Mechanism and Interaction of Nanoparticle-Induced Programmed Cell Death in Plants

  • Fatma Yanik
  • Filiz Vardar


Programmed cell death (PCD) is a genetically controlled process which originates during development and under stress conditions. In natural habitats, plants frequently face a variety of environmental stresses because of their sessile nature. Plants have developed alternative adaptive mechanisms in which the cells and tissues undergo PCD under biotic and abiotic stresses, to provide the survival of the whole organism. The rapid development of nanotechnology and wide range usage of nano-sized functional materials will culminate in accumulation of nanoparticles (NPs) in the soil, water, and atmosphere, where their fate and behavior are largely unknown. Therefore, detailed researches on biochemical, physiological, and molecular effects of NPs in living organisms are critically needed. Principally NP-induced PCD responses as a self-defending process should be under consideration, both for principal and adventive perspectives concerning the protection of environment. The aim of this review is to characterize the potential impacts of NPs correlating with the PCD for a better understanding of the toxicity mechanism of NP.


  1. Alemdar A, Sain M (2008) Isolation and characterization of nanofibers from agricultural residues – wheat straw and soy hulls. Bioresour Technol 99:1664–1671PubMedCrossRefGoogle Scholar
  2. Andón FT, Fadell B (2013) Programmed cell death: molecular mechanisms and implications for safety assessment of nanomaterials. Acc Chem Res 46:733–742PubMedCrossRefGoogle Scholar
  3. Anjali CH, Sharma Y, Mukherjee A et al (2012) Neem oil (Azadirachta indica) nanoemulsion – a potent larvicidal agent against Culex quinquefasciatus. Pest Manag Sci 68:158–163PubMedCrossRefGoogle Scholar
  4. Anjum NA, Rodrigo MAM, Moulick A et al (2016) Transport phenomena of nanoparticles in plants and animals/humans. Environ Res 151:233–243PubMedCrossRefGoogle Scholar
  5. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  6. Arora S, Sharma P, Kumar S et al (2012) Gold- nanoparticle induced enhancement in growth and seed yield of Brassica juncea. Plant Growth Regul 66:303–310CrossRefGoogle Scholar
  7. Asli S, Neumann PM (2009) Colloidal suspensions of clay or titanium dioxide nanoparticles can inhibit leaf growth and transpiration via physical effects on root water transport. Plant Cell Environ 32:577–584PubMedPubMedCentralCrossRefGoogle Scholar
  8. Atha DH, Wang H, Petersen EJ et al (2012) Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ Sci Technol 46:1819–1827CrossRefPubMedGoogle Scholar
  9. Balk J, Chew SK, Leaver CJ et al (2003) The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death. Plant J 34:1–11CrossRefGoogle Scholar
  10. Batley GE, Kirby JK, Mclaughlin MJ (2011) Fate and risks of nanomaterials in aquatic and terrestrial environments. Acc Chem Res 46:854–862CrossRefGoogle Scholar
  11. Bayles KW (2014) Bacterial programmed cell death: Making sense of a paradox. Nat Rev Microbiol 12:63–69PubMedPubMedCentralCrossRefGoogle Scholar
  12. Begum P, Ikhtiari R, Fugetsu B (2011) Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. Carbon 49:3907–3019CrossRefGoogle Scholar
  13. Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:MR17–MR71CrossRefPubMedGoogle Scholar
  14. Castiglione MR, Giorgetti L, Cremonini R et al (2014) Impact of TiO2 nanoparticles on Vicia narbonensis L.: potential toxicity effects. Protoplasma 251:1471–1479CrossRefGoogle Scholar
