Skip to main content
SpringerLink
Log in

Boron excess affects photosynthesis and antioxidant apparatus of greenhouse Cucurbita pepo and Cucumis sativus

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

This study aimed to evaluate the behavior of zucchini (Cucurbita pepo L.) and cucumber (Cucumis sativus L.) under boron (B) excess. Plants were grown under greenhouse conditions in a sandy soil–peat mixture using a nutrient solution containing 0.2 (control), 10 and 20 mg L−1 B. Visible symptoms were quantified and leaf B accumulation, gas exchanges, chlorophyll (Chl) a fluorescence, malondialdehyde by-products and antioxidants were investigated 20 days after the beginning of the treatments. Boron toxicity induced oxidative load and leaf necrotic burns coupled with the reduction of leaf growth and biomass accumulation in both species. Boron excess resulted in a decrease of Chl a/b ratio, potential (Fv/Fm) and actual (ΦPSII) PSII quantum efficiency, photosynthetic rate (Pn), stomatal conductance (gs), and transpiration (E) as well. A general stimulation of the antioxidant enzymes ascorbate peroxidase, catalase and superoxide dismutase was observed, and a significant increase in the oxidized form of ascorbate and glutathione was evidenced for treated plants of both species. A difference between the two species was observed: C. pepo appeared to be more sensitive to B stress being damaged at all B concentration. C. sativus grown at 10 mg L−1 B in nutrient solution showed some down-regulated mechanisms, i.e. increase in Chl b content and a good photochemical PSII efficiency as well as a higher amount of constitutive antioxidant molecules, that, however, are not sufficient to contrast the negative effects of B.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams WW III, Baker DH (1998) Seasonal changes in xanthophylls cycle-dependent energy dissipation in Yucca glauca Nuttall. Plant Cell Environ 21:501–511

    Article  CAS  Google Scholar 

  • Adams WW, Zarter CR, Ebbert V, Demmig-Adams B (2004) Photoprotective strategies of overwintering evergreens. Bioscience 54:41–49

    Article  Google Scholar 

  • Alpaslan M, Gunes A (2001) Interactive effects of boron and salinity stress on the growth, membrane permeability and mineral composition of tomato and cucumber plants. Plant Soil 136:128–133

    Google Scholar 

  • Ardic M, Sekmen AH, Tokur S, Ozdemir F, Turkan I (2009) Antioxidant response of chickpea plants subjected to boron toxicity. Plant Biol 11:328–338

    Article  PubMed  CAS  Google Scholar 

  • Bellaloui N, Brown PH (1998) Cultivar differences in boron uptake and distribution in celery (Apium graveolens), tomato (Lycopersicon esculentum) and wheat (Triticum aestivum). Plant Soil 198:153–158

    Article  CAS  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  PubMed  CAS  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Google Scholar 

  • Brown PH, Hu H (1996) Phloem mobility of boron is species dependent: evidence for phloem in sorbitol-rich species. Ann Bot 77:497–505

    Article  CAS  Google Scholar 

  • Cakmak I, Marschner H (1992) Magnesium-deficiency and high light-intensity enhance activities of superoxide-dismutase, ascorbate peroxidase, and glutathione-reductase in bean-leaves. Plant Physiol 98:1222–1227

    Article  PubMed  CAS  Google Scholar 

  • Cervilla LM, Blasco B, Rios JJ, Romero L, Ruiz JM (2007) Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plant subjected to boron toxicity. Ann Bot 100:747–756

    Article  PubMed  CAS  Google Scholar 

  • Di Cagno R, Guidi L, De Gara L, Soldatini GF (2001) Combined cadmium and ozone treatments affect photosynthesis and ascorbate-dependent defences in sunflower. New Phytol 151:627–636

    Article  Google Scholar 

  • Dordas C, Brown PH (2001) Evidence for channel mediated transport of boric acid in squash (Cucurbita pepo). Plant Soil 235:95–103

