Abstract
Boron remobilization (BR) occurs in plants that form and export phloem–mobile borate–polyol complexes. Previous studies demonstrate that a quantitative relationship exists between polyol translocation and BR. Here we investigate if mannitol translocation is quantitatively related to BR in olive plants thus allowing acclimation to boron limiting conditions. Plants were cultivated under different boron supply ranging from adequate (23 μM) to insufficient or zero supply (0.5 μM or 0 μM). Measurement of boron in the leaf phloem sap exudates (BP) of olive leaves of low or zero boron supply treatments showed that, whereas boron was remobilized, its absolute amounts in the phloem were lower compared to the control. However, BR from source leaves at 0.5 μM or 0 μM was maintained at relatively high levels in regard to the amounts of boron available in the cells of these leaves, indicating a strategy of the source leaves to remobilize boron by depleting their cell sap boron pool. Concurrently, in the above treatments, leaf phloem mannitol (MP) was up to two-fold higher, resulting in a up to five-fold higher ratio of mannitol to boron in the phloem (MP/BP), compared to the control. Furthermore, both MP and MP/BP were negatively correlated with cell sap boron concentration of the leaves indicating the trend for BR under boron limitation. It is concluded that, in this plant species, mannitol concentrations in the leaf phloem may be involved in the promotion of BR under inadequate external supply of boron.
Similar content being viewed by others
Abbreviations
- BR:
-
Boron remobilization
- MP :
-
Mannitol concentration in phloem sap exudates
- BP :
-
Boron concentration in leaf phloem sap exudates
- BC :
-
Boron concentration in cell sap (plus apoplastic fluid)
- B23/B05/B0:
-
23 μM/0.5 μM/0 μM boron nutrient solution treatments
References
Banuelos GS, Cardon G, Pflaum T, Akohoue S (1992) Comparison of dry ashing and wet acid digestion on the determination of boron in plant tissue. Commun Soil Plant Anal. 23:2383–2397. doi:10.1080/00103629209368745
Bellaloui N, Brown PH, Dandekar AM (1999) Manipulation of in vivo sorbitol production alters boron uptