, Volume 28, Issue 1, pp 295–307 | Cite as

The physiological and nutritional responses of seven different citrus rootstock seedlings to boron deficiency

  • Gao F. Zhou
  • Shu A. PengEmail author
  • Yong Z. Liu
  • Qing J. Wei
  • Jia Han
  • Md. Zahidul Islam
Original Paper


Key message

Carrizo citrange was the most tolerant citrus rootstock to B-deficiency and some physiological performance could be attributed to the decreased mineral nutrient concentrations caused by B-deficiency.


Boron (B) is an essential microelement for normal growth and development in vascular plants, and adequate B nutrition is crucial for agricultural production. Although citrus plants are not classified as the most sensitive species to B-deficiency, the occurrence of B-deficiency has been reported in the major citrus producing countries of the world, including the east and south of China. In this study, in order to evaluate the effects of B-deficiency on plant growth, root-morphological traits, B and other nutritional responses of citrus rootstock and to investigate the relationship between this physiological performance and mineral nutrients seven common rootstock seedlings, including Trifoliate orange (TO), Carrizo citrange (CC), Chongyi tangerine (CT), Red tangerine (RT), Cleopatra mandarin (CM), Fragrant citrus (FC), and Sour orange (SO), were treated by B-deficiency (0 mg L−1) or moderate B (0.25 mg L−1). All the seedlings were grown in hydroponics situation with modified 1/2-strength Hoagland’s solution under greenhouse conditions for 10 weeks. The results showed that B-deficiency inhibited the growth and development of all tested citrus rootstocks, but substantial differences were observed among these rootstocks. Different visible symptoms were observed both in the leaf and root. Corking of the leaf veins and leaf yellowing symptoms were observed on all rootstock genotypes except on CC, which exhibited a little discoloration at the end of the experiment. In addition, root growth of the citrus seedlings were also decreased by B-deficiency, but the decreases were more obvious in TO and FC. It was worth noting that B-deficiency inhibited lateral root growth and development more significantly than tap root, but not in lateral root initiation. The different performance of these rootstock genotypes indicated that CC was the most tolerant while TO was the most sensitive to B-deficiency. In addition, under B-deficiency conditions, not only the B concentration, but also the other mineral nutrient concentrations were influenced, especially in Mg, Fe and Mn. This change in nutrient concentrations might partly contribute to the seedlings’ physiological performances under B-deficiency.


Boron deficiency Citrus rootstock Visual symptom Physiological performance Mineral nutrients 



This work was supported by the National Natural Science Foundation of China (30871687 and 31071761). We are grateful to Dr. Huoyan Wang (Institute of Soil Science, Chinese Academy of Sciences) for his valuable technical assistance on this experiment.

Conflict of interest

The authors declare that they have no competing interests.


