Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Emerging evidence for potential role of Ca2+-ATPase-mediated calcium accumulation in symbiosomes of infected root nodule cells

Igor M. Andreev
+ Author Affiliations
- Author Affiliations

Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya st. 35, Moscow 127276, Russia. Email: pmembrane@ippras.ru

Functional Plant Biology 44(10) 955-960 https://doi.org/10.1071/FP17042
Submitted: 6 February 2017  Accepted: 28 May 2017   Published: 31 July 2017

Abstract

Symbiosomes are organelle-like compartments responsible for nitrogen fixation in infected nodule cells of legumes, which are formed as a result of symbiotic association of soil bacteria rhizobia with certain plant root cells. They are virtually the only source of reduced nitrogen in the Earth’s biosphere, and consequently, are of great importance. It has been proven that the functioning of symbiosomes depends to a large extent on the transport of various metabolites and ions – most likely including Ca2+ – across the symbiosome membrane (SM). Although it has been well established that this cation is involved in the regulation of a broad spectrum of processes in cells of living organisms, its role in the functioning of symbiosomes remains obscure. This is despite available data indicating both its transport through the SM and accumulation within these compartments. This review summarises the results obtained in the course of studies on the given aspects of calcium behaviour in symbiosomes, and on this basis gives a possible explanation of the proper functional role in them of Ca2+.

Additional keywords: bacteroid, calcium signaling, calcium signalling, symbiosome, symbiosome membrane.


References

Andreev IM, Dubrovo PN, Krylova VV, Andreeva IN, Koren’kov VD, Sorokin EM, Izmailov SF (1997) Characterization of ATP-hydrolyzing and ATP-driven proton-translocating activities associated with the peribacteroid membrane from root nodules of Lupinus luteus L. Journal of Plant Physiology 151, 563–569.
Characterization of ATP-hydrolyzing and ATP-driven proton-translocating activities associated with the peribacteroid membrane from root nodules of Lupinus luteus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXns12gtbk%3D&md5=0c54cd92d411ee9fb393cfd6e3962b78CAS |

Andreev IM, Dubrovo PN, Krylova VV, Izmailov SF (1998) Calcium uptake by symbiosomes and the peribacteroid membrane vesicles isolated from yellow lupin root nodules. Journal of Plant Physiology 151, 203–211.

Andreev IM, Dubrovo PN, Krylova VV, Izmailov SF (1999) Functional identification of ATP-driven Ca2+ pump in the peribacteroid membrane of broad bean root nodules. FEBS Letters 447, 49–52.
Functional identification of ATP-driven Ca2+ pump in the peribacteroid membrane of broad bean root nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVClsr8%3D&md5=7836ea2ae3b3bfcee6fe0a7463b244a2CAS |

Andreev IM, Andreeva IN, Dubrovo PN, Krylova VV, Kozharinova GM, Izmailov SF (2001) Calcium status of yellow lupin symbiosomes as a potential regulator of their nitrogenase activity: the role of the peribacteroid membrane. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 48, 308–317.
Calcium status of yellow lupin symbiosomes as a potential regulator of their nitrogenase activity: the role of the peribacteroid membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjvVShtrw%3D&md5=25413fa7b2f13e7245cf487414716a19CAS |

Andreeva IN, Andreev IM, Dubrovo PN, Kozharinova GM, Krylova VV, Izmailov SF (1999) Calcium stores in symbiosomes from yellow lupin root nodules. Journal of Plant Physiology 155, 357–363.
Calcium stores in symbiosomes from yellow lupin root nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXms1Gmu7s%3D&md5=ee35343d341e80426c8688d8103dad9cCAS |

Blackstone NW (2015) The impact of mitochondrial endosymbiosis on the evolution of calcium signaling. Cell Calcium 57, 133–139.
The impact of mitochondrial endosymbiosis on the evolution of calcium signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVSgu73I&md5=b31d046878374c4cf358a87f0e95379eCAS |

Carafoli E (2005) Calcium – a universal carrier of biological signals. FEBS Journal 272, 1073–1089.
Calcium – a universal carrier of biological signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXit12rtbk%3D&md5=8f74e7aa6377433532a8ab1ee1b09347CAS |

