Skip to main content
Log in

Influence of seed priming with iron and/or zinc in the nucleolar activity and protein content of bread wheat

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Seed priming with iron (Fe) and/or zinc (Zn) can overcome the reduced availability of these micronutrients in soils and crops, but suitable dosages should be predetermined. Nucleolus responds to stress, such as cytotoxicity, with alterations perceivable by cytogenetic analyses. This work intends to study how seed priming with Fe and/or Zn affects the nucleolar activity in roots and the total soluble protein content in the flour of bread wheat cv. ‘Jordão’. Seven priming treatments with 0 mg L−1 to 8 mg L−1 of Fe and/or Zn were performed. In all treatments, each metaphase cell presented a maximum of six nucleolar organizer regions positively stained with silver nitrate (Ag-NORs). Also, a maximum number of six nucleoli per nucleus were observed in all treatments, except in the hydroprimed seeds (used as control) that showed a maximum of five nucleoli, probably due to nucleolar fusion. Irregular interphases were frequent in treatments with the highest dosage of micronutrients (8 mg L−1 Fe and/or 8 mg L−1 Zn). The nucleolar area reduced (p < 0.001) as the number of nucleoli increased, and it was lower in treatments with a combination of Fe and Zn. However, the combinations of Fe and Zn showed the highest concentrations of total soluble protein (p ≤ 0.001). Although a reduced nucleolar area represents low ribosomal RNA gene transcription and ribosomal production, the significant increase of the number of nucleoli in the seeds primed with Fe and Zn enhanced the total soluble protein content as compared to the hydroprimed seeds (control) probably due to an increase of nucleolar surface-to-volume ratio that improved the protein synthesis. Overall, this work revealed that priming of bread wheat seeds with suited dosages of Fe and Zn can improve the nutritional value of flour, and the nucleolar number, morphology, and area can be useful biomarkers in cytotoxicity studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ajouri A, Asgedom H, Becker M (2004) Seed priming enhances germination and seedling growth of barley under conditions of P and Zn deficiency. J Plant Nutr Soil Sci 167:630–636

    Article  Google Scholar 

  • Al-Baker EA, Oshin M, Hutchison CJ, Kill IR (2005) Analysis of UV-induced damage and repair in young and senescent human dermal fibroblasts using the comet assay. Mech Ageing Dev 126:664–672

    Article  CAS  PubMed  Google Scholar 

  • Angelov D, Bondarenko VA, Almagro S, Menoni H, Mongélard F, Hans F, Mietton F, Studitsky VM, Hamiche A, Dimitrov S, Bouvet P (2006) Nucleolin is a histone chaperone with FACT-like activity and assists remodelling of nucleosomes. EMBO J 25:1669–1679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aquila AD, Spada P (1992) Regulation of protein synthesis in germination wheat embryos under polyethylene glycol and salt stress. Seed Sci Res 2:75–80

    Article  Google Scholar 

  • Arkhipchuk VV, Garanko NN (2002) A novel nucleolar biomarker in plant and animal cells for assessment of substance cytotoxicity. Environ Toxicol 17(3):187–194

    Article  CAS  PubMed  Google Scholar 

  • Balcerzak L, Glińska S, Godlewski M (2011) The reaction of Lupinus angustifolius L. root meristematic cell nucleoli to lead. Protoplasma 248:353–361

    Article  CAS  PubMed  Google Scholar 

  • Balmer Y, Vensel WH, Dupont FM, Buchanan BB, Hurkman WJ (2006) Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J Exp Bot 57:1591–1602

    Article  CAS  PubMed  Google Scholar 

  • Bam RK, Kumaga FK, Ori K, Asiedu EA (2006) Germination: vigour and dehydrogenase activity of naturally aged rice (Oryza sativa L.) seeds soaked in potassium and phosphorus. Asian J Plant Sci 5:948–955

    Article  CAS  Google Scholar 

  • Basra SMA, Farooq M, Tabassum R (2005) Physiological and biochemicalaspects of seed vigor enhancement treatments in fine rice (Oryza sativa L.). Seed Sci Technol 33:623–628