  15. Caverzan A, Casassola A, Brammer SP (2016) Reactive oxygen species and antioxidant enzymes involved in plant tolerance to stress. In: Shanker A (ed) Recent advances and future perspectives. InTech, Croatia, pp 463–480Google Scholar
  16. Cekic FÖ, Ekinci S, İnal MS et al (2017) Silver nanoparticles induced genotoxicity and oxidative stress in tomato plants. Turk J Biol 41:700–707CrossRefGoogle Scholar
  17. Chen J, Liu X, Wang C et al (2015) Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J Hazard Mater 297:173–182PubMedCrossRefGoogle Scholar
  18. Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195–213PubMedCrossRefGoogle Scholar
  19. Coll NS, Vercammen D, Smidler A et al (2010) Arabidopsis type I metacaspases control cell death. Science 330:1393–1397PubMedCrossRefGoogle Scholar
  20. Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cornelis G, Hund-Rinke K, Kuhlbusch T et al (2014) Fate and bioavailability of engineered nanoparticles in soils: a review. Crit Rev Environ Sci Technol 44:2720–2764CrossRefGoogle Scholar
  22. Corredor E, Testillano PS, Coronado MJ et al (2009) Nanoparticle penetration and transport in living pumpkin plants: in situ subcellular identification. BMC Plant Biol 9:45PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dan Y, Zhang W, Xue R (2015) Characterization of gold nanoparticle uptake by tomato plants using enzymatic extraction followed by single particle inductively coupled plasma–mass spectrometry analysis. Environ Sci Technol 49:3007–3014PubMedPubMedCentralCrossRefGoogle Scholar
  24. Danon A, Rotari VI, Gordon A (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis which is mediated by caspase-like activities and which can be suppressed by caspase ınhibitors, p35 and defender against apoptotic death. J Biol Chem 279:779–787PubMedCrossRefGoogle Scholar
  25. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53CrossRefGoogle Scholar
  26. Delorme VGR, McCabe PF, Kim DJ et al (2000) A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiol 123:917–928PubMedPubMedCentralCrossRefGoogle Scholar
  27. Denault JB, Salvesen GS (2002) Caspases: keys in the ignition of cell death. Chem Rev 102:4489–4499PubMedCrossRefGoogle Scholar
  28. Deng YQ, White DC, Xing BS (2014) Interactions between engineered nanomaterials and agricultural crops: implications for food safety. J Zhejiang Univ-Sci 15:552–572CrossRefGoogle Scholar
  29. Diamond M, McCabe PF (2011) Mitochondrial regulation of plant programmed cell death. In: Kemden F (ed) Plant mitochondria. Advances in plant biology. Springer, NewYork, pp 439–465CrossRefGoogle Scholar
  30. Dietz KJ, Herth S (2011) Plant nanotoxicology. Trends Plant Sci 16:582–589PubMedPubMedCentralCrossRefGoogle Scholar
  31. Dimkpa C, McLean J, Latta D et al (2012) CuO and ZnO nanoparticles: phytotoxicity, metal speciation, and induction of oxidative stress in sandgrown wheat. J Nanopart Res 14:1–15CrossRefGoogle Scholar
  32. Domej W, Oettl K, Renner W (2014) Oxidative stress and free radicals in COPD – implications and relevance for treatment. Int J Chron Obstruct Pulmon Dis 9:1207–1224PubMedPubMedCentralCrossRefGoogle Scholar
  33. Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in root. Trends Plant Sci 5:123–127PubMedCrossRefGoogle Scholar
  34. Earnshaw WC, Martins LM, Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates and functions during apoptosis. Annu Rev Biochem 68:383–424PubMedCrossRefGoogle Scholar
