Low-boron acclimation induces uptake of boric acid against a concentration gradient in root cells of Olea europaea
Sotiria Stavrianakou A , Georgios Liakopoulos A B , Evangelos Karvonis A , Evangelia Resta A and George Karabourniotis AA Laboratory of Plant Physiology, Department of Agricultural Biotechnology, Agricultural University of Athens, Iera Odos 75, Botanikos 11855, Athens, Greece.
B Corresponding author. Email: g_liak@aua.gr
Functional Plant Biology 33(2) 189-193 https://doi.org/10.1071/FP05097
Submitted: 26 April 2005 Accepted: 26 August 2005 Published: 3 February 2006
Abstract
Low concentrations of boron (B) in the external medium can induce uptake mechanisms whereby plants can develop a concentration gradient for B against the external medium. These mechanisms seem to be widespread among herbaceous species. In this study, olive (Olea europaea L.) plants were acclimated to either high (23 μm; controls) or low (0.5 μm; low-B plants) concentrations of B for 45 d, in a hydroponic culture. Afterwards, a 7-h uptake experiment was conducted by transferring plants of both groups to a series of nutrient solutions with B concentrations ranging from 0.5 to 23 μm. Analysis of B concentration in cell sap of root and xylem exudate was performed by the borate–chromotropic acid HPLC assay. Plants acclimated to high-B concentration showed root cell and xylem exudate B concentrations that were comparable to those of the external medium. In contrast, plants acclimated to low-B concentration were able to develop concentrations of B in root cells up to 2-fold higher than those of the external medium. Moreover, B concentrations in xylem exudate for both plant groups corresponded to those of the root cell sap, indicating diffusion equilibrium. These results support the existence of a mechanism that concentrates B in the root cell sap against the nutrient solution when olive plants are acclimated to low-B conditions.
Keywords: chromotropic acid, HPLC assay, olive tree, root cell sap, xylem exudates.
Acknowledgments
We thank Mr G Kostelenos (Kostelenos Olive Nurseries) for supplying the plant material.
Asad A,
Bell RW,
Dell B, Huang L
(1997) External boron requirements for canola (Brassica napus L.) in boron buffered solution culture. Annals of Botany 80, 65–73.
| Crossref | GoogleScholarGoogle Scholar |
Asad A,
Bell RW, Dell B
(2001) A critical comparison of the external and internal boron requirements for contrasting species in boron-buffered solution culture. Plant and Soil 233, 31–45.
| Crossref | GoogleScholarGoogle 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 and Soil 198, 153–158.
| Crossref | GoogleScholarGoogle Scholar |
Brown JC, Jones WE
(1971) Differential transport of boron in tomato. Plant Physiology 25, 279–282.
Brown PH,
Bellaloui N,
Wimmer MA,
Bassil ES,
Ruiz J,
Hu H,
Pfeffer H,
Dannel F, Römheld V
(2002) Boron in plant biology. Plant Biology 4, 205–223.
| Crossref | GoogleScholarGoogle Scholar |
Chapman, VJ ,
Edwards, DG ,
Blamey, FPC ,
and
Asher, CJ (1997). Challenging the dogma of a narrow supply range between deficiency and toxicity of boron. In ‘Boron in soils and plants’. pp. 151–155. (Kluwer Academic Publishers: The Netherlands)
Dannel, F ,
Pfeffer, H ,
and
Römheld, V (1997). Effect of pH and boron concentration in the nutrient solution on translocation of boron in the xylem of sunflower. In ‘Boron in soils and plants’. pp. 183–186. (Kluwer Academic Publishers: The Netherlands)
Dannel F,
Pfeffer H, Römheld V
(1998) Compartmentation of boron in roots and leaves of sunflower as affected by boron supply. Journal of Plant Physiology 153, 615–622.
Dannel F,
Pfeffer H, Römheld V
(2000) Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotopes 10B and 11B. Australian Journal of Plant Physiology 27, 397–405.