    Article  Google Scholar 

  • Belousov MV, Mashkina OS, Popov VN (2012) Cytogenetic response of Scots pine (Pinus sylvestris Linnaeus, 1753) (Pinaceae) to heavy metals. Comp Cytogenet 6:93–106

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhowal JG (1972) Nucleolar chromosomes in wheat. Z Pflanzenzücht 68:253–257

    Google Scholar 

  • Borg S, Brinch-Pedersen H, Tauris B, Holm P (2009) Iron transport, deposition and bioavailability in the wheat and barley grain. Plant Soil 325:15–24

    Article  CAS  Google Scholar 

  • Borrill P, James CM, Balk J, Miller JA, Sanders D, Cristobal U (2014) Biofortification of wheat grain with iron and zinc: integrating novel genomic resources and knowledge from model crops. Front Plant Sci 21(5):53. https://doi.org/10.3389/fpls.2014.00053

    Article  Google Scholar 

  • Boudet J, Buitnink J, Hoekstra FA, Rogniaux H, Larré C, Satour P, Leprince O (2006) Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140:1418–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouis HE, Saltzman A (2017) Improving nutrition through biofortification: a review of evidence from HarvestPlus, 2003 through 2016. Glob Food Sec 12:49–58

    Article  PubMed  PubMed Central  Google Scholar 

  • Boulon S, Westman BJ, Hutten S, Boisvert F-M, Lamond AI (2010) The nucleolus under stress. Mol Cell 40(2):216–227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bray CM, Davison PA, Ashraf M, Taylor RM (1989) Biochemical events during osmopriming of leek seed. Ann Appl Biol 102:185–193

    Google Scholar 

  • Briggs DE (1987) Endosperm breakdown and its regulation in germinating barley. In: Pollock JRH (ed) Brewing science, vol 3. Academic, London, pp 441–532

    Google Scholar 

  • Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I (2002) Plant nutrition research: priorities to meet human needs for food in sustainable ways. Plant Soil 247:3–24

    Article  CAS  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

    Article  CAS  Google Scholar 

  • Caldelas C, Weiss DJ (2017) Zinc homeostasis and isotopic fractionation in plants: a review. Plant Soil 411:17–46

    Article  CAS  Google Scholar 

  • Carvalho A, Polanco C, Lima-Brito J, Guedes-Pinto H (2010) Differential rRNA genes expression in hexaploid wheat related to NOR methylation. Plant Mol Biol Rep 28:403–412

    Article  CAS  Google Scholar 

  • Carvalho AIF, Morais F, Coutinho JP, Guedes-Pinto HP, Lima-Brito JE (2011) Cytogenetics, morphological, yield and molecular characterization of the Portuguese bread wheat ‘Barbela’. Plant Biosyst 145:540–552

    Article  Google Scholar 

  • Carvalho A, Leal F, Matos M, Lima-Brito J (2018) Effects of heat stress in the leaf mitotic cell cycle and chromosomes of four wine-producing grapevine varieties. Protoplasma 255(6):1725–1740

    Article  PubMed  Google Scholar 

  • Castiglione MR, Giorgetti L, Geri C, Cremonini R (2011) The effects of nano-TiO2 on seed germination, development and mitosis of root tip cells of Vicia narbonensis, L. and Zea mays, L. J Nanopart Res 13:2443–2449

    Article  CAS  Google Scholar 

  • Catálogo Nacional de Variedades de Espécies Agrícolas e Hortícolas (2018) Ministério da Agricultura, Florestas e Desenvolvimento Rural, Direção-Geral de Alimentação e Veterinária (Ed.), Lisboa, Portugal, 66 p., ISSN 0871-0295

  • Coutinho J, Maçãs B, Almeida AS, Gomes C, Costa R, Pinheiro N, Coco J, Costa A (2014) Melhoramento genético de cereais de outono/inverno em Portugal, Revista Agronegócios, pp. 1–27, [http://www.agronegocios.eu/noticias/melhoramento-genetico-de-cereais-de-outono-inverno-em-portugal/]. Acessed 22 June 2018

  • Crosby AR (1957) Nucleolar activity of lagging chromosomes in wheat. Am J Bot 44:813–822

    Article  Google Scholar 

  • Dagne K, Heneen WK (1992) The karyotype and nucleoli of Guizotia abyssinica (Compositae). Hereditas 117:73–83