  35. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516PubMedPubMedCentralCrossRefGoogle Scholar
  36. EPA (2007) Nanotechnology White Paper. U.S. Environmental Protection Agency Report EPA 100/B-07/001, Washington, DCGoogle Scholar
  37. Faisal M, Saquib Q, Alatar AA et al (2013) Phytotoxic hazards of NiO-nanoparticles in tomato: a study on mechanism of cell death. J Hazard Mater 250–251:318–332PubMedPubMedCentralCrossRefGoogle Scholar
  38. Faisal M, Saquib Q, Alatar AA et al (2016) Cobalt oxide nanoparticles aggravate DNA damage and cell death in eggplant via mitochondrial swelling and NO signaling pathway. Biol Res 49:20PubMedPubMedCentralCrossRefGoogle Scholar
  39. Galluzzi L, Vitale I, Kroemer G (2011) Cell death signaling and anticancer therapy. Front Oncol 1:1–18PubMedPubMedCentralGoogle Scholar
  40. Galluzzi L, Vitale I, Abrams JM et al (2012) Molecular definitions of cell death subroutines: recommendations of the nomenclature committee on cell death. Cell Death Differ 19:107–120PubMedCrossRefGoogle Scholar
  41. Galluzzi L, Bravo-San Pedro JM, Vitale I et al (2015) Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ 22:58–73PubMedCrossRefGoogle Scholar
  42. Gechev TS, Van Breusegem F, Stone JM et al (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101CrossRefPubMedGoogle Scholar
  43. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stres tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedPubMedCentralCrossRefGoogle Scholar
  44. González-Melendi P, Fernández-Pacheco R, Coronado MJ et al (2008) Nanoparticles as smart treatment-delivery systems in plants: assessment of different techniques of microscopy for their visualization in plant tissues. Ann Bot 101:187–195PubMedCrossRefGoogle Scholar
  45. Gottschalk F, Sonderer T, Scholz RW et al (2009) Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ Sci Technol 43:9216–9222CrossRefPubMedGoogle Scholar
  46. Gozuacik D, Kimchi A (2007) Autophagy and cell death. Curr Top Dev Biol 78:217–225PubMedCrossRefGoogle Scholar
  47. Green DR, Galluzzi L, Kroemer G (2011) Mitochondria and the autophagy–inflammation–cell death axis in organismal aging. Science 333:1109–1112PubMedPubMedCentralCrossRefGoogle Scholar
  48. Gunawardena AH (2008) Programmed cell death and tissue remodelling in plants. J Exp Bot 59:445–451PubMedCrossRefGoogle Scholar
  49. Gunawardena AHLA, Greenwood JS, Dengler NG (2004) Programmed cell death remodels lace plant leaf shape during development. Plant Cell 16:60–73PubMedPubMedCentralCrossRefGoogle Scholar
  50. Gunjan B, Zaidi MGH, Sandeep A (2014) Impact of gold nanoparticles on physiological and biochemical characteristics of Brassica juncea. J Plant Biochem Physiol 2:1–6Google Scholar
  51. Hatsugai N, Kuroyanagi M, Yamada K et al (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–858PubMedCrossRefGoogle Scholar
  52. Hatsugai N, Yamada K, Goto-Yamada S et al (2015) Vacuolar processing enzyme in plant programmed cell death. Front Plant Sci 6:234PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776PubMedCrossRefGoogle Scholar
  54. Homaee MB, Ehsanpour AA (2016) Silver nanoparticles and silver ions: oxidative stress responses and toxicity in potato (Solanum tuberosum L) grown in vitro. Hortic Environ Biotechnol 57:544–553CrossRefGoogle Scholar
  55. Hossain Z, Mustafa G, al SKE (2016) Insights into the proteomic response of soybean towards Al2O3, ZnO, and Ag nanoparticles stress. J Hazard Mater 304:291–305PubMedCrossRefGoogle Scholar