    Article  CAS  Google Scholar 

  • Duysens LNM (1952) Transfer of excitation energy in photosynthesis. PhD thesis, University of Utrecht, The Netherlands

  • Edelstein M, Ben-Hur M, Cohen R, Burger Y, Ravina I (2005) Boron and salinity on grafted and non-grafted melon plants. Plant Soil 269:273–284

    Article  CAS  Google Scholar 

  • Eraslan F, Inal A, Gunes A, Alpaslan M (2007a) Impact of exogenous salicylic acid on the growth, antioxidant activity and physiology of carrot plants subjected to combined salinity and boron toxicity. Sci Hortic 113:120–128

    Article  CAS  Google Scholar 

  • Eraslan F, Inal A, Savasturk O, Gunes A (2007b) Changes in antioxidative system and membrane damage of lettuce in response to salinity and boron toxicity. Sci Hortic 114:5–10

    Article  CAS  Google Scholar 

  • Eskling M, Arvidsson PO, Åkerlund HE (1997) The xanthophyll cycle, its regulation and components. Physiol Plant 100:806–816

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signaling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Guidi L, Mori S, Degl’Innocenti E, Pecchia S (2007) Effects of ozone exposure or fungal pathogen on white lupin leaves as determined by imaging of chlorophyll a fluorescence. Plant Physiol Biochem 45:851–857

    Article  PubMed  CAS  Google Scholar 

  • Guidi L, Degl’Innocenti E, Carmassi G, Massa D, Pardossi A (2011) Effects of boron on leaf chlorophyll fluorescence of greenhouse tomato grown with saline water. Environ Exp Bot 73:57–63

    Article  CAS  Google Scholar 

  • Han S, Tang N, Jiang H-X, Yang LT, Lee Y, Chen LS (2009) CO2 assimilation, photosystem II photochemistry, carbohydrate metabolism and antioxidant system of citrus leaves in response to boron stress. Plant Sci 176:143–153

    Article  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Horn R, Grundmann G, Paulsen H (2007) Consecutive binding of chlorophylls a and b during the assembly in vitro of light-harvesting chlorophyll-a/b protein (LHCIIb). J Mol Biol 366:1045–1054

    Article  PubMed  CAS  Google Scholar 

  • Jingxian Z, Kirkham MB (1996) Antioxidant response to drought in sunflower and sorghum seedlings. New Phytol 132:361–373

    Article  Google Scholar 

  • Kampfenkel K, Van Montagu M, Inze D (1995) Extraction and determination of ascorbate and dehydroascorbate from plant tissue. Anal Biochem 225:165–167

    Article  PubMed  CAS  Google Scholar 

  • Landi M, Pardossi A, Remorini D, Guidi L (2013) Antioxidant and photosynthetic response of a purple-leaved and a green-leaved cultivar of sweet basil (Ocimum basilicum) to boron excess. Environ Exp Bot 85:64–75

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Lovatt CJ, Bates LM (1984) Early effects of excess boron on photosynthesis and growth of Cucurbita pepo. J Exp Bot 35:297–305

    Article  CAS  Google Scholar 

  • Meguro M, Ito H, Takabayashi A, Tanaka R, Tanaka A (2011) Identification of the 7-hydroxymethyl chlorophyll a reductase of the chlorophyll cycle in Arabidopsis. Plant Cell 23:3442–3453

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux PM, Baker NR (2010) Oxidative stress: antagonistic signaling for acclimation or cell death? Plant Physiol 154:521–525

    Article  PubMed  CAS  Google Scholar 

  • Nable RO, Bañuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193:181–198

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  PubMed  CAS  Google Scholar 

  • Ottander C, Campbell D, Oquist G (1995) Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. Planta 197:176–183

    Article  CAS  Google Scholar 

  • Oxborough K (2004) Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. J Exp Bot 55:1195–1205