    Article  Google Scholar 

  • Derenzini M (2000) The Ag-NORs. Micron 31:117–120

    Article  CAS  PubMed  Google Scholar 

  • Dias-Gómez J, Twyman RM, Zhu C, Farré G, Serrano JCE, Portero-Otin M, Munõz P, Sandmann G, Capell T, Christou P (2017) Biofortification of crops with nutrients: factors affecting utilization and storage. Curr Opin Biotechnol 44:115–123

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F, Xie Y (2015) Heavy metal stress and some mechanisms of plant defense response. Sci World J. 2015. Article ID 756120, 18 pages:1–18. https://doi.org/10.1155/2015/756120

    Article  CAS  Google Scholar 

  • FAOSTAT (2018) Food and Agriculture Organization of the United Nations, [http://www.fao.org/statistics/en/] (Accessed in 19 May 2018)

  • Farooq M, Basra SMA, Wahid A (2006) Priming of field-sown rice seed enhances germination, seedling establishment, allometry and yield. Plant Growth Regul 49:285–294

    Article  CAS  Google Scholar 

  • Farooq M, Aziz T, Habib M (2011) Boron nutripriming improves the germination and early seedling growth of rice (Oryza sativa L.). J Plant Nutr 34:1507–1515

    Article  CAS  Google Scholar 

  • Flavell RB, O’Dell M, Thompson WF (1988) Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J Mol Biol 204:523–534

    Article  CAS  PubMed  Google Scholar 

  • Gibson RS (2006) Zinc: the missing link in combating micronutrient malnutrition in developing countries. Proc Nutr Soc 65:51–60

    Article  CAS  PubMed  Google Scholar 

  • Giovanni M, Tay CY, Setyawati MI, Xie J, Ong CN, Fan R, Yue J, Zhang L, Leong DT (2015) Toxicity profiling of water contextual zinc oxide, silver, and titanium dioxide nanoparticles in human oral and gastrointestinal cell systems. Environ Toxicol 10:1–11

    Google Scholar 

  • Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50

    Article  CAS  PubMed  Google Scholar 

  • Haaf T, Ward DC (1996) Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp Cell Res 224:163–173

    Article  CAS  PubMed  Google Scholar 

  • Hafeez B, Khanif YM, Saleem M (2013) Role of zinc in plant nutrition—a review. Am J Exp Agric 3:374–391

    CAS  Google Scholar 

  • Hariharan N, Sussman MA (2014) Stressing on the nucleolus in cardiovascular disease. Biochim Biophys Acta 1842:798–801

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Verdun D (2011) Assembly and disassembly of the nucleolus during the cell cycle. Nucleus 2:189–194

    Article  PubMed  PubMed Central  Google Scholar 

  • Imran M, Mahmood A, Römheld V, Neumann G (2013) Nutrient seed priming improves seedling development of maize exposed to low root zone temperatures during early growth. Eur J Agron 49:141–148

    Article  CAS  Google Scholar 

  • Jiang WS, Liu DH (1999) Effects of Pb2+ on root growth, cell division and nucleolus of Brassica juncea L. Israel J Plant Sci 47:153–156

    Article  CAS  Google Scholar 

  • Jiang WS, Liu DH (2000) Effects of Pb2+ on root growth, cell division, and nucleolus of Zea mays L. Bull Environ Contam Toxicol 65:786–793

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Liu D, Liu X (2001) Effects of copper on root growth, cell division, and nucleolus of Zea mays. Biol Plant 44:105–109

    Article  CAS  Google Scholar 

  • Jiang Z, Zhang H, Qin R, Zou J, Wang J, Shi Q, Jiang W, Liu D (2014) Effects of lead on the morphology and structure of the nucleolus in the root tip meristematic cells of Allium cepa L. Int J Mol Sci 15:13406–13423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jisha KC, Vijayakumari K, Puthur JT (2013) Seed priming for abiotic stress tolerance: an overview. Acta Physiol Plant 35:1381–1396. https://doi.org/10.1007/s11738-012-1186-5