  56. Huang X, Stein BD, Cheng H et al (2011) Magnetic virus-like nanoparticles in N. benthamiana plants: a new paradigm for environmental and agronomic biotechnological research. ACS Nano 5:4037–4045PubMedPubMedCentralCrossRefGoogle Scholar
  57. Huang S, Mira MM, Stasolla C (2016) Dying with style: death decision in plant embryogenesis. In: Germaná MA, Lambardi M (eds) In vitro embryogenesis in higher plants. Springer, New York, pp 101–115CrossRefGoogle Scholar
  58. Hussain H, Yi Z, Rookes JE et al (2013) Mesoporous silica nanoparticles as a biomolecule delivery vehicle in plants. J Nanopart Res 15:1–15CrossRefGoogle Scholar
  59. Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57:231–245PubMedCrossRefGoogle Scholar
  60. Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biol 1:274–287CrossRefGoogle Scholar
  61. Jacob F, Vernaldi S, Maekawa T (2013) Evolution and conservation of plant NLR functions. Front Immunol 4:297PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kacprzyk J, Daly CT, Mccabe PF (2011) The botanical dance of death: programmed cell death in plants. In: Kader JC, Delseny M (eds) Advances in botanical research. Elsevier, Burlington, pp 169–261Google Scholar
  63. Kerr JFR, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedPubMedCentralCrossRefGoogle Scholar
  64. Koo Y, Wang J, Zhang Q et al (2015) Fluorescence reports intact quantum dot uptake into roots and translocation to leaves of Arabidopsis thaliana and subsequent ingestion by insect herbivores. Environ Sci Technol 49:626–632PubMedCrossRefGoogle Scholar
  65. Kurepa J, Paunesku T, Vogt S et al (2010) Uptake and distribution of ultrasmall anatase TiO2 alizarin red S nanoconjugates in Arabidopsis thaliana. Nano Lett 10:2296–2302PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kurusu T, Higaki T, Kuchitsu K (2015) Programmed cell death in plant immunity: cellular reorganization, signaling, and cell cycle dependence in cultured cells as a model system. In: Gunawardena AN, McCabe P (eds) Plant programmed cell death. Springer, NewYork, pp 77–96CrossRefGoogle Scholar
  67. Larue C, Laurette J, Herlin-Boime N et al (2012) Accumulation, translocation and impact of TiO2 nanoparticles in wheat (Triticum aestivum spp.) influence of diameter and crystal phase. Sci Total Environ 43:197–208CrossRefGoogle Scholar
  68. Lee WM, An YJ, Yoon H et al (2008) Toxicity and bioavailability of copper nanoparticles to the terrestrial plants mung bean (Phaseolus radiatus) and wheat (Triticum aestivum): plant agar test for water-insoluble nanoparticles. Environ Toxicol Chem 27:1915–1921CrossRefPubMedGoogle Scholar
  69. Leist M, Jaattela M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2:589–598PubMedCrossRefGoogle Scholar
  70. Lin D, Xing B (2007) Phytotoxicity of nanoparticles: inhibition of seed germination and root growth. Environ Pollut 50:243–250CrossRefGoogle Scholar
  71. Lin D, Xing B (2008) Root uptake and phytotoxicity of ZnO nanoparticles. Environ Sci Technol 42:5580–5585PubMedPubMedCentralCrossRefGoogle Scholar
  72. Lin S, Reppert J, Hu Q et al (2009) Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small 5:1128–1132PubMedPubMedCentralCrossRefGoogle Scholar
  73. Liu Q, Zhao Y, Wan Y et al (2010) Study of the inhibitory effect of water-soluble fullerenes on plant growth at the cellular level. ACS Nano 4:5743–5748CrossRefPubMedGoogle Scholar
