Boron uptake by the root cortex symplast of tomato and pea plants: evidence for low-boron-induced active transport
Jasna Savic A C , Miroslav Nikolic B D , Slaven Prodanovic A and Volker Römheld CA Faculty of Agriculture, University of Belgrade, 11080 Zemun-Belgrade, Serbia.
B Department of Natural Resources and Environmental Sciences, Centre for Multidisciplinary Studies, University of Belgrade, 11030 Belgrade, Serbia.
C Institute of Plant Nutrition (330), University of Hohenheim, 70593 Stuttgart, Germany.
D Corresponding author. Email: mnikolic@cms.bg.ac.yu
Functional Plant Biology 34(12) 1130-1136 https://doi.org/10.1071/FP07175
Submitted: 16 July 2007 Accepted: 23 October 2007 Published: 27 November 2007
Abstract
The objective of this research was to test the hypothesis of the existence of an active boron (B) uptake into the cortical cells induced by low B supply. The uptake of B was characterised in two tomato (Lycopersicon esculentum Mill.) genotypes: B-efficient FER and B-inefficient mutant T3238. In addition, pea (Pisum sativum L.) was used as an anatomically appropriate model for obtaining intact root cortex. Time course uptake studies in tomato indicate that the B-inefficient mutant was defective by the absence of an active low-B-induced uptake system in the cortex. Pea roots showed up to 10-fold higher accumulation of B into the cortex symplast at low (0.5 µm) external B supply in comparison to adequate B (10 µm) supply. Also, low-B-induced uptake of B was strongly inhibited by 2,4-dinitrophenol, indicating a metabolic energy-derived active component of B uptake at low external supply. Uptake of B by the cortical cells of tomato and pea plants appears to be a combination of both passive and active components, with a passive component prevailing at higher external B. An active component of B uptake suppressed by either adequate or high B supply might indicate a downregulation of plasma membrane-associated B transporter(s) in root cortical cells.
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 |
Bellaloui N,
Brown PH, Dandekar AM
(1999) Manipulation of in vivo sorbitol production alters boron uptake and transport in tobacco. Plant Physiology 119, 735–741.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brown JC
(1979) Effect of boron stress on copper enzyme and activity in tomato. Journal of Plant Nutrition 1, 39–53.
Brown JC, Jones WE
(1971) Differential transport of boron in tomato. Plant Physiology 25, 279–282.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Brown PH, Hu H
(1994) Boron uptake by sunflower, squash and cultured tobacco cells. Physiologia Plantarum 91, 435–441.
| Crossref | GoogleScholarGoogle Scholar |
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 26, 95–99.
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. The Journal of Membrane Biology 175, 95–105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
Hayes JE, Reid RE
(2004) Boron tolerance in barley is mediated by efflux of boron from the roots. Plant Physiology 136, 3376–3382.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hu H, Brown PH
(1997) Absorption of boron by plant roots. Plant and Soil 193, 49–58.
| Crossref | GoogleScholarGoogle Scholar |
Hu H,
Brown PH, Labavitch JM
(1996) Species variability in boron requirements is correlated with cell wall pectin. Journal of Experimental Botany 47, 227–232.
| Crossref | GoogleScholarGoogle Scholar |
Kochian LV, Lucas WJ
(1982) Potassium transport in corn roots. I. Resolution of kinetics into a saturable and linear component. Plant Physiology 70, 1723–1731.
| PubMed |
Lasat MM,
Baker AJM, Kochian LV
(1996) Physiological characterisation of root Zn2+ absorbtion and translocation to shoots in Zn hyper-accumulator and nonaccumulator species of Thlaspi. Plant Physiology 112, 1715–1722.
| PubMed |
Nikolic M,
Nikolic N,
Liang Y,
Kirkby EA, Römheld V
(2007) Germanium-68 as an adequate tracer for silicon transport in plants. Characterization of silicon uptake in different crop species. Plant Physiology 143, 495–503.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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.
Noguchi K,
Yasumori M,
Imai T,
Naito S,
Matsunaga T,
Oda H,
Hayashi H,
Chino M, Fujiwara T
(1997) bor1–1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiology 115, 901–906.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pfeffer H,
Dannel F, Römheld V
(1999) Are there two mechanisms for boron uptake in sunflower? Journal of Plant Physiology 154, 283–288.
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 |
Raven JA
(1980) Short-and-long distance transport of boric acid in plants. The New Phytologist 84, 231–249.
| Crossref | GoogleScholarGoogle Scholar |
Siddiqi MY,
Glass ADM,
Ruth TJ, Rufty TWJ
(1990) Studies on the uptake of nitrate in barley. I. Kinetics of 13NO3-influx. Plant Physiology 93, 1426–1432.
| PubMed |
Stangoulis JCR,
Grewal HS,
Bell RW, Graham RD
(2000) Boron efficiency in oilseed rape. I. Genotypic variation demonstrated in field and pot grown Brassica napus L. and Brassica juncea L. Plant and Soil 225, 243–251.
| Crossref | GoogleScholarGoogle Scholar |
Stangoulis JCR,
Reid RJ,
Brown PH, Graha RD
(2001) Kinetic analysis of boron transport in Chara. Planta 213, 142–146.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stavrianakou S,
Liakopulos G,
Karvonis E,
Resta E, Karabourniotis G
(2006) Low-boron acclimation induces uptake of boric acid against a concentration gradient in root cells of Olea europea. Functional Plant Biology 33, 189–193.
| Crossref | GoogleScholarGoogle Scholar |
Takano J,
Miwa K,
Yuan L,
von Wirén N, Fujiwara T
(2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proceedings of the National Academy of Sciences of the United States of America 102, 12276–12281.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
Takano J,
Wada M,
Ludewig U,
Schaaf G,
von Wirén N, Fujiwara T
(2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. The Plant Cell 18, 1498–1509.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Thellier M,
Duval Y, Demarty M
(1979) Borate exchanges of Lemna minor L. as studied with help of enriched stable isotopes and of a (n,α) nuclear reaction. Plant Physiology 63, 283–288.
| PubMed |
Wall JR, Andrus CF
(1962) The inheritance and physiology of boron response in the tomato. American Journal of Botany 49, 758–762.
| Crossref | GoogleScholarGoogle Scholar |
