Skip to main content
SpringerLink
Log in

Effects of boron toxicity on root and leaf anatomy in two Citrus species differing in boron tolerance

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Typical toxic symptom only occurred in B-toxic C. grandis leaves. B-toxicity induced PCD of C. grandis leaf phloem tissue. The lower leaf free B might contribute to the higher B-tolerance of C. sinensis.

Abstract

Seedlings of ‘Xuegan’ (Citrus sinensis) and ‘Sour pummelo’ (Citrus grandis) differing in boron (B)-tolerance were irrigated with nutrient solution containing 10 (control) or 400 (B-toxic) μM H3BO3 for 15 weeks. Thereafter, the effects of B-toxicity on leaf photosynthesis, chlorophyll, plant B absorption and distribution, root and leaf anatomy were investigated to elucidate the possible B-tolerant mechanisms of Citrus plants. Typical toxic symptom only occurred in B-toxic C. grandis leaves. Similarly, B-toxicity only affected C. grandis photosynthesis and chlorophyll. Although total B concentration in B-toxic roots and leaves was similar between the two species, leaves from B-toxic C. grandis plant middle had higher free B and lower bound B as compared with those from C. sinensis. Effects of B-toxicity on leaf structure were mainly limited to the mesophyll cells and the phloem of leaf veins. Although irregular cell wall thickening was observed in leaf cortex cells and phloem tissue of B-toxic C. grandis and C. sinensis leaves, exocytosis only occurred in the companion cells and the parenchyma cells of B-toxic C. sinensis leaf phloem. Also, B-toxicity induced cell death of phloem tissue through autophagy in C. grandis leaf veins. B-toxicity caused death of root epidermal cells of the two Citrus species. B-toxicity restrained degradation of middle lamella, but did not alter ultrastructure of Golgi apparatus and mitochondria in root elongating zone cells. In conclusion, C. sinensis was more tolerant to B-toxicity than C. grandis. The lower leaf free B and higher bound B might contribute to the higher B-tolerance of C. sinensis.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aquea F, Federici F, Moscoso C, Vega A, Jullian P, Haseloff J, Arce-Johnson P (2012) A molecular framework for the inhibition of Arabidopsis root growth in response to boron toxicity. Plant Cell Environ 35:719–734

    Article  CAS  PubMed  Google Scholar 

  • Ardic M, Sekmen AH, Turkan I, Tokur S, Ozdemir F (2009) The effects of boron toxicity on root antioxidant systems of two chickpea (Cicer arietinum L.) cultivars. Plant Soil 314:99–108

    Article  CAS  Google Scholar 

  • Battey NH, James NC, Greenland AJ, Brownlee C (1999) Exocytosis and endocytosis. Plant Cell 11:643–659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Berlyn GP, Miksche JP (1976) Botanical microtechnique and cytochemistry. Iowa State University Press, Ames

    Google Scholar 

  • Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500

    Article  CAS  PubMed  Google Scholar 

  • Bursch W, Hochegger K, Török L, Marian B, Ellinger A, Hermann RS (2000) Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J Cell Sci 113:1189–1198

    CAS  PubMed  Google Scholar 

  • Cakmak I, Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 156:127–130

    Google Scholar 

  • Camacho-Cristóbal JJ, Rexach J, González-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50:1247–1255

    Article  PubMed  Google Scholar 

  • Camacho-Cristóbal JJ, Rexach J, Herrera-Rodríguez MB, Navarro-Gochicoa MT, González-Fontes A (2011) Boron deficiency and transcript level changes. Plant Sci 181:85–89

    Article  PubMed  Google Scholar 

  • Cervilla LM, Blasco B, Ríos J, Romero L, Ruiz J (2007) Oxidative stress and antioxidants in tomato (Solanum lycopericum) plants subjected to boron toxicity. Ann Bot 100:747–756

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cervilla LM, Rosales MA, Rubio-Wilhelmi MM, Sánchez-Rodríguez E, Blasco B, Ríos JJ, Romero L, Rui JM (2009) Involvement of lignification and membrane permeability in the tomato root response to boron toxicity. Plant Sci 176:545–552