  74. Lockshin RA, Williams CM (1964) Programmed cell death II: endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. J Insect Physiol 10:643–649CrossRefGoogle Scholar
  75. Lockshin RA, Zakeri Z (2004) Apoptosis, autophagy, and more. Int J Biochem Cell Biol 36:2405–2419PubMedCrossRefGoogle Scholar
  76. López-Moreno ML, Avilés LL, Pérez NG et al (2016) Effect of cobalt ferrite (CoFe2O4) nanoparticles on the growth and development of Lycopersicon lycopersicum (tomato plants). Sci Total Environ 550:45–52CrossRefPubMedGoogle Scholar
  77. Ma X, Geiser-Lee J, Deng Y et al (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061CrossRefPubMedGoogle Scholar
  78. Ma X, Wang Q, Rossi L et al (2016) Multigenerational exposure to cerium oxide nanoparticles: physiological and biochemical analysis reveals transmissible changes in rapid cycling Brassica rapa. Nano Impact 1:46–54Google Scholar
  79. Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49CrossRefGoogle Scholar
  80. Majumdar S, Peralta-Videa JR, Bandyopadhyay S et al (2014) Exposure of cerium oxide nanoparticles to kidney bean shows disturbance in the plant defense mechanisms. J Hazard Mater 278:279–287CrossRefPubMedGoogle Scholar
  81. McCall K (2010) Genetic control of necrosis – another type of programmed cell death. Curr Opin Cell Biol 22:882–888PubMedPubMedCentralCrossRefGoogle Scholar
  82. McMurray TA, Dunlop PSM, Byrne JA (2006) The photocatalytic degradation of atrazine on nanoparticulate TiO2 films. J Photochem Photobiol A 182:43–51CrossRefGoogle Scholar
  83. Meriga B, Reddy BK, Rao KR (2004) Aluminium-induced production of oxygen radicals, lipid peroxidation and DNA damage in seedlings of rice (Oryza sativa). J Plant Physiol 161:63–68PubMedCrossRefGoogle Scholar
  84. Milani N, McLaughlin MJ, Stacey SP (2012) Dissolution kinetics of macronutrient fertilizers coated with manufactured zinc oxide nanoparticles. J Agric Food Chem 60:3991–3998PubMedCrossRefGoogle Scholar
  85. Miralles P, Church TL, Harris AT (2012) Toxicity, uptake, and translocation of engineered nanomaterials in vascular plants. Environ Sci Technol 46:9224–9239CrossRefPubMedGoogle Scholar
  86. Mirzajani F, Askari H, Hamzelou S (2013) Effect of silver nanoparticles on Oryza sativa L and its rhizosphere bacteria. Ecotoxicol Environ Saf 88:48–54PubMedPubMedCentralCrossRefGoogle Scholar
  87. Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248:565–577PubMedCrossRefPubMedCentralGoogle Scholar
  88. Mittler R, Vanderauwera S, Gollery M et al (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498CrossRefPubMedGoogle Scholar
  89. Morales MI, Rico CM, Hernandez-Viezcas JA et al (2013) Toxicity assessment of cerium oxide nanoparticles in cilantro (Coriandrum sativum L.) plants grown in organic soil. J Agric Food Chem 61:6224–6230CrossRefPubMedGoogle Scholar
  90. Mukherjee A, Peralta-Videa JR, Bandyopadhyay S et al (2014) Physiological effects of nanoparticulate ZnO in green peas (Pisum sativum L.) cultivated in soil. Metallomics 6:132–138CrossRefPubMedGoogle Scholar
  91. Nagaonkar D, Shende S, Rai M (2015) Biosynthesis of copper nanoparticles and its effect on actively dividing cells of mitosis in Allium cepa. Biotechnol Prog 31:557–565PubMedCrossRefGoogle Scholar
  92. Nair PMG, Chung IM (2014) Impact of copper oxide nanoparticles exposure on Arabidopsis thaliana growth, root system development, root lignification and molecular level changes. Environ Sci Pollut Res 21:12709–12722CrossRefGoogle Scholar
