Early and long-term responses of cucumber cells to high cadmium concentration are modulated by nitric oxide and reactive oxygen species

• Autorzy: Piterkova J. , Lubova L. , Navratilova B. , Sedlarova M. , Petrivalsky M.
• Języki publikacji: EN

Abstrakty

EN

Plants are increasingly exposed to heavy metal pollution in the environment. Cadmium (Cd), a non-essential metal, is known to exert strong phytotoxic effects. The aim of the present study was to examine the role of nitric oxide (NO), reactive nitrogen (RNS) and reactive oxygen (ROS) species in the responses of cucumber (Cucumis sativus) cell culture to high Cd concentration. We observed that the early responses to Cd included enhanced levels of NO, RNS and ROS and the induction of cell death, whereas the levels of both RNS and ROS were suppressed as a long-term response to Cd. The Cd-induced increase of NO level was localized in the chloroplasts, while increased ROS and RNS levels were observed in the cytoplasm. We employed an NO scavenger, an NO synthase inhibitor and an NO donor to evaluate the involvement of RNS and ROS in the responses of C. sativus cells to Cd. The observed changes in cell viability and growth were not related to changes in NO, RNS and ROS levels. Long-term Cd exposure inhibited cell division and de-differentiation as assessed by microcallus formation. We conclude that increased NO level belongs to the early responses of plant cells to high Cd concentration and is associated with an NO synthase-like enzyme activity, whereas decreased cell viability and division in long-term Cd treatment are related to interferences with NO signalling and decreased level of both RNS and ROS.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2015
• Tom: 37
• Numer: 02
• Opis fizyczny: Article: 19 [12 p.], fig.,ref.

Twórcy

autor

Piterkova J.

• Department of Biochemistry, Faculty of Science, Palacky University, Slechtitelu 11, 78371 Olomouc, Czech Republic

autor

Lubova L.

• Department of Biochemistry, Faculty of Science, Palacky University, Slechtitelu 11, 78371 Olomouc, Czech Republic

autor

Navratilova B.

• Department of Botany, Faculty of Science, Palacký University, Faculty of Science, Palacky University, Slechtitelu 11, 78371 Olomouc, Czech Republic

autor

Sedlarova M.

• Department of Botany, Faculty of Science, Palacký University, Faculty of Science, Palacky University, Slechtitelu 11, 78371 Olomouc, Czech Republic

autor

Petrivalsky M.

• Department of Biochemistry, Faculty of Science, Palacky University, Slechtitelu 11, 78371 Olomouc, Czech Republic