    Article  Google Scholar 

  • Jordan EG, Martini G, Bennett MD, Flavell RB (1982) Nucleolar fusion in wheat. J Cell Sci 56:485–495

    Google Scholar 

  • Kalinina NO, Makarova S, Makhotenko A, Love AJ, Taliansky M (2018) The multiple functions of the nucleolus in plant development, disease and stress responses. Front Plant Sci 9:132. https://doi.org/10.3389/fpls.2018.00132

    Article  PubMed  PubMed Central  Google Scholar 

  • Laity JH, Lee BM, Wright PE (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin in Struc Biol 11:39–46

    Article  CAS  Google Scholar 

  • Lee SS, Kim JH (1999) Morphological change, sugar content, and α-amylaseactivity of rice seeds under various priming conditions. Kor J Crop Sci 44:138–142

    Google Scholar 

  • Lee SS, Kim JH (2000) Total sugars, α-amylase activity, and germination after priming of normal and aged rice seeds. Kor J Crop Sci 45:108–111

    Google Scholar 

  • Lima-Brito J, Guedes-Pinto H, Harrison GE, Heslop-Harrison JS (1996) Chromosome identification and nuclear architecture in Triticale x tritordeum F1 hybrids. J Exp Bot 47:583–588

    Article  CAS  Google Scholar 

  • Liu DH, Jiang WS (1991) Effects of Al3+ on the nucleolus in root tip cells of Allium cepa. Hereditas 115:213–219

    Article  CAS  Google Scholar 

  • Liu DH, Jiang WS (1996) Effects of Zn2+ on root growth, cell division, and nucleolus of Allium cepa L. J Environ Sci 8:21–27

    CAS  Google Scholar 

  • Liu DH, Jiang WS, Wang W, Zhao FM, Lu C (1994) Effects of lead on root growth, cell division and nucleolus of Allium cepa. Environ Pollut 86:1–4

    Article  CAS  PubMed  Google Scholar 

  • Liu DH, Jiang WS, Wang W, Zhai L (1995) Evaluation of metal ion toxicity on root tip cells by the Allium test. Israel J Plant Sci 43:125–133

    Article  CAS  Google Scholar 

  • Lutts S, Benincasa P, Wojtyla L, Kubala S, Pace R, Lechowska K, Quinet M, Garnczarska M (2016) Seed priming: new comprehensive approaches for an old empirical technique—chapter 1, pp. 1-47 [https://doi.org/10.5772/64420]. In: New challenges in seed biology—basic and translational research driving seed technology [http://www.intechopen.com/books/new-challenges-in-seedbiology-basic-and-translational-research-driving-seed-technology]. Acessed 01 July 2018. INTECH (Publisher)

  • Martini G, Flavell R (1985) The control of nucleolus volume in wheat, a genetic study at three developmental stages. Gen Soc Great Brit Hered 54:111–120

    Google Scholar 

  • Mayer C, Grummt I (2005) Cellular stress and nucleolar function. Cell Cycle 4(8):1036–1038

    Article  CAS  PubMed  Google Scholar 

  • McClintock B (1934) The relationship of a particular chromosomal element to the development of the nucleoli in Zea mays. Z Zellforsch Mikrosk Anat 21:294–328

    Article  Google Scholar 

  • Mehta R (1995) The potential for the use of cell-proliferation and oncogene expression as intermediate markers during liver carcinogenesis. Cancer Lett 93:85–102

    Article  CAS  PubMed  Google Scholar 

  • Nawaz A, Farooq M, Ahmad R, Maqsood S, Basra A, Lal R (2016) Seed priming improves stand establishment and productivity of no tillwheat grown after direct seeded aerobic and transplanted flooded rice. Eur J Agron 76:130–137

    Article  Google Scholar 

  • Nestel P, Bouis HE, Meenakshi JV, Pfeiffer W (2006) Biofortification of staple food crops. J Nutr 136:1064–1067 New Phytol 173:677–702

    Article  CAS  PubMed  Google Scholar 

  • Ng KW (2011) The role of the tumor suppressor p53 pathway in the cellular DNA damage response to zinc oxide nanoparticles. Biomaterials 32:8218–8225