  93. Nair PMG, Chung M (2015) Physiological and molecular level studies on the toxicity of silver nanoparticles in germinating seedlings of mung bean (Vigna radiata L.). Acta Physiol Plant 37:1719CrossRefGoogle Scholar
  94. Nel AE, Madler L, Velegol D et al (2009) Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8:543–557PubMedCrossRefGoogle Scholar
  95. Nowack B, Bucheli TD (2007) Occurence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22CrossRefPubMedGoogle Scholar
  96. Ouyang W, Liao W, Luo CT et al (2012) Novel foxo1-dependent transcriptional programs control T(reg) cell function. Nature 22:554–559CrossRefGoogle Scholar
  97. Öz-Arslan D, Korkmaz G, Gözüaçık D (2009) Autophagy: a cellular stress and cell death mechanism Otofaji: Bir hücresel stres yanıtı ve ölüm mekanizması. Acıbadem Uni J Health Sci 2:184–194. (In Turkish)Google Scholar
  98. Panda KK, Achary MM, Krishnaveni R (2011) In vitro biosynthesis and genotoxicity bioassay of silver nanoparticles using plants. Toxicol In Vitro 25:1097–1105PubMedPubMedCentralCrossRefGoogle Scholar
  99. Parisi C, Vigani M, Rodríguez-Cerezo E (2015) Agricultural nanotechnologies: what are the current possibilities? Nano Today 10:124–127CrossRefGoogle Scholar
  100. Poborilova Z, Opatrilova R, Babula P (2013) Toxicity of aluminium oxide nanoparticles demonstrated using a BY-2 plant cell suspension culture model. Environ Exp Bot 91:1–11CrossRefGoogle Scholar
  101. Rajeshwari A, Kavitha S, Alex SA et al (2015) Cytotoxicity of aluminum oxide nanoparticles on Allium cepa root tip—effects of oxidative stress generation and biouptake. Environ Sci Pollut Res 22:11057–11066CrossRefGoogle Scholar
  102. Rao S, Shekhawat GS (2016) Phytotoxicity and oxidative stress perspective of two selected nanoparticles in Brassica juncea. 3 Biotech 6:244PubMedPubMedCentralCrossRefGoogle Scholar
  103. Reape TJ, Brogan NP, McCabe PF (2015) Mitochondrion and chloroplast regulation of plant programmed cell death. In: Gunawardena AN, McCabe MF (eds) Plant programmed cell death. Springer, NewYork, pp 33–54CrossRefGoogle Scholar
  104. Reddy PVL, Hernandez-Viezcas JA, Peralta-Videa JR et al (2016) Lessons learned: are engineered nanomaterials toxic to terrestrial plants? Sci Total Environ 568:470–479CrossRefPubMedGoogle Scholar
  105. Rico CM, Majumdar S, Duarte-Gardea M (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59:3485–3498PubMedPubMedCentralCrossRefGoogle Scholar
  106. Rico CM, Morales MI, McCreary R (2013) Cerium oxide nanoparticles modify the antioxidative stress enzyme activities and macromolecule composition in rice seedlings. Environ Sci Technol 47:14110–14118CrossRefPubMedGoogle Scholar
  107. Roduner E (2006) Size matters: why nanomaterials are different. Chem Soc Rev 35:583–592PubMedCrossRefGoogle Scholar
  108. Serag MF, Kaji N, Gaillard C (2011a) Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells. ACS Nano 5:493–499CrossRefPubMedGoogle Scholar
  109. Serag MF, Kaji N, Venturelli E (2011b) Functional platform for controlled subcellular distribution of carbon nanotubes. ACS Nano 5:9264–9270CrossRefPubMedGoogle Scholar
  110. Serag MF, Kaji N, Habuchi S et al (2013) Nanobiotechnology meets plant cell biology: carbon nanotubes as organelle targeting nanocarriers. RSC Adv 3:4856–4862CrossRefGoogle Scholar
  111. Shah K, Kumar RG, Verma S et al (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144CrossRefGoogle Scholar
  112. Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221CrossRefGoogle Scholar