  1. Bolaños L, Lukaszewski K, Bonilla I, Blevins D (2004) Why boron? Plant Physiol Biochem 42:907–912PubMedCrossRefGoogle Scholar
  2. Brown PH, Bellaloui N, Wimmer MA (2002) Boron in plant biology. Plant Biol 4:205–223CrossRefGoogle Scholar
  3. Camacho-Cristóbal JJ, González-Fontes A (2007) Boron deficiency decreases plasmalemma H+-ATPase expression and nitrate uptake, and promotes ammonium assimilation into asparagine in tobacco roots. Planta 226:443–451PubMedCrossRefGoogle Scholar
  4. Dell B, Huang LB (1997) Physiological response of plants to low boron. Plant Soil 193:103–120CrossRefGoogle Scholar
  5. Edelstein M, Ben-Hur M, Cohen R, Burger Y, Ravina I (2005) Boron and salinity effects on grafted and non-grafted melon plants. Plant Soil 269:273–284CrossRefGoogle Scholar
  6. El-Motaium R, Hu H, Brown PH (1994) The relative tolerance of six prunus rootstocks to boron and salinity. J Am Soc Hortic Sci 119:1169–1175Google Scholar
  7. Forner-Giner MA, Alcaide A, Primo-Millo E, Forner JB (2003) Performance of ‘Navelina’ orange on 14 rootstocks in Northern Valencia (Spain). Sci Hortic 98:223–232CrossRefGoogle Scholar
  8. Han S, Chen LS, Jiang HX, Smith BR, Yang LT, Xie CY (2008) Boron deficiency decreases growth and photosynthesis, and increases starch and hexoses in leaves of citrus seedlings. J Plant Physiol 165:1331–1341PubMedCrossRefGoogle Scholar
  9. 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 176:143–153CrossRefGoogle Scholar
  10. Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266PubMedCrossRefGoogle Scholar
  11. Hoagland DR, Arnon DS (1950) The water culture method for growing plants without soil. Cal Agric Exp St Circ 347:305–311Google Scholar
  12. Kato Y, Miwa K, Takano J, Wada M, Fujiwara T (2008) Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant Cell Physiol 50:58–66PubMedCrossRefGoogle Scholar
  13. Kocábek T, Svoboda Z, Al-Zwi AM, Rolfe SA, Fellner M (2009) Boron-regulated hypocotyl elongation is affected in Arabidopsis mutants with defects in light signalling pathways. Environ Exp Bot 67:101–111CrossRefGoogle Scholar
  14. Koshiba T, Kobayashi M, Ishihara A, Matoh T (2010) Boron nutrition of cultured tobacco BY-2 cells. VI. Calcium is involved in early responses to boron deprivation. Plant Cell Physiol 51:323–327PubMedCrossRefGoogle Scholar
  15. Lisa CW, Sebastien PCR, Ribriowx Alasrair HF (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–8821CrossRefGoogle Scholar
  16. Liu J, Han L, Chen F, Bao J, Zhang F, Mi G (2008) Microarray analysis reveals early responsive genes possibly involved in localized nitrate stimulation of lateral root development in maize (Zea mays L.). Plant Sci 175:272–282CrossRefGoogle Scholar
  17. Liu GD, Jiang CC, Wang YH (2011) Distribution of boron and its forms in young “Newhall” navel orange (Citrus sinensis Osb.) plants grafted on two rootstocks in response to deficient and excessive boron. Soil Sci Plant Nutr 57:93–104CrossRefGoogle Scholar
  18. López-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287PubMedCrossRefGoogle Scholar
  19. Lukaszewski KM, Blevins DG (1998) Boron in plant structure and function. Annu Rev Plant Biol 49:481–500Google Scholar
  20. Maathuis FJM (2009) Physiological functions of mineral macronutrients. Curr Opin Plant Biol 12:250–258PubMedCrossRefGoogle Scholar
  21. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, LondonGoogle Scholar
  22. Matas MA, González-Fontes A, Camacho-Cristóbal JJ (2009) Effect of boron supply on nitrate concentration and its reduction in roots and leaves of tobacco plants. Biol Plant 53:120–124CrossRefGoogle Scholar
  23. Mei L, Sheng O, Peng SA, Zhou GF, Wei QJ, Li QH (2011) Growth, root morphology and boron uptake by citrus rootstock seedlings differing in boron-deficiency responses. Sci Hortic 129:426–432CrossRefGoogle Scholar
  24. Mourão Filho FDAA, Espinoza-Núñez E, Stuchi ES, Ortega EMM (2007) Plant growth, yield, and fruit quality of ‘Fallglo’ and ‘Sunburst’ mandarins on four rootstocks. Sci Hortic 114:45–49CrossRefGoogle Scholar
  25. Norton GJ, Deacon CM, Xiong LZ, Huang SY, Meharg AA, Price AH (2010) Genetic mapping of the rice ionome in leaves and grain: identification of QTLs for 17 elements including arsenic, cadmium, iron and selenium. Plant Soil 329:139–153CrossRefGoogle Scholar
  26. 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 166:539–547CrossRefGoogle Scholar
  27. 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 51:247–257CrossRefGoogle Scholar
  28. Quiles-Pando C, Rexach J, Navarro-Gochicoa MT, Camacho-Cristóbal JJ, Herrera-Rodríguez MB, González-Fontes A (2013) Boron deficiency increases the levels of cytosolic Ca2+ and expression of Ca2+-related genes in Arabidopsis thaliana roots. Plant Physiol Biochem 65:55–60PubMedCrossRefGoogle Scholar
  29. Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59:709–733PubMedCrossRefGoogle Scholar
  30. Sánchez-Rodríguez E, MdM Rubio-Wilhelmi, Cervilla LM, Blasco B, Rios JJ, Leyva R, Romero L, Ruiz JM (2010) Study of the ionome and uptake fluxes in cherry tomato plants under moderate water stress conditions. Plant Soil 335:339–347CrossRefGoogle Scholar
  31. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417PubMedCentralPubMedGoogle Scholar
  32. Sha ZM, Oka N, Watanabe T, Tampubolon BD, Okazaki K, Osaki M, Shinano T (2012) Ionome of soybean seed affected by previous cropping with mycorrhizal plant and manure application. J Agric Food Chem 60:9543–9552PubMedCrossRefGoogle Scholar
  33. Sheng O, Song SW, Chen YJ, Peng SA, Deng XX (2008) Effects of exogenous boron supply on growth, B accumulation and distribution of two navel orange cultivars. Trees 23:59–68CrossRefGoogle Scholar
  34. Sheng O, Song SW, Peng SA, Deng XX (2009) The effects of low boron on growth, gas exchange, boron concentration and distribution of ‘Newhall’ navel orange (Citrus sinensis Osb.) plants grafted on two rootstocks. Sci Hortic 121:278–283CrossRefGoogle Scholar
  35. Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148CrossRefGoogle Scholar
  36. Smith MW, Shaw RG, Chapman JC, Owen-Turner J, Slade Lee L, Bruce McRae K, Jorgensen KR, Mungomery WV (2004) Long-term performance of ‘Ellendale’ mandarin on seven commercial rootstocks in sub-tropical Australia. Sci Hortic 102:75–89CrossRefGoogle Scholar
  37. Sofo A, Scopa A, Manfra M, De Nisco M, Tenore GC, Nuzzo V (2013) Different water and light regimes affect ionome composition in grapevine (Vitis vinifera L.). Vitis 52:13–20Google Scholar
  38. Storey R, Treeby MT (2000) Nutrient uptake into navel orange during fruit development. J Hortic Sci Biotechnol 77:91–99Google Scholar
  39. Wójcik P, Lewandowski M (2003) Effect of calcium and boron sprays on yield and quality of “Elsanta” strawberry. J Plant Nutr 26:671–682CrossRefGoogle Scholar
  40. Xiao JX, Yang X, Peng SA, Fang YW (2007) Seasonal changes of mineral nutrients in fruit and leaves of ‘Newhall’ and ‘Skagg’s Bonanza’ navel orange. J Plant Nutr 30:671–690CrossRefGoogle Scholar
  41. Zhu JH, Geng MJ, Cao XY, Song SW, Liu WD (2001) Uptake and distribution of B, K, Ca, Mg in cotton cultivars responding differently to B deficiency. J Huazhong Agric Univ 20:134–137Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Gao F. Zhou
    • 1
  • Shu A. Peng
    • 1
    Email author
  • Yong Z. Liu
    • 1
  • Qing J. Wei
    • 1
  • Jia Han
    • 1
  • Md. Zahidul Islam
    • 1
  1. 1.Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry ScienceHuazhong Agricultural UniversityWuhanChina

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