Dannel F,
Pfeffer H, Römheld V
(2002) Update on boron in higher plants. Uptake, primary translocation and compartmentation. Plant Biology 4, 193–204.
| Crossref | GoogleScholarGoogle Scholar |
Dordas C, Brown PH
(2000) Permeability of boric acid across lipid bilayers and factors affecting it. Journal of Membrane Biology 175, 95–105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dordas C, Brown PH
(2001) Evidence for channel mediated transport of boric acid in squash (Cucurbita pepo). Plant and Soil 235, 95–103.
| Crossref | GoogleScholarGoogle Scholar |
Dordas C,
Chrispeels MJ, Brown PH
(2000) Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiology 124, 1349–1361.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hu H, Brown PH
(1994) Localisation of boron in cell walls of squash and tobacco and its association with pectin; evidence for a structural role of boron in cell wall. Plant Physiology 105, 681–689.
| PubMed |
Hu H, Brown PH
(1997) Absorption of boron by plant roots. Plant and Soil 193, 49–58.
| Crossref | GoogleScholarGoogle Scholar |
Liakopoulos G, Karabourniotis G
(2005) Boron deficiency and concentrations and composition of phenolic compounds in Olea europaea leaves: a combined growth chamber and field study. Tree Physiology 25, 307–315.
| PubMed |
Liakopoulos G,
Stavrianakou S,
Filippou M,
Fasseas K,
Tsadilas C,
Drossopoulos I, Karabourniotis G
(2005) Boron remobilization at low boron supply in olive (Olea europaea) in relation to leaf and phloem mannitol concentrations. Tree Physiology 25, 157–165.
| PubMed |
Lo Gullo AM, Salleo S
(1988) Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. New Phytologist 108, 267–276.
Loomis WD, Durst RW
(1992) Chemistry and biology of boron. BioFactors 3, 229–239.
| PubMed |
Matoh T,
Akaike R, Kobayashi M
(1997) A sensitive and convenient assay for boron in plant using chromotropic acid and HPLC. Plant and Soil 192, 115–118.
| Crossref | GoogleScholarGoogle Scholar |
Noguchi K,
Dannel F,
Pfeffer H,
Römheld V,
Hayashi H, Fujiwara T
(2000) Defect in root–shoot translocation of boron in Arabidopsis thaliana mutant bor1-1. Journal of Plant Physiology 156, 751–755.
Pfeffer H,
Dannel F, Römheld V
(2001) Boron compartmentation in roots of sunflower plants of different boron status: a study using the stable isotopes 10B and 11B adopting two independent approaches. Physiologia Plantarum 113, 346–351.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pfeffer H,
Dannel F, Römheld V
(1999) Are there two mechanisms for boron uptake in sunflower? Journal of Plant Physiology 155, 34–40.
Power PP, Woods WG
(1997) The chemistry of boron and its speciation in plants. Plant and Soil 193, 1–13.
| Crossref | GoogleScholarGoogle Scholar |
Raven JA
(1980) Short- and long-distance transport of boric acid in plants. New Phytologist 84, 231–249.
Stangoulis JCR,
Reid RJ,
Brown PH, Graham RD
(2001) Kinetic analysis of boron transport in Chara. Planta 213, 142–146.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shelp BJ,
Kitheka AM,
Vanderpool RA,
Van Cauwenberghe OR, Spiers GA
(1998) Xylem-to-phloem transfer of boron in broccoli and lupin during early reproductive growth. Physiologia Plantarum 104, 533–540.
| Crossref | GoogleScholarGoogle Scholar |
Sofo A,
Dichio B,
Xiloyannis C, Masia A
(2005) Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Functional Plant Biology 32, 45–53.
| Crossref | GoogleScholarGoogle Scholar |
Takano J,
Noguchi K,
Yasumori M,
Kobayashi M,
Gajdos Z,
Miwa K,
Hayashi H,
Yoneyama T, Fujiwara T
(2002) Arabidopsis boron transporter for xylem loading. Nature 420, 337–340.
| Crossref | GoogleScholarGoogle Scholar | PubMed |