  113. Sharma P, Jha AB, Dubey RS et al (2012a) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot.
  114. Sharma P, Bhatt D, Zaidi MGH et al (2012b) Silver nanoparticle-mediated enhancement in growth and antioxidant status of Brassica juncea. Appl Biochem Biotechnol 167:2225–2233PubMedCrossRefGoogle Scholar
  115. Shaw AK, Hossain Z (2013) Impact of nano-CuO stress on rice (Oryza sativa L.) seedlings. Chemosphere 93:906–915CrossRefPubMedGoogle Scholar
  116. Shaw AK, Ghosh S, Kalaji HM et al (2014) Nano-CuO stress induced modulation of antioxidative defense and photosynthetic performance of Syrian barley (Hordeum vulgare L.). Environ Exp Bot 102:37–47CrossRefGoogle Scholar
  117. Shen CX, Zhang QF, Li J et al (2010) Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am J Bot 97:1602–1609CrossRefPubMedGoogle Scholar
  118. Shi Y (2002) Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 9:459–470PubMedCrossRefGoogle Scholar
  119. Slomberg DL, Schoenfisch MH (2012) Silica nanoparticle phytotoxicity to Arabidopsis thaliana. Environ Sci Technol 46:10247–10254PubMedGoogle Scholar
  120. Song U, Jun H, Waldman B et al (2013) Functional analyses of nanoparticle toxicity: a comparative study of the effects of TiO2 and Ag on tomatoes (Lycopersicon esculentum). Ecotoxicol Environ Safe 93:60–67CrossRefGoogle Scholar
  121. Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16CrossRefGoogle Scholar
  122. Stampoulis D, Saion KS, Jason CW (2009) Assay-dependent phytotoxicity of nanoparticles to plants. Environ Sci Technol 43:9473–9479CrossRefPubMedGoogle Scholar
  123. Strambeanu N, Demetrovici L, Dragos N (2015) Natural sources of nanoparticles. In: Lungu M, Neculae A, Bunoiu M et al (eds) Nanoparticles promises and risks characterization, manipulation, and potential hazards to humanity and the environment. Springer, New York, pp 9–19Google Scholar
  124. Subbenaik SC (2016) Physical and chemical nature of nanoparticles. In: Kole C, Kumar DS, Khodakovskaya MV (eds) Plant nanotechnology principles and practices. Springer, New York, pp 15–27CrossRefGoogle Scholar
  125. Tan X, Lin C, Fugetsu B (2009) Studies on toxicity of multi-walled carbon nanotubes on suspension rice cells. Carbon 47:3479–3487CrossRefGoogle Scholar
  126. Tepfer M, Taylor IE (1981) The permeability of plant cell walls as measured by gel filtration chromatography. Science 213:761–763PubMedCrossRefGoogle Scholar
  127. Torney F, Trewyn BG, Lin VSY et al (2007) Mesoporous silica nanoparticles deliver DNA and chemicals into plants. Nat Nanotechnol 2:295–300PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tripathi DK, Gaur S, Singh S et al (2017) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiol Biochem 110:2–12CrossRefPubMedGoogle Scholar
  129. Vacca RA, Valenti D, Bobba A et al (2006) Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death. Plant Physiol 141:208–219PubMedPubMedCentralCrossRefGoogle Scholar
  130. Vamvakaki V, Chaniotakis NA (2007) Pesticide detection with a liposome-based nano-biosensor. Biosens Bioelectron 22:2848–2853PubMedCrossRefGoogle Scholar
  131. van Doorn WG, Beers EP, Dang JL et al (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246PubMedPubMedCentralCrossRefGoogle Scholar
  132. Vardar F, Ünal M (2012) Ultrastructural aspects and programmed cell death in the tapetal cells of Lathyrus undulatus Boiss. Acta Biol Hung 63:52–66PubMedCrossRefGoogle Scholar
  133. Vercammen D, van de Cotte B, Jaeger GD et al (2004) Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 279:45329–45336PubMedCrossRefGoogle Scholar
