Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effects of Ni2+ and Cu2+ on K+ and H+ currents in lily pollen protoplasts

Maria Breygina A B C * , Denis V. Abramochkin A B * , Nikita Maksimov A and Igor Yermakov A
+ Author Affiliations
- Author Affiliations

A Lomonosov Moscow State University, Leninskiye gory 1-12, Moscow, 119991, Russia.

B Pirogov Russian National Research Medical University, Ostrovitjanova street 1, Moscow, 117997, Russia.

C Corresponding author. Email: pollen-ions@yandex.ru

Functional Plant Biology 44(12) 1171-1177 https://doi.org/10.1071/FP17033
Submitted: 27 January 2017  Accepted: 17 July 2017   Published: 24 August 2017

Abstract

Heavy metals affect plant development and reproduction if they are present in excessive amounts, a situation that is becoming increasingly common. Pollen is a convenient object for pollution assessment as it is in most cases a 2- or 3-cellular organism exposed to the environment. At the same time, pollen is a key stage in the life cycle of seed plants; pollen viability and efficiency of germination are crucial for reproductive success and crop yield. In the present study we reveal for the first time, to our knowledge, targets for heavy metals (Cu2+ and Ni2+) in the pollen grain plasma membrane using the patch-clamp technique. Ni2+ dramatically decreases K+ current in pollen grain protoplasts, whereas Cu2+ does not alter the current density. Instead, Cu2+ strongly enhances H+ current driven by H+-ATPase, whereas Ni2+ fails to affect this current. The short-term treatment with Cu2+ also leads to reactive oxygen species (ROS) accumulation in pollen grain protoplasts but intracellular pH and membrane potential remain unchanged. Ni2+ had no significant effect on ROS content or membrane potential. Thus, plasmalemma K+ channels in pollen grains are sensitive to Ni2+ and H+-ATPase is sensitive to Cu2+, possibly, in a ROS-mediated way. Both metals leave pollen viable since membrane potential is maintained at the control level.

Additional keywords: copper, heavy metal, H+-ATPase, ion channel, nickel.


References

Anjum NA, Singh HP, Khan MIR, Masood A, Per TS, Negi A, Batish DR, Khan NA, Duarte AC, Pereira E, Ahmad I (2015) Too much is bad – an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions. Environmental Science and Pollution Research International 22, 3361–3382.
Too much is bad – an appraisal of phytotoxicity of elevated plant-beneficial heavy metal ions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFyqu73F&md5=0aa7c4cf79c8030a06dcbbe428a6893dCAS |

Breygina MA, Smirnova AV, Matveeva NP, Yermakov IP (2009) Membrane potential changes during pollen germination and tube growth. Cell and Tissue Biology 3, 573–582.
Membrane potential changes during pollen germination and tube growth.Crossref | GoogleScholarGoogle Scholar |

Breygina MA, Matveyeva NP, Andreyuk DS, Yermakov IP (2012a) Transmembrane transport of K+ and Cl– during pollen grain activation in vivo and in vitro. Russian Journal of Developmental Biology 43, 85–93.
Transmembrane transport of K+ and Cl during pollen grain activation in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVCntb8%3D&md5=9ff22ed8ecb27a7d2148828605289123CAS |

Breygina M, Matveyeva N, Polevova S, Meychik N, Nikolaeva Y, Mamaeva A, Yermakov I (2012b) Ni2+ effects on Nicotiana tabacum L. pollen germination and pollen tube growth. BioMetals 25, 1221–1233.
Ni2+ effects on Nicotiana tabacum L. pollen germination and pollen tube growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1OgtLzI&md5=e6a3e724f01bb49b75ad1a356343904eCAS |

Breygina MA, Abramochkin DV, Maksimov NM, Yermakov IP (2016) Hydrogen peroxide affects ion channels in lily pollen grain protoplasts. Plant Biology 18, 761–767.
Hydrogen peroxide affects ion channels in lily pollen grain protoplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1yhtLzI&md5=cdac51321cbfe10dcb1673a57baebe45CAS |