Carafoli E, Krebs J (2016) Why calcium? How calcium became the best communicator. The Journal of Biological Chemistry 291, 20 849–20 857.
Why calcium? How calcium became the best communicator.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1amurjE&md5=0d0a363959d5540000572056673dba62CAS |

Chen T-H, Huang T-C, Chow T-J (1988) Calcium requirement in nitrogen fixation in the cyanobacterium Synechococcus RF-1. Planta 173, 253–256.
Calcium requirement in nitrogen fixation in the cyanobacterium Synechococcus RF-1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhtV2gtrs%3D&md5=7bdbf6f48969d6b68d0b486a191a5dbaCAS |

Clarke VC, Loughin PC, Day DA, Smith PMC (2015a) Transport processes of the legume symbiosome membrane. Frontiers in Plant Science 5, 699

Clarke VC, Loughin PC, Garvin A, Chen C, Brear EM, Day DA, Smith PMC (2015b) Proteomic analysis of the soybean symbiosome identifies new symbiotic proteins. Molecular & Cellular Proteomics 14, 1301–1322.
Proteomic analysis of the soybean symbiosome identifies new symbiotic proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXotVWjsb8%3D&md5=5953e0cd7602a5e33171aecfefd1b286CAS |

del Arco A, Contreras L, Pardo B, Satrustegui J (2016) Calcium regulation of mitochondrial carriers. Biochimica et Biophysica Acta 1863, 2413–2421.
Calcium regulation of mitochondrial carriers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XltlOqs7w%3D&md5=72c1d256667ec1daeb52e3b936bc6dd3CAS |

Denton RM (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochimica et Biophysica Acta 1787, 1309–1316.
Regulation of mitochondrial dehydrogenases by calcium ions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVentb%2FO&md5=ae7b04c166111b7e47c8372f2c8568d6CAS |

Domínguez DC, Guragain M, Patrauchan M (2015) Calcium binding proteins and calcium signaling in prokaryotes. Cell Calcium 57, 151–165.
Calcium binding proteins and calcium signaling in prokaryotes.Crossref | GoogleScholarGoogle Scholar |

Emerich DW, Krishnan HB (2014) Symbiosomes: temporary moonlighting organelles. The Biochemical Journal 460, 1–11.
Symbiosomes: temporary moonlighting organelles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvFCjtLs%3D&md5=3a592d926411e9ade54659622803babfCAS |

Engelmann B, Schumacher U, Duhm J (1990) Use of chlortetracycline fluorescence for the detection of Ca storing intracellular vesicles in normal human erythrocytes. Journal of Cellular Physiology 143, 357–363.
Use of chlortetracycline fluorescence for the detection of Ca storing intracellular vesicles in normal human erythrocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXksFKgu7c%3D&md5=914da2365d8578ef18543d4ca7f47a57CAS |

Felle HHE, Kondorosi E, Kondorosi A, Schultze M (1999) Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the Nod factor signal in alfalfa. Plant Physiology 121, 273–280.
Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the Nod factor signal in alfalfa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGltr0%3D&md5=f745d89c09cdd4f654786ee5f71796ecCAS |

Gazarini ML, Thomas AP, Pozzan T, Garcia CRS (2003) Calcium signaling in a low calcium environment: how the intracellular malaria parasite solves the problem. Journal of Cell Biology 161, 103–110.
Calcium signaling in a low calcium environment: how the intracellular malaria parasite solves the problem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVait70%3D&md5=20f68049002e480b309ddc197d50a471CAS |

Heyen BJ, Alsheikh MK, Smith EA, Torvik CF, Seals DF, Randal SK (2002) The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiology 130, 675–687.
The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVKnt7Y%3D&md5=ae74c7f9bd75c94f0149dc0753c44e8eCAS |

Jacobson J, Duchen MR (2004) Interplay between mitochondria and cellular calcium signaling. Molecular and Cellular Biochemistry 256/257, 209–218.
Interplay between mitochondria and cellular calcium signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSjs7jK&md5=ba80ed2560b81a67e4b0f68eb1c3fb2eCAS |