    Article  PubMed  CAS  Google Scholar 

  • Papadakis IE, Dimassi KN, Bosabalidis AM, Theorios IN, Patakas A, Giannakoula A (2004a) Effects of B excess on some physiological and anatomical parameters of ‘Navelina’ orange plants grafted on two rootstocks. Environ Exp Bot 51:247–257

    Article  CAS  Google Scholar 

  • Papadakis IE, Dimassi KN, Bosabalidis AM, Theorios IN, Patakas A, Giannakoula A (2004b) Boron toxicity in ‘Clementine’ mandarin plants grafted on two rootstocks. Plant Sci 166:539–547

    Article  CAS  Google Scholar 

  • Pennisi M, Gonfiantini R, Grassi S, Squarci P (2006) The utilization of boron and strontium isotopes for the assessment of boron contamination of the Cecina River alluvial aquifer (central-western Tuscany, Italy). Appl Geochem 21:643–655

    Article  CAS  Google Scholar 

  • Ruuhola T, Keinanen M, Keski-Saari S, Lehto T (2011) Boron nutrition affects the carbon metabolism of silver birch seedlings. Tree Physiol 31:1251–1261

    Article  PubMed  CAS  Google Scholar 

  • Ryang SZ, Woo SY, Know SY, Kim SH, Lee SH, Kim KN, Lee KD (2009) Changes of net photosynthesis, antioxidant enzyme activities, and antioxidant contents of Liriodendron tulipifera under elevated ozone. Photosynthetica 47:19–25

    Article  CAS  Google Scholar 

  • Sakuraba Y, Yokono M, Akimoto S, Tanaka R, Tanaka A (2010) Deregulated chlorophyll b synthesis reduces the energy transfer rate between photosynthetic pigments and induces photodamage in Arabidopsis thaliana. Plant Cell Physiol 51:1055–1065

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Bilger W (1993) Progress in chlorophyll-fluorescence research: major developments during the past years in retrospect. Prog Bot 54:151–173

    CAS  Google Scholar 

  • Schreiber U, Schliva U, Bilger B (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Soylemezoglu G, Demir K, Inal A, Gunes A (2009) Effect of silicon on antioxidant and stomatal response of two grapevine (Vitis vinifera L.) rootstocks grown in boron toxic saline and boron toxic-saline soil. Sci Hortic 123:240–246

    Article  CAS  Google Scholar 

  • Tanaka M, Fujiwara T (2008) Physiological roles and transport mechanisms of boron: perspectives from plants. Eur J Physiol 456:671–677

    Article  CAS  Google Scholar 

  • Tanaka R, Tanaka A (2011) Chlorophyll cycle regulates the construction and destruction of the light-harvesting complexes. Biochim Biophys Acta 1807:968–976

    Article  PubMed  CAS  Google Scholar 

  • Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228

    Article  PubMed  Google Scholar 

  • Wang JZ, Tao ST, Qi KJ, Wu J, Wu HQ, Zhang SL (2011) Changes in photosynthetic and antioxidative system of pear leaves to boron toxicity. Afr J Biotechnol 10:19693–19700

    CAS  Google Scholar 

  • Wolf B (1974) Improvement in the Azomethine-H method for determination of boron. Comm Soil Sci Plant Anal 5:39–44

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by MIUR-PRIN 2009 (Ministero dell’Istruzione, dell’Università e della Ricerca, Italy, Project “Physiological response of vegetables crops to boron excess”).

Author information

Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto, 80, 56124, Pisa, Italy

    Marco Landi, Damiano Remorini, Alberto Pardossi & Lucia Guidi

Authors
  1. Marco Landi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Damiano Remorini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alberto Pardossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lucia Guidi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucia Guidi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Landi, M., Remorini, D., Pardossi, A. et al. Boron excess affects photosynthesis and antioxidant apparatus of greenhouse Cucurbita pepo and Cucumis sativus . J Plant Res 126, 775–786 (2013). https://doi.org/10.1007/s10265-013-0575-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-013-0575-1

Keywords

Search

Navigation