  134. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  135. Wang J, Bayles KW (2013) Programmed cell death in plants: lessons from bacteria? Trends Plant Sci 18:133–139PubMedCrossRefGoogle Scholar
  136. Wang B, Feng WY, Zhao YL (2005) Status of study on biological and toxicological effects of nanoscale materials. Sci China Ser B-Chem 48:385–394CrossRefGoogle Scholar
  137. Wang H, Kou X, Pei Z et al (2011a) Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L.) and pumpkin (Cucurbita mixta) plants. Nanotoxicology 5:30–42PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wang S, Kurepa J, Smalle JA (2011b) Ultra- small TiO2 nanoparticles disrupt microtubular networks in Arabidopsis thaliana. Plant Cell Environ 34:811–820PubMedPubMedCentralCrossRefGoogle Scholar
  139. Wang Z, Xu L, Zhao J (2016) CuO nanoparticle interaction with Arabidopsis thaliana: toxicity, parent-progeny transfer, and gene expression. Environ Sci Technol 50:6008–6016CrossRefPubMedGoogle Scholar
  140. Watanabe N, Lam E (2005) Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem 280:14691–14699PubMedCrossRefGoogle Scholar
  141. Wild E, Jones KC (2009) Novel method for the direct visualization of in vivo nanomaterials and chemical interactions in plants. Environ Sci Technol 43:5290–5294CrossRefPubMedGoogle Scholar
  142. Wituszyńska W, Karpiński S (2013) Programmed cell death as a response to high light, UV and drought stress in plants. In: Vahdati K (ed) Abiotic stress plant responses and applications in agriculture. InTech, Croatia, pp 207–246Google Scholar
  143. Woltering EJ, van der Bent A, Hoeberichts FA (2002) Do plant caspases exist? Plant Physiol 130:1764–1769PubMedPubMedCentralCrossRefGoogle Scholar
  144. Wu JJ, Poon KY, Channual JC et al (2012) Association between tumor necrosis factor inhibitor therapy and myocardial infarction risk in patients with psoriasis. Arch Dermatol 148:1244–1250PubMedCrossRefGoogle Scholar
  145. Yang L, Watts DJ (2005) Particle surface characteristics may play an important role in phytotoxicity of alumina nanoparticles. Toxicol Lett 158:122–132CrossRefPubMedPubMedCentralGoogle Scholar
  146. Yanik F, Vardar F (2015) Toxic effects of aluminum oxide Al2O3 nanoparticles on root growth and development in Triticum aestivum. Water Air Soil Pollut 226:296–309CrossRefGoogle Scholar
  147. Yanik F, Aytürk Ö, Vardar F (2017) Programmed cell death evidence in wheat (Triticum aestivum L.) roots induced by aluminum oxide (Al2O3) nanoparticles. Caryologia 70:112–119CrossRefGoogle Scholar
  148. Zhai G, Walters KS, Peate DW et al (2014) Transport of gold nanoparticles through plasmodesmata and precipitation of gold ions in woody poplar. Environ Sci Technol Lett 1:146–151PubMedPubMedCentralCrossRefGoogle Scholar
  149. Zhang Z, He X, Zhang H et al (2011) Uptake and distribution of ceria nanoparticles in cucumber plants. Metallomics 3:816–822PubMedPubMedCentralCrossRefGoogle Scholar
  150. Zhao L, Peng B, Hernandez-Viezcas JA et al (2012a) Stress response and tolerance of Zea mays to CeO2 nanoparticles: cross talk among H2O2, heat shock protein, and lipid peroxidation. ACS Nano 6:9615–9622PubMedPubMedCentralCrossRefGoogle Scholar
  151. Zhao L, Peralta-Videa JR, Ren M et al (2012b) Transport of Zn in a sandy loam soil treated with ZnO NPs and uptake by corn plants: electron microprobe and confocal microscopy studies. Chem Eng J 184:1–8CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Fatma Yanik
    • 1
  • Filiz Vardar
    • 1
  1. 1.Science and Arts Faculty, Department of BiologyMarmara UniversityIstanbulTurkey

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