Jones HE, Holland IB, Campbell AK (2002) Direct measurements of free Ca2+ shows different regulation of Ca2+ between the periplasm and the cytosol of Escherichia coli. Cell Calcium 32, 183–192.
Direct measurements of free Ca2+ shows different regulation of Ca2+ between the periplasm and the cytosol of Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xos1ymt7s%3D&md5=fa88643c207dc2ccd9b73483830af580CAS |

Kazmierczak J, Kempe S, Kremer B (2013) Calcium in the early evolution of living systems: biohistorical approach. Current Organic Chemistry 17, 1738–1750.
Calcium in the early evolution of living systems: biohistorical approach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsV2itbvL&md5=cea6af718a15aec464f295e9eea7eecdCAS |

Kleist TJ, Luan S (2016) Constant change: dynamic regulation of membrane transport by calcium signaling networks keeps plants in tune with their environment. Plant, Cell & Environment 39, 467–481.
Constant change: dynamic regulation of membrane transport by calcium signaling networks keeps plants in tune with their environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xit1Kru70%3D&md5=420f7d732dde5be6706096b1a97f6e04CAS |

Krylova VV, Andreev IM, Andreeva IN, Dubrovo PN, Kozharinova GM, Izmailov SF (2002) Verapamil-sensitive calcium transporter in the peribacteroid membrane from Vicia faba root nodules. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 49, 746–753.
Verapamil-sensitive calcium transporter in the peribacteroid membrane from Vicia faba root nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xotl2rsrk%3D&md5=2fd2496c4d93965ffd80d46716994adfCAS |

Krylova VV, Andreev IM, Zartdinova R, Izmailov SF (2013) Biochemical characteristics of the Ca2+ pumping ATPase in the peribacteroid membrane from broad bean root nodules. Protoplasma 250, 531–538.
Biochemical characteristics of the Ca2+ pumping ATPase in the peribacteroid membrane from broad bean root nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksF2nsL8%3D&md5=a378cde264bf4dc31ef92a9dc6d12315CAS |

Krylova VV, Zartdinova RF, Andreev IM, Izmailov SF (2016) Ca2+/H+ antiport as a possible mechanism of the Ca2+-translocating ATPase functioning in vesicles of bean root nodule’s symbiosome membrane. Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology 10, 218–222.

Leborgne-Castel N, Bouhidel K (2014) Plasma membrane protein trafficking in plant-microbe interactions: a plant cell point of view. Frontiers in Plant Science 5, 735
Plasma membrane protein trafficking in plant-microbe interactions: a plant cell point of view.Crossref | GoogleScholarGoogle Scholar |

Liu J, Miller SS, Graham M, Bucciarelli B, Catalano CM, Sherrier DJ, Samac DA, Ivashuta S, Fedorova M, Matsumoto P, Gantt JS, Vance CP (2006) Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiology 141, 167–177.
Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVyqtrc%3D&md5=60a1d31dda84c99557eed00a2c60674eCAS |

Magalon A, Arias-Cartin R, Walburger A (2012) Supramolecular organization in prokaryotic respiratory systems. Advances in Microbial Physiology 61, 217–266.
Supramolecular organization in prokaryotic respiratory systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotFeitrg%3D&md5=33137f594ce6867bb29ca47605616745CAS |

Nomura H, Shiina T (2014) Calcium signaling in plant endosymbiotic organelles: mechanism and role in physiology. Molecular Plant 7, 1094–1104.
Calcium signaling in plant endosymbiotic organelles: mechanism and role in physiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlejtbnI&md5=1e9319577f5eeebb047d27f8165f9f64CAS |

Oke V, Long SR (1999) Bacteroid formation in the Rhizobium-legume symbiosis. Current Opinion in Microbiology 2, 641–646.
Bacteroid formation in the Rhizobium-legume symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2Fns12iuw%3D%3D&md5=b5751d6e4208da35e34698005bb95789CAS |

Oldroyd GE, Downie JA (2004) Calcium, kinases and nodulation signaling in legumes. Nature Reviews. Molecular Cell Biology 5, 566–576.
Calcium, kinases and nodulation signaling in legumes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1Ortbw%3D&md5=8aafd1c9e8971b802bce17bea1b36ee8CAS |