Burzyński M, Kolano E (2003) In vivo and in vitro effects of copper and cadmium on the plasma membrane H+-ATPase from cucumber (Cucumis sativus L.) and maize (Zea mays L.) roots. Acta Physiologiae Plantarum 25, 39–45.
In vivo and in vitro effects of copper and cadmium on the plasma membrane H+-ATPase from cucumber (Cucumis sativus L.) and maize (Zea mays L.) roots.Crossref | GoogleScholarGoogle Scholar |

Cocucci SM, Morgutti S (1986) Stimulation of proton extrusion by K+ and divalent cations (Ni2+, Co2+, Zn2+) in maize root segments. Physiologia Plantarum 68, 497–501.
Stimulation of proton extrusion by K+ and divalent cations (Ni2+, Co2+, Zn2+) in maize root segments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXjtVSqsQ%3D%3D&md5=11b286714fdb7eb5aeac68811e0c516fCAS |

Corem S, Carpaneto A, Soliani P, Cornara L, Gambale F, Scholz-Starke J (2009) Response to cytosolic nickel of slow vacuolar channels in the hyperaccumulator plant Alyssum bertolonii. European Biophysics Journal 38, 495–501.
Response to cytosolic nickel of slow vacuolar channels in the hyperaccumulator plant Alyssum bertolonii.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtF2kt7w%3D&md5=a71e3129a0ee343dc15f2fa1ec864ec5CAS |

Demidchik V (2010) Reactive oxygen species, oxidative stress and plant ion channels. In ‘Ion channels plant stress responses’. (Eds V Demidchik, JMF Maathuis) pp. 207–232. (Springer: Dordrecht, The Netherlands)

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, Sokolik A, Yurin V (1997) The effect of Cu2+ on ion transport systems of the plant cell plasmalemma. Plant Physiology 114, 1313–1325.
The effect of Cu2+ on ion transport systems of the plant cell plasmalemma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsleisbw%3D&md5=4a8c1a6e9f03fa6b2871d081f994d61dCAS |

Fan L-M, Wang Y-F, Wu W-H (2003) Outward K+ channels in Brassica chinensis pollen protoplasts are regulated by external and internal pH. Protoplasma 220, 143–152.
Outward K+ channels in Brassica chinensis pollen protoplasts are regulated by external and internal pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlyrtLk%3D&md5=c4b55c156c7dcb93a33b35684131f9cdCAS |

Fernandes AR, Sa-Correia I (2001) The activity of plasma membrane H+-ATPase is strongly stimulated during Saccharomyces cerevisiae adaptation to growth under high copper stress, accompanying intracellular acidification. Yeast 18, 511–521.
The activity of plasma membrane H+-ATPase is strongly stimulated during Saccharomyces cerevisiae adaptation to growth under high copper stress, accompanying intracellular acidification.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtVehtL8%3D&md5=c06e1a517655a9a70410c11cfad85c97CAS |

Gehwolf R, Griessner M, Pertl H, Obermeyer G (2002) First patch, then catch: Measuring the activity and the mRNA transcripts of a proton pump in individual Lilium pollen protoplasts. FEBS Letters 512, 152–156.
First patch, then catch: Measuring the activity and the mRNA transcripts of a proton pump in individual Lilium pollen protoplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtlGhtbs%3D&md5=3f0de81eabeb2c46a2268b4d0a2b165cCAS |

Gottardini E, Cristofolini F, Paoletti E, Lazzeri P, Pepponi G (2004) Pollen viability for air pollution bio-monitoring. Journal of Atmospheric Chemistry 49, 149–159.
Pollen viability for air pollution bio-monitoring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslemurY%3D&md5=9ddbba9895fb092ca6e1121fe950a413CAS |

Gür N, Topdemir A (2008) Effects of some heavy metals on in vitro pollen germination and tube growth of apricot (Armenica vulgaris Lam.) and cherry (Cerasus avium L.). World Applied Sciences Journal 4, 195–198.