    Article  CAS  PubMed  Google Scholar 

  • Oladele EO, Odeigah PGC, Taiwa IA (2013) The genotoxic effect of lead and zinc on bambara groundnut (Vigna subterranean). Afr J Environ Sci Technol 7:9–13

    CAS  Google Scholar 

  • Olson MOJ, Dundr M, Szebeni A (2000) The nucleolus: an old factory with unexpected capabilities. Trends Cell Biol 10:189–196

    Article  CAS  PubMed  Google Scholar 

  • Paparella S, Araújo SS, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the art and new perspectives. Plant Cell Rep 34:1281–1293

    Article  CAS  PubMed  Google Scholar 

  • Pederson T (1998) The plurifunctional nucleolus. Nucleic Acids Res 26:3871–3876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pekol S, Baloglu MC, Celik Altunoglu Y (2016) Evaluation of genotoxic and cytotoxic effects of environmental stress in wheat species with different ploidy levels. Turk J Biol 40:580–588

    Article  CAS  Google Scholar 

  • Pontvianne F, Matía I, Douet J, Tourmente S, Medina FJ, Echeverria M, Sáez-Vásquez J (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol Biol Cell 18:369–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Probst AV, Scheid OM (2015) Stress-induced structural changes in plant chromatin. Curr Opin Plant Biol 27:8–16

    Article  CAS  PubMed  Google Scholar 

  • Qin R, Jiang W, Liu D (2013) Cadmium can induce alterations in the cellular localization and expression of three major nucleolar proteins in root tip cells of Vicia faba L. Plant Soil 368:365–373

    Article  CAS  Google Scholar 

  • Rashid A, Hollington PA, Harris D, Khan P (2006) On-farm seed priming for barley on normal, saline and saline-sodic soils in North West Frontier Province, Pakistan. Eur J Agron 24:276–281

    Article  CAS  Google Scholar 

  • Regvar M, Eichert D, Kaulich B, Gianoncelli A, Pongrac P, Vogel-Mikuš K et al (2011) New insights into globoids of protein storage vacuoles in wheat aleurone using synchrotron soft x-ray microscopy. J Exp Bot 62:3929–3939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehman A, Farooq M, Naveed M, Nawaz A, Shahzad B (2018) Seed priming of Zn with endophytic bacteria improves the productivity and grain biofortification of bread wheat. Eur J Agron 94:98–107

    Article  CAS  Google Scholar 

  • Reis S, Pavia I, Carvalho A, Moutinho-Pereira J, Correia C, Lima-Brito J (2018) Seed priming with Iron and zinc in bread wheat: effects in germination, mitosis and grain yield. Protoplasma 255:1179–1194

    Article  CAS  PubMed  Google Scholar 

  • Rout GR, Sahoo S (2015) Role of Iron in plant growth and metabolism. Rev Agric Sci 3:1–24

    Article  Google Scholar 

  • Rubbi CP, Milner J (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22:6068–6077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruttanaruangboworn A, Chanprasert W, Tobunluepop P, Onwimol D (2017) Effect of seed priming with different concentrations of potassium nitrate on the pattern of seed imbibition and germination of rice (Oryza sativa L.). J Integr Agric 16:605–613

    Article  CAS  Google Scholar 

  • Sardana R, O’Dell M, Flavell RB (1993) Correlation between the size of the intergenic regulatory region, the status of cytosine methylation of rRNA genes and nucleolar expression in wheat. Mol Gen Genet 236:155–162

    Article  CAS  PubMed  Google Scholar 

  • Sengupta S, Peterson TR, Sabatini DM (2010) Regulation of the mTor complex 1 by nutrients, growth factors, and stress. Mol Cell 40:310–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43

    Article  CAS  PubMed  Google Scholar 

  • Sharma AD, Rathore SVS, Srinivasan K, Tyagi RK (2014) Comparison of various seed priming methods for seed germination, seedling vigour and fruit yield in okra (Abelmoschus esculentus L. Moench). Sci Hortic 165:75–81

    Article  CAS  Google Scholar 

  • Shaw P, Brown J (2012) Nucleoli: composition, function, and dynamics. Plant Physiol 158:44–51