Ouyang L-J, Whelan J, Weaver CD, Roberts DM, Day DA (1991) Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. FEBS Letters 293, 188–190.
Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhvVClug%3D%3D&md5=6323cb2559c2141323ad390d0a41f592CAS |

Plattner H, Verkhratsky A (2015) The ancient roots of calcium signaling evolutionary tree. Cell Calcium 57, 123–132.
The ancient roots of calcium signaling evolutionary tree.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkslWhtA%3D%3D&md5=0c16bc556b50934b4dd8636e4e0725bbCAS |

Plieth C (2005) Calcium: just another regulator in the machinery of life? Annals of Botany 96, 1–8.
Calcium: just another regulator in the machinery of life?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnsVejtrc%3D&md5=a01fb4db4ee8ed243439002319f5f6cfCAS |

Rizzuto R, Marchi S, Bonora M, Aguiari P, Bononi A, De Stefani D, Giorgi C, Leo S, Rimessi A, Siviero R, Zecchini E, Pinton P (2009) Ca2+ transfer from the ER to mitochondria: when, how and why. Biochimica et Biophysica Acta 1787, 1342–1351.
Ca2+ transfer from the ER to mitochondria: when, how and why.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVentb%2FL&md5=de191c1b54b94570c8e9e82646f5c110CAS |

Roberts DM, Tyerman SD (2002) Voltage-dependent cation channels permeable to NH4 +, K+ and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus. Plant Physiology 128, 370–378.
Voltage-dependent cation channels permeable to NH4 +, K+ and Ca2+ in the symbiosome membrane of the model legume Lotus japonicus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVSrurw%3D&md5=c7142c9cf8a5a6d44aa961f86b4373c9CAS |

Rocha AG, Vothknecht UC (2012) The role of calcium in chloroplasts – an intriguing and unresolved puzzle. Protoplasma 249, 957–966.
The role of calcium in chloroplasts – an intriguing and unresolved puzzle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVCjtL%2FI&md5=ee7f432024053decc9debfe18a25bb46CAS |

Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Annual Review of Plant Physiology and Plant Molecular Biology 48, 493–523.
Metabolite transport across symbiotic membranes of legume nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1emt7g%3D&md5=469a96c7415332a89d150d3ee38b45ddCAS |

Udvardi M, Pool PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annual Review of Plant Biology 64, 781–805.
Transport and metabolism in legume-rhizobia symbioses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosFSku7w%3D&md5=07593e274bf3a377b09a7aacdf31119bCAS |

Verhaert J, Vanderleyden J, Michiels J (2005) Bacterial endocytic systems in plants and animals: Ca2+ as a common theme? Critical Reviews in Plant Sciences 24, 283–308.
Bacterial endocytic systems in plants and animals: Ca2+ as a common theme?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtV2gsr7E&md5=1320e802d0a0de3a6c0a1c31f25785a2CAS |

Weaver CD, Crombie B, Stacey G, Roberts DM (1991) Calcium-dependent phosphorylation of symbiosome membrane proteins from nitrogen-fixing soybean nodules. Plant Physiology 95, 222–227.
Calcium-dependent phosphorylation of symbiosome membrane proteins from nitrogen-fixing soybean nodules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpvVertQ%3D%3D&md5=a45b11dd15dd281480eab0c8c7aa4de3CAS |

Wick SM, Hepler PK (1982) Selective localization of intracellular Ca2+ with potassium pyroantimonate. Journal of Histochemistry and Cytochemistry 30, 1190–1204.
Selective localization of intracellular Ca2+ with potassium pyroantimonate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XlsVWjt7Y%3D&md5=6bd4709a78bd5fa7127c80e8e6c5b4b2CAS |

Yamaguchi T, Aharon GS, Sottosanto JB, Blumwald E (2005) Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proceedings of the National Academy of Sciences of the United States of America 102, 16107–16112.
Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1WqsrzJ&md5=1f9295ef51a41d07fb3646cba672ef7cCAS |

Yuasa K, Maeshima M (2000) Purification, properties, and molecular cloning of a novel Ca2+-binding protein in radish vacuoles. Plant Physiology 124, 1069–1078.
Purification, properties, and molecular cloning of a novel Ca2+-binding protein in radish vacuoles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlWru7o%3D&md5=c15f8802aa97d41e19bbcda87ca257ddCAS |