Bibliografia

• Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876–887
• Balcerczyk A, Soszynski M, Bartosz G (2005) On the specificity of 4-amino-5-methylamino-20,70-difluorofluorescein as a probe for nitric oxide. Free Radic Biol Med 39:327–335
• Barroso JB, Corpas FJ, Carreras A, Rodriguez-Serrano M, Esteban FJ, Fernandez-Ocana A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, Del Rio LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793
• Barroso JB, Valderrama R, Corpas FJ (2013) Immunolocalization of S-nitrosoglutathione, S-nitrosoglutathione reductase and tyrosine nitration in pea leaf organelles. Acta Physiol Plant 35:2635–2640
• Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biol Szeged 49:9–12
• Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signalling in plants. Annu Rev Plant Biol 59:21–39
• Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315
• Bočová B, Huttová J, Liptáková Ĺ , Mistrík I, Ollé M, Tamás L (2012) Impact of short-term cadmium treatment on catalase and ascorbate peroxidase activities in barley root tips. Biol Plantarum 56:724–728
• Chen F, Wang F, Sun H, Cai Y, Mao W, Zhang G, Vincze E, Wu F (2010) Genotype-dependent effect of exogenous nitric oxide on Cd-induced changes in antioxidative metabolism, ultrastructure, and photosynthetic performance in barley seedlings (Hordeum vulgare). J Plant Growth Regul 29:394–408
• Cho UH, Park JO (2000) Mercury-induced oxidative stress in tomato seedlings. Plant Sci 156:1–9
• Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486
• Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88:1707–1719
• Corpas FJ, Barroso JB, Del Río LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci 6:145–150
• De Gara L, de Pinto MC, Tommasi F (2003) The antioxidant systems vis-á-vis reactive oxygen species during plant–pathogen interaction. Plant Physiol Biochem 41:863–870
• De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, di Toppi LS, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228
• Debeaujon I, Branchard M (1992) Induction of somatic embryogenesis and calogenesis from cotyledons and leaf protoplast—derived colonies of melon (Cucumis melo L.). Plant Cell Rep 12:37–40
• Drazkiewicz M, Skórzinka-Polit E, Krupa Z (2004) Copper-induced stress and antioxidant defence in Arabidopsis thaliana. Biometals 17:379–387
• Fan HF, Du CX, Ding L, Xu YL (2013) Effects of nitric oxide on the germination of cucumber seeds and antioxidant enzymes under salinity stress. Acta Physiol Plant 35:2707–2719
• Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistence. Proc Nat Acad Sci USA 102:8054–8059
• Gajdová J, Navrátilová B, Smolná J, Lebeda A (2007) Factors affecting protoplast isolation and cultivation of Cucumis spp. J App Bot Food Qual 81:1–6
• Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Plein JP, Ranjeva R, Montillet JL (2006) Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxity. Plant Cell Environ 29:1956–1969
• Gas E, Flores-Pérez U, Sauret-Güeto S, Rodríguez-Concepción M (2009) Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21:18–23
• Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261
• Gomes A, Fernandes E, Lima JL (2006) Use of fluorescence probes for detection of reactive nitrogen species: a review. J Fluoresc 16:119–139
• Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494
• Gzyl J, Przymusiński R, Gwóźdź EA (2009) Ultrastructure analysis of cadmium-tolerant and -sensitive cell lines of cucumber (Cucumis sativus L.). Plant Cell Tissue Organ Cult 99:227–232
• Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11
• He H, He L, Gu M (2014) The diversity of nitric oxide function in plant responses to metal stress. Biometals 27:219–228
• Heikal L, Martin GP, Dailey LA (2009) Characterisation of the decomposition behaviour of S-nitrosoglutathione and a new class of analogues: S-nitrosophytochelatins. Nitric Oxide 20:157–165
• Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227–238
• Illéš P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluška F, Ovečka M (2006) Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J Exp Bot 57:4201–4213
• Iori V, Pietrini F, Massacci A, Zacchini M (2012) Induction of metal binding compounds and antioxidative defence in callus cultures of two black poplar (P. nigra) clones with different tolerance to cadmium. Plant Cell Tissue Organ Cult 108:17–26
• Ismail GSM (2012) Protective role of nitric oxide against arsenicinduced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303–1311
• Jasid S, Simontacchi M, Bartoli CB, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255
• Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017
• Kopyra M, Stachon-Wilk M, Gwóźdź EA (2006) Effects of endogenous nitric oxide on the antioxidant capacity of cadmiumtreated soybean cell suspension. Acta Physiol Plant 28:525–536
• Korshunova YO, Eide D, Clark WG, Guerinot ML, Pakrasi HB (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol Biol 40:37–44
• Krežel A, Bal W (2004) Contrasting effects of metal ions on S-nitrosoglutathione, related to coordination equilibria: GSNO decomposition assisted by Ni(II) vs stability increase in the presence of Zn(II) and Cd(II). Chem Res Toxicol 17:392–403
• Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330
• Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220:731–739
• Mur LAJ, Carver TLW, Prats E (2006) NO way to live; the various roles of nitric oxide in plant–pathogen interactions. J Exp Bot 57:489–505
• Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35