    Article  CAS  PubMed  Google Scholar 

  • Shaw PJ, Jordan EG (1995) The nucleolus. Annu Rev Cell Dev Biol 11:93–121

    Article  CAS  PubMed  Google Scholar 

  • Sheteiwy MS, Guan Y, Cao D, Li J, Nawaz A, Hu Q, HuW NM, Hu J (2015) Seed priming with polyethylene glycol regulating the physiological and molecular mechanism in rice (Oryza sativa L.) under nano-ZnO stress. Sci Rep 5:14278

    Article  CAS  Google Scholar 

  • Sheteiwy MS, Fu Y, Hu Q, Nawaz A, Guan Y, Li Z, HuangY HJ (2016) Seed priming with polyethylene glycol induces antioxidative defense and metabolic regulation of rice under nano-ZnO stress. Environ Sci Pollut Res 23:19989–20002. https://doi.org/10.1007/s11356-016-7170-7

    Article  CAS  Google Scholar 

  • Sheteiwy M, Shen H, Xu J, Guan Y, Song W, Hu J (2017a) Seed polyamines metabolism induced by seed priming with spermidine and 5-aminolevulinic acid for chilling tolerance improvement in rice (Oryza sativa L.) seedlings. Environ Exp Bot 137:58–72

    Article  CAS  Google Scholar 

  • Sheteiwy MS, Dong Q, An J, Song W, Guan Y, He F, Huang Y, Hu J (2017b) Regulation of ZnO nanoparticles-induced physiological and molecular changes by seed priming with humic acid in Oryza sativa seedlings. Plant Growth Regul 83:27–41

    Article  CAS  Google Scholar 

  • Sheteiwy MS, An J, Yin M, Jia X, Guan Y, He F, Hu J (2018a) Cold plasma treatment and exogenous salicylic acid priming enhances salinity tolerance of Oryza sativa seedlings. Protoplasma. https://doi.org/10.1007/s00709-018-1279-0

  • Sheteiwy MS, Gonga D, Gaoa Y, Pana R, Hua J, Guana Y (2018b) Priming with methyl jasmonate alleviates polyethylene glycol-induced osmotic stress in rice seeds by regulating the seed metabolic profile. Environ Exp Bot 153:236–248

    Article  CAS  Google Scholar 

  • Singh K, Kayastha AM (2014) α-Amylase from wheat (Triticum aestivum) seeds: its purification, biochemical attributes and active site studies. Food Chem 162:1–9

    Article  CAS  PubMed  Google Scholar 

  • Singh SP, Keller B, Gruissem W, Bhullar NK (2017) Rice NICOTIANAMINE SYNTHASE 2 expression improves dietary iron and zinc levels in wheat. Theor Appl Genet 130:283–292

    Article  CAS  PubMed  Google Scholar 

  • Smetana K, Busch H (1974) The nucleolus and nucleolar DNA. In: Busch H (ed) The cell nucleus. Academic Press, New York, pp 73–147

    Chapter  Google Scholar 

  • Stack S, Herikhoff L, Sherman J, Anderson L (1991) Staining plant cells with silver. I. the salt nylon technique. Biotech Histochem 1:69–78

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama M, Machida Y (2018) Editorial: novel aspects of nucleolar functions in plant growth and development. Front Plant Sci 9:814. https://doi.org/10.3389/flps.2018.00814

    Article  PubMed  PubMed Central  Google Scholar 

  • Tajrishi MM, Tuteja R, Tuteja N (2011) Nucleolin. The most abundant multifunctional phosphoprotein of nucleolus. Commun Integr Biol 4:267–275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi M, Absalon MJ, McLure KG, Kastan MB (2005) Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 123:49–63

    Article  CAS  PubMed  Google Scholar 

  • Taylor AG, Allen PS, Bennett MA, Bradford JK, Burris JS, Mishra MK (1998) Seed enhancements. Seed Sci Res 8:245–256. https://doi.org/10.1017/S0960258500004141

    Article  Google Scholar 

  • Teerarak M, Bhinija K, Thitavasanta S, Laosinwattana C (2009) The impact of sodium chloride on root growth, cell division, and interphase silver-stained nucleolar organizer regions (AgNORs) in root tip cells of Allium cepa L. Sci Hortic 121:228–232

