic cells proliferation but not on the transition to differentiation.Crossref | GoogleScholarGoogle Scholar |
Ivanov BN, Borisova-Mubarakshina MM, Kozuleva MA (2017) Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signaling by hydrogen peroxide. Functional Plant Biology
| Formation mechanisms of superoxide radical and hydrogen peroxide in chloroplasts, and factors determining the signaling by hydrogen peroxide.Crossref | GoogleScholarGoogle Scholar |
Jain P, Bhatla SC (2017) Molecular mechanisms accompanying nitric oxide signalling through tyrosine nitration and S-nitrosylation of proteins in plants. Functional Plant Biology
| Molecular mechanisms accompanying nitric oxide signalling through tyrosine nitration and S-nitrosylation of proteins in plants.Crossref | GoogleScholarGoogle Scholar |
Joudoi T, Shichiri Y, Kamizono N, Akaike T, Sawa T, Yoshitake J, Yamada N, Iwai S (2013) Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. The Plant Cell 25, 558–571.
| Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVOisr4%3D&md5=1546377952d3a9bbb7ea3a399283598aCAS |
Kisnieriene V, Lapeikaite I, Pupkis V (2017) Electrical signaling in Nitellopsis obtusa: potential biomarkers of biologically active compounds. Functional Plant Biology
| Electrical signaling in Nitellopsis obtusa: potential biomarkers of biologically active compounds.Crossref | GoogleScholarGoogle Scholar |
Komarova AV, Sukhov VS, Bulychev AA (2017) Cyclosis-mediated long distance communications of chloroplasts in giant cells of Characeae. Functional Plant Biology
| Cyclosis-mediated long distance communications of chloroplasts in giant cells of Characeae.Crossref | GoogleScholarGoogle Scholar |
Lomin SN, Myakushina YA, Arkhipov DV, Leonova OG, Popenko VI, Schmülling T, Romanov GA (2017) Studies of cytokinin receptor–phosphotransmitter interaction provide evidences for the initiation of cytokinin signaling in the endoplasmic reticulum. Functional Plant Biology
| Studies of cytokinin receptor–phosphotransmitter interaction provide evidences for the initiation of cytokinin signaling in the endoplasmic reticulum.Crossref | GoogleScholarGoogle Scholar |
Luo S, Zhang X, Wang J, Jiao C, Chen Y, Shen Y (2017) Plant ion channels and transporters in herbivory-induced signaling. Functional Plant Biology
| Plant ion channels and transporters in herbivory-induced signaling.Crossref | GoogleScholarGoogle Scholar |
Mithofer A (2016) Local and systemic calcium and phytohormone signaling in biotic interactions. In ‘Proceedings of fourth international symposium on plant signaling and behavior’. pp. 99. (SINEL Co. Ltd: Saint Petersburg, Russia)
Pottosin I, Dobrovinskaya O (2017) Two-pore cation (TPC) channel: not a shorthanded one. Functional Plant Biology
| Two-pore cation (TPC) channel: not a shorthanded one.Crossref | GoogleScholarGoogle Scholar |
Reagan BC, Kim PJ-Y, Perry PD, Dunlap JR, Burch-Smith TM (2017) Spatial distribution of organelles in leaf cells and soybean root nodules revealed by focused ion beam-scanning electron microscopy. Functional Plant Biology
| Spatial distribution of organelles in leaf cells and soybean root nodules revealed by focused ion beam-scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Santisree P, Bhatnagar-Mathur P, Sharma KK (2017) Molecular insights into the functional role of nitric oxide (NO) as a signal for plant responses in chickpea. Functional Plant Biology
| Molecular insights into the functional role of nitric oxide (NO) as a signal for plant responses in chickpea.Crossref | GoogleScholarGoogle Scholar |
Sineshchekov VA, Koppel LA, Bolle C (2017) Two native types of phytochrome A, phyAʹ and phyAʹʹ, differ by the state of phosphorylation at the N-terminus as revealed by fluorescence investigations of the Ser/Ala mutant of rice phyA expressed in transgenic Arabidopsis. Functional Plant Biology
Stahlberg R (2006) Historical overview on plant neurobiology. Plant Signaling & Behavior 1, 6–8.
| Historical overview on plant neurobiology.Crossref | GoogleScholarGoogle Scholar |
Tsyganova AV, Kitaeva AB, Tsyganov VE (2017) Cell differentiation in nitrogen-fixing nodules hosting symbiosomes. Functional Plant Biology
| Cell differentiation in nitrogen-fixing nodules hosting symbiosomes.Crossref | GoogleScholarGoogle Scholar |
Tyutereva EV, Dobryakova KS, Schiermeyer A, Shishova MF, Pawlowski K, Demidchik V, Reumann S, Voitsekhovskaja OV (2017) The levels of peroxisomal catalase protein and activity modulate the onset of cell death in tobacco BY-2 cells via ROS levels and autophagy. Functional Plant Biology
| The levels of peroxisomal catalase protein and activity modulate the onset of cell death in tobacco BY-2 cells via ROS levels and autophagy.Crossref | GoogleScholarGoogle Scholar |
Veselov DS, Sharipova GV, Veselov SY, Kudoyarova G (2017) Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand. Functional Plant Biology
| Rapid changes in root HvPIP2;2 aquaporins abundance and ABA concentration are required to enhance root hydraulic conductivity and maintain leaf water potential in response to increased evaporative demand.Crossref | GoogleScholarGoogle Scholar |
Vodeneev V, Mudrilov M, Akinchits E, Balalaeva I, Sukhov V (2017) Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus. Functional Plant Biology
| Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus.Crossref | GoogleScholarGoogle Scholar |
Volkov AG (2012) ‘Plant electrophysiology. Methods and cell electrophysiology.’ (Springer: Berlin)
Volkov AG, Nyasani EK (2017) Sunpatiens Compact Hot Coral: memristors in flowers. Functional Plant Biology
| Sunpatiens Compact Hot Coral: memristors in flowers.Crossref | GoogleScholarGoogle Scholar |
Yu L, Wan F, Dutta S, Welsh S, Liu Z-H, Freundt E, Baehrecke EH, Lenardo M (2006) Autophagic programmed cell death by selective catalase degradation. Proceedings of the National Academy of Sciences of the United States of America 103, 4952–4957.
| Autophagic programmed cell death by selective catalase degradation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjsVGls7k%3D&md5=47c4f54203eb23a58f0bd1063ebc0675CAS |