    Article  CAS  Google Scholar 

  • Chen LS, Han S, Qi YP, Yang LT (2012) Boron stresses and tolerance in Citrus. Afr J Biotechnol 11:5961–5969

    CAS  Google Scholar 

  • Christensen JJ (1934) Non-parasitic leaf spots of barley. Phytopathology 24:726–742

    Google Scholar 

  • Fernández-Ballester G, García-Sánchez F, Cerdá A, Martínez V (2003) Tolerance of citrus rootstock seedlings to saline stress based on their ability to regulate ion uptake and transport. Tree Physiol 23:265–271

    Article  PubMed  Google Scholar 

  • García PC, Rivero RM, López-Lefebre LR, Sánchez E, Ruiz JM, Romero L (2001) Response of oxidative metabolism to the application of carbendazim plus boron in tobacco. Aust J Plant Physiol 28:801–806

    Google Scholar 

  • Han S, Tang N, Jiang HX, Yang LT, Li 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 

  • Havel L, Durzan DJ (1996) Apoptosis during diploid parthenogenesis and early somatic embryogenesis of Norway spruce. Int J Plant Sci 157:8–16

    Article  Google Scholar 

  • Hayes JE, Reid RJ (2004) Boron tolerance in barley is mediated by efflux of boron from the roots. Plant Physiol 136:3376–3382

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hu H, Brown PH (1997) Absorption of boron by plant roots. Plant Soil 193:49–58

    Article  CAS  Google Scholar 

  • Jiang C, Wang Y, Liu G, Xia Y, Peng S, Zhong B, Zeng Q (2009) Effect of boron on the leaves etiolation and fruit fallen of Newhall navel orange. Plant Nutr Fert Sci 15:656–661

    CAS  Google Scholar 

  • Kamali A, Childers N (1966) Effect of boron nutrition on peach anatomy. J Amer Soc Hort Sci 90:33–38

    Google Scholar 

  • Kobayashi M, Matoh T, Azuma J (1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 110:1017–1020

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kuo CY, Yeh DM (2006) Effects of boric acid concentration and shading on growth, leaf physiology, and anatomy of Guzmania. Hortscience 41:618–621

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3:229–239

    CAS  PubMed  Google Scholar 

  • Luft JH (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409–414

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matoh T, Ochiai K (2005) Distribution and partitioning of newly taken-up boron in sunflower. Plant Soil 278:351–360

    Article  CAS  Google Scholar 

  • Miwa K, Takano J, Omori H, Seki M, Shinozaki K, Fujiwara T (2007) Plants tolerant of high boron levels. Science 318:1417

    Article  CAS  PubMed  Google Scholar 

  • Nable RO, Lance RC, Cartwright B (1990) Uptake of boron and silicon by barley genotypes with differing susceptibility to boron toxicity. Ann Bot 66:83–90

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nuttall CY (2000) Boron tolerance and uptake in higher plants. Dissertation, University of Cambridge, Cambridge

  • Papadakis IE, Dimassi KN, Therios IN (2003) Response of two citrus genotypes to six boron concentrations: concentration and distribution of nutrients, total absorption, and nutrient use efficiency. Aust J Agr Res 54:571–580

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Papadakis IE, Dimassi KN, Bosabalidis AM, Therios IN, Patakas A, Giannakoula A (2004b) 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 

  • Parks JL, Edwards M (2005) Boron in the environment. Crit Rev Environ Sci Technol 35:81–114

    Article  CAS  Google Scholar 

  • Redondo-Nieto M, Maunoury N, Mergaert P, Kondorosi E, Bonilla I, Bolaños L (2012) Boron and calcium induce major changes in gene expression during legume nodule organogenesis. Does boron have a role in signalling? New Phytol 195:14–19

    Article  CAS  PubMed  Google Scholar 

  • Reid R (2007) Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley. Plant Cell Physiol 48:1673–1678

    Article  CAS  PubMed  Google Scholar 

  • Reid RJ, Fitzpatrick KL (2009a) Redistribution of boron in leaves reduces boron toxicity. Plant Signal Behav 4:1091–1093