Jammes F, Hu HC, Villiers F, Bouten R, Kwak JM (2011) Calcium-permeable channels in plant cells. The FEBS Journal 278, 4262–4276.
Calcium-permeable channels in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFaksrbM&md5=58193a77d217d74c58b1afc613cec821CAS |

Janicka-Russak M (2011) Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. In ‘Abiotic stress response in plants – physiological, biochemical and genetic perspectives’. (Eds A Shanker, B Venkateswarlu) p. 346. (InTech: Rijeka, Croatia)

Janicka-Russak M, Kabała K, Burzyński M (2012) Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots. Journal of Experimental Botany 63, 4133–4142.
Different effect of cadmium and copper on H+-ATPase activity in plasma membrane vesicles from Cucumis sativus roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSlsLvP&md5=a1cf97d335d3115b4a2946fcc0790a3cCAS |

Matveeva NP, Andreyuk DS, Voitsekh OO, Ermakov IP (2003) Regulatory changes in the intracellular pH and Cl– efflux at early stages of pollen grain germination in vitro. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 50, 318–323.
Regulatory changes in the intracellular pH and Cl efflux at early stages of pollen grain germination in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFyisbs%3D&md5=5fa9869c924956e72394799d69bb16e2CAS |

Mesejo C, Martínez-Fuentes A, Reig C, Rivas F, Agustí M (2006) The inhibitory effect of CuSO4 on citrus pollen germination and pollen tube growth and its application for the production of seedless fruit. Plant Science 170, 37–43.
The inhibitory effect of CuSO4 on citrus pollen germination and pollen tube growth and its application for the production of seedless fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFektbrK&md5=5fa82964af7a8f84318609aa082bc4deCAS |

Michard E, Simon AA, Tavares B, Wudick MM, Feijó JA (2017) Signaling with ions: the keystone for apical cell growth and morphogenesis in pollen tubes. Plant Physiology 173, 91–111.
Signaling with ions: the keystone for apical cell growth and morphogenesis in pollen tubes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXptFKqsr8%3D&md5=64dd0fd1d915be4c4d469d14d51d37ddCAS |

Mohsenzadeh F, Chehregani A (2011) Effect of the heavy metals on developmental stages of ovule, pollen, and root proteins in Reseda lutea L. (Resedaceae). Biological Trace Element Research 143, 1777–1788.
Effect of the heavy metals on developmental stages of ovule, pollen, and root proteins in Reseda lutea L. (Resedaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFSis7fO&md5=5064723d49f117a597afdba5472c5328CAS |

Morgutti S, Ferrari-Bravo P, Marre MT, Cocucci SM (1981) Effects of Ni2+ on proton extrusion and related transport processes and on the transmembrane electrical potential in maize roots. Plant Science Letters 23, 123–128.
Effects of Ni2+ on proton extrusion and related transport processes and on the transmembrane electrical potential in maize roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjvFaj&md5=e98f409aea7d307f939ccd9e435f216fCAS |

Murphy AS, Eisinger WR, Shaff JE, Kochian LV, Taiz L (1999) Early copper-induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux. Plant Physiology 121, 1375–1382.
Early copper-induced leakage of K+ from Arabidopsis seedlings is mediated by ion channels and coupled to citrate efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFyis7k%3D&md5=732e845187186eba7514b65bab347aefCAS |

Pertl H, Pöckl M, Blaschke C, Obermeyer G (2010) Osmoregulation in Lilium pollen grains occurs via modulation of the plasma membrane H+-ATPase activity by 14-3-3 proteins. Plant Physiology 154, 1921–1928.
Osmoregulation in Lilium pollen grains occurs via modulation of the plasma membrane H+-ATPase activity by 14-3-3 proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2jsbfF&md5=aac85b698f182e10e87007ed9d0c35c2CAS |

Pham AN, Xing G, Miller CJ, Waite TD (2013) Fenton-like copper redox chemistry revisited: hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production. Journal of Catalysis 301, 54–64.
Fenton-like copper redox chemistry revisited: hydrogen peroxide and superoxide mediation of copper-catalyzed oxidant production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlslWms7k%3D&md5=2e935ceb557b244c12190e97ffa7aaa6CAS |