• Ortega-Villasante C, Rellán-Alvarez R, Del Campo FF, Carpena-Ruiz RO, Hernández LE (2005) Cellular damage induced by cadmium and mercury in Medicago sativa. J Exp Bot 56:2239–2251
• Ortega-Villasante C, Hernández LE, Rellán-Alvarez R, Del Campo FF, Carpena-Ruiz RO (2007) Rapid alteration of cellular redox homeostasis upon exposure to cadmium and mercury in alfalfa seedlings. New Phytol 176:96–107
• Ötvös K, Pasternak TP, Miskolczi P, Domoki M, Dorjgotov D, Szucs A, Bottka S, Dudits D, Feher A (2005) Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J 43:849–860
• Papadakis KA, Roubelakis-Angelakis AK (2002) Oxidative stress could be responsible for the recalcitrance of plant protoplasts. Plant Physiol Biochem 40:549–559
• Petřivalský M, Vaníčková P, Ryzí M, Navrátilová B, Piterková J, Sedlářová M, Luhová L (2012) The effects of reactive nitrogen and oxygen species on the regeneration and growth of cucumber cells from isolated protoplasts. Plant Cell Tissue Organ Cult 108:237–249
• Piterková J, Petřivalský M, Luhová L, Mieslerová B, Sedlářová M, Lebeda A (2009) Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Mol Plant Pathol 10:201–213
• Qiu ZB, Guo JL, Zhang MM, Lei MY, Li ZL (2013) Nitric oxide acts as a signal molecule in microwave pretreatment induced cadmium tolerance in wheat seedlings. Acta Physiol Plant 35:65–73
• Ramos I, Esteban E, Lucena JJ, Gárate A (2002) Cadmium uptake and subcellular distribution in plants of Lactuca sp. Cd-Mn interaction. Plant Sci 162:761–767
• Rivetta A, Negrini N, Cocucci M (1997) Involvement of Ca2+- calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20:600–608
• Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544
• Rodríguez-Serrano M, Romero-Puertas MC, Pazmino DM, Testillano PS, Risueno MC, Del Río LA, Sandalio LM (2009a) Cellular response of pea plants to cadmium toxicity: cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229–243
• Rodríguez-Serrano M, Romero-Puertas MC, Sparkes I, Hawes C, Del Río LA, Sandalio LM (2009b) Peroxisome dynamics in Arabidopsis plants under oxidative stress induced by cadmium. Free Radic Biol Med 47:1632–1639
• Romanov GA, Lomin SN, Rakova NU, Heyl A, Schmülling T (2008) Does NO play a role in cytokinin signal transduction? FEBS Lett 582:874–880
• Romero-Puertas MC, McCarthy T, Sandalio LM, Palma JM, Corpas FJ, Gómez M, Del Río LA (1999) Cadmim toxicity and oxidative metabolism of pea leaf peroxisomes. Free Radic Res 31:25–31
• Sandalio LM, Dalurzo HC, Gomez M, Romero-Puertas MC, Del Rio LA (2011) Cadmium–induced changes in the growth and antioxidative metabolism of pea plants. J Exp Bot 52:2115–2126
• Sedlářová M, Petřivalský M, Piterková J, Kočířová J, Luhová L, Lebeda A (2011) Influence of nitric oxide and reactive oxygen species on development of lettuce downy mildew in Lactuca spp. Eur J Plant Pathol 129:267–280
• Singh HP, Batish DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167
• Šírová J, Sedlářová M, Piterková J, Luhová L, Petřivalský M (2011) The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci 181:560–571
• Song L, Yue L, Zhao H, Hou M (2013) Protection effect of nitric oxide on photosynthesis in rice under heat stress. Acta Physiol Plant 35:3323–3333
• Tao YM, Chen YZ, Tan T, Liu XC, Yang DL, Liang SC (2012) Comparison of antioxidant responses to cadmium and lead in Bruguiera gymnorrhiza seedlings. Biol Plantarum 56:149–152
• Tewari RK, Hahn EJ, Paek KY (2008) Modulation of copper toxicityinduced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171–181
• Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331
• Tian SK, Lu LL, Yang XE, Huang HG, Wang K, Brown PH (2012) Root adaptations to cadmium-induced oxidative stress contribute to Cd tolerance in the hyperaccumulator Sedum alfredii. Biol Plantarum 56:344–350
• Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, Del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461
• Verma K, Mehta SK, Shekhawat GS (2013) Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals 26:255–269
• Wang YS, Yang YM (2005) Nitric oxide reduces aluminium toxicity by preventing oxidative stress in root of Cassia tora L. Plant Cell Physiol 46:1915–1923
• Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in abiotic stress response. Trends Plant Sci 9:244–253
• Wardman P (2007) Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 43:995–1022
• Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31:622–631
• Wiseman DA, Wells SM, Wilham J, Hubbard M, Welker JE, Black SM (2006) Endothelial response to stress from exogenous Zn2+ resembles that of NO-mediated nitrosative stress, and is protected by MT-1 overexpression. Am J Physiol Cell Physiol 291:555–568
• Xiong J, Lu H, Lu K, Duan Y, An L, Zhu C (2009a) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610
• Xiong J, An L, Lu H, Zhu C (2009b) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765
• Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20
• Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction of reactive oxygen species in plant cells. Plant Physiol 128:63–72
• Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inze D, Delledonne M, Van Breusegem F (2006) Nitric oxide- and hydrogen peroxide responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:404–411
• Zangger K, Öz G, Haslinger E, Kunert O, Armitage IM (2001) Nitric oxide selectively releases metals from the amino-terminal domain of metallothioneins: potential role at inflammatory sites. FASEB J 15:1303–1305

Identyfikatory

DOI

10.1007/s11738-014-1756-9