    Article  CAS  Google Scholar 

  • Tripathi R, Girjesh K (2010) Genetic loss through heavy metal induced chromosomal stickiness in grass pea. Caryologia 63:223–228

    Article  Google Scholar 

  • Tsekrekou M, Stratigi K, Chatzinikolaou G (2017) The nucleolus: in genome maintenance and repair. Int J Mol Sci 18:1411. https://doi.org/10.3390/ijms18071411

    Article  CAS  PubMed Central  Google Scholar 

  • Ugrinova I, Monier K, Ivaldi C, Thiry M, Storck S, Mongelard F, Bouvet P (2007) Inactivation of nucleolin leads to nucleolar disruption, cell cycle arrest and defects in centrosome duplication. BMC Mol Biol 8:66. https://doi.org/10.1186/1471-2199-8-66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Underwood JCE, Giri D (1988) Nucleolar organizer regions as diagnostic discriminants for malignancy. J Pathol 155:95–96

    Article  CAS  PubMed  Google Scholar 

  • Valença AW, Bake A, Brouwer ID, Giller KE (2017) Agronomic biofortification of crops to fight hidden hunger in Sub-Saharan Africa. Glob Food Sec 12:8–14

    Article  Google Scholar 

  • Vallee BL, Falchuk KH (1993) The biochemical basis of zinc physiology. Physiol Rev 73:79–118

    Article  CAS  PubMed  Google Scholar 

  • Velu G, Ortiz-Monasterio I, Cakmak I, Hao Y, Singh RP (2014) Biofortification strategies to increase grain zinc and iron concentrations in wheat. J Cereal Sci 59:365–372

    Article  CAS  Google Scholar 

  • Virk P, Govindan V (2014) Zinc wheat. The 2nd Global Conference on Biofortification: Getting Nutritious Foods to People, August 2014, Progress Brief #2 – Crop Development 2 p

  • Wojtyla L, Lechowska K, Kubala S, Garnczarska M (2016) Molecular processes induced in primed seeds—increasing the potential to stabilize crop yields under drought conditions. J Plant Physiol 203:116–126

    Article  CAS  PubMed  Google Scholar 

  • Yacoubi R, Job C, Belghazi M, Chaibi W, Job D (2013) Proteomic analysis of the enhancement of seed vigour in osmoprimed alfalfa seeds germinated under salinity stress. Seed Sci Res 23:99–110. https://doi.org/10.1017/S0960258513000093

    Article  CAS  Google Scholar 

  • Zhang Y, Shi R, Rezaul KM, Zhang F, Zou C (2010) Iron and zinc concentrations in grain and flour of winter wheat as affected by foliar application. J Agric Food Chem 58:12268–12274

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Jiang Z, Qin R, Zhang H, Zou J, Jiang W, Liu D (2014) Accumulation and cellular toxicity of aluminum in seedling of Pinus massoniana. BMC Plant Biol 14:264. https://doi.org/10.1186/s12870-014-0264-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Eng. Coutinho from the INIAV (Elvas) for kindly providing the seeds of the bread wheat cultivar ‘Jordão’. The authors A.C. and J.L.-B. acknowledge the projects UID/MULTI/04046/2013 and UID/AGR/04033/2013 (supported by the FCT - Portuguese Foundation for the Science and Technology) and POCI-01-0145-FEDER-006958 (supported by FEDER/COMPETE/POCI – Operational Competitiveness and Internationalization Programme) and the COST ACTION CA16212, “INDEPTH” - “Impact of nuclear domains on gene expression and plant traits” (European Cooperation in Science and Technology).

Funding

This work was supported by the “Fundação para a Ciência e a Tecnologia” (FCT) (grant number PD/BD/113611/2015) attributed to author I.P. in the scope of the Ph.D. program “Agricultural production chains—from fork to farm” (PD/00122/2012).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to José Eduardo Lima-Brito.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Peter Nick

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carvalho, A., Reis, S., Pavia, I. et al. Influence of seed priming with iron and/or zinc in the nucleolar activity and protein content of bread wheat. Protoplasma 256, 763–775 (2019). https://doi.org/10.1007/s00709-018-01335-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-01335-1

Keywords

Navigation