Polevova S, Breygina M, Matveyeva N, Yermakov I (2014) Periplasmic multilamellar membranous structures in Nicotiana tabacum L. pollen grains treated with Ni2+ or Cu2+. Protoplasma 251, 1521–1525.
Periplasmic multilamellar membranous structures in Nicotiana tabacum L. pollen grains treated with Ni2+ or Cu2+.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXns1Wlsb8%3D&md5=85999017b68e60c7184fabfb4180d11bCAS |

Rodrigo-Moreno A, Andrés-Colás N, Poschenrieder C, Gunsé B, Peñarrubia L, Shabala S (2013) Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production. Plant, Cell & Environment 36, 844–855.
Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjs1eksrg%3D&md5=adc1d2722b20e767435dacd364e82f65CAS |

Sabrine H, Afif H, Mohamed B, Hamadi B, Maria H (2010) Effects of cadmium and copper on pollen germination and fruit set in pea (Pisum sativum L.). Scientia Horticulturae 125, 551–555.
Effects of cadmium and copper on pollen germination and fruit set in pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1Gnu7w%3D&md5=326f4fc66317efa994a61ef6b9ce1e43CAS |

Serrano R, Cano A, Pestaña A (1985) The plasma membrane ATPase of Dictyostelium discoideum. Biochimica et Biophysica Acta (BBA) – Biomembranes 812, 553–560.
The plasma membrane ATPase of Dictyostelium discoideum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXptFylug%3D%3D&md5=ac466a55af11102861ce37825456a625CAS |

Speranza A, Taddei AR, Gambellini G, Ovidi E, Scoccianti V (2009) The cell wall of kiwifruit pollen tubes is a target for chromium toxicity: alterations to morphology, callose pattern and arabinogalactan protein distribution. Plant Biology 11, 179–193.
The cell wall of kiwifruit pollen tubes is a target for chromium toxicity: alterations to morphology, callose pattern and arabinogalactan protein distribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFWqsro%3D&md5=f1c77b56d05452d927136c1d79a7a48dCAS |

Sze H, Frietsch S, Li X, Bock KW, Harper JF (2006) Genomic and molecular analyses of transporters in the male gametophyte. In ‘Plant cell monographs. Vol. 3’. pp. 71–93. (Springer: Berlin)

Taylor AR, Assmann SM (2001) Apparent absence of a redox requirement for blue light activation of pump current in broad bean guard cells. Plant Physiology 125, 329–338.
Apparent absence of a redox requirement for blue light activation of pump current in broad bean guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjslylsrs%3D&md5=afbb50f5d87861e705b020c840d7965cCAS |

Tuna AL, Bürün B (2002) The effects of heavy metals on pollen germination and pollen tube length in the tobacco plant. Turkish Journal of Biology 26, 109–113.

Viehweger K (2014) How plants cope with heavy metals. Botanical Studies 55, 35
How plants cope with heavy metals.Crossref | GoogleScholarGoogle Scholar |

Wang X, Zhang S, Gao Y, Lü W, Sheng X (2015) Different heavy metals have various effects on Picea wilsonii pollen germination and tube growth. Plant Signaling & Behavior 10, e989015
Different heavy metals have various effects on Picea wilsonii pollen germination and tube growth.Crossref | GoogleScholarGoogle Scholar |

Yu W, Jiang L-H, Zheng Y, Hu X, Luo J, Yang W (2014) Inactivation of TRPM2 channels by extracellular divalent copper. PLoS One 9, e112071
Inactivation of TRPM2 channels by extracellular divalent copper.Crossref | GoogleScholarGoogle Scholar |

Zamponi G, Striessnig J, Koschak A, Dolphin A (2015) The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacological Reviews 67, 821–870.
The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xns1Gms7s%3D&md5=400baf9b977d8865ad20dc7a093bd223CAS |