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reid RJ, Fitzpatrick KL (2009b) Influence of leaf tolerance mechanisms and rain on boron toxicity in barley and wheat. Plant Physiol 151:413–420

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reid RJ, Hayes JE, Post A, Stangoulis JCR, Graham RD (2004) Acritical analysis of the causes of boron toxicity in plants. Plant Cell Environ 27:1405–1414

    Article  CAS  Google Scholar 

  • Ruiz JM, Rivero RM, Romero L (2003) Preliminary studies on the involvement of biosynthesis of cysteine and glutathione concentration in the resistance to B toxicity in sunflower plants. Plant Sci 165:811–817

    Article  CAS  Google Scholar 

  • Schnurbusch T, Hayes J, Hrmova M, Baumann U, Ramesh SA, Tyerman SD, Langridge P, Sutton T (2010) Boron toxicity tolerance in barley through reduced expression of the multifunctional aquaporin HvNIP2;1. Plant Physiol 153:1706–1715

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sheng O, Zhou G, Wei Q, Peng S, Deng X (2010) Effects of excess boron on growth, gas exchange, and boron status of four orange scion-rootstock combinations. J Plant Nutr Soil Sci 173:469–476

    Article  CAS  Google Scholar 

  • Smith TE, Grattan SR, Grieve CM, Poss JA, Suarez DL (2010) Salinity’s influence on boron toxicity in broccoli: II impacts on boron uptake, uptake mechanisms and tissue ion relations. Agr Water Manag 97:783–791

    Article  Google Scholar 

  • Sotiropoulos TE, Therios IN, Dimassi KN, Bosabalidis A, Kofidis G (2002) Nutritional status, growth, CO2 assimilation, and leaf anatomical responses in two kiwifruit species under boron toxicity. J Plant Nutr 25:1249–1261

    Article  CAS  Google Scholar 

  • Wang J, Nakazato T, Sakanishi K, Yamada O, Tao H, Saito I (2006) Single-step microwave digestion with HNO3 alone for determination of trace elements in coal by ICP spectrometry. Talanta 68:1584–1590

    Article  CAS  PubMed  Google Scholar 

  • Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot 37:629–672

    Google Scholar 

  • Wimmer MA, Lochnit G, Bassil E, Mühling KH, Goldbach HE (2009) Membrane-associated, boron-interacting proteins isolated by boronate affinity chromatography. Plant Cell Physiol 50:1292–1304

    Article  CAS  PubMed  Google Scholar 

  • Woods WG (1996) A review of possible boron speciation relating to essentiality. J Trace Elem Exp Med 9:153–163

    Article  CAS  Google Scholar 

  • Yu X, Bell PF (1998) Nutrient deficiency symptoms and uptake mechanisms of rice. J Plant Nutr 21:2077–2088

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the earmarked fund for China Agriculture Research System.

Conflict of interest

No conflicts of interest declared.

Author information

Authors and Affiliations

  1. Institute of Horticultural Plant Physiology, Biochemistry and Molecular Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Jing-Hao Huang, Peng Guo & Li-Song Chen

  2. College of Life Sciences, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Jing-Hao Huang

  3. Pomological Institute, Fujian Academy of Agricultural Sciences, Fuzhou, 350013, China

    Jing-Hao Huang, Zi-Jian Cai & Shou-Xing Wen

  4. College of Resource and Environmental Science, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Xin Ye, Gui-Zhu Lin & Li-Song Chen

  5. Fujian Key Laboratory for Plant Molecular and Cell Biology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Li-Song Chen

Authors
  1. Jing-Hao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zi-Jian Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shou-Xing Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peng Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xin Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gui-Zhu Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Li-Song Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Li-Song Chen.

Additional information

Communicated by U. Lüttge.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, JH., Cai, ZJ., Wen, SX. et al. Effects of boron toxicity on root and leaf anatomy in two Citrus species differing in boron tolerance. Trees 28, 1653–1666 (2014). https://doi.org/10.1007/s00468-014-1075-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-014-1075-1

Keywords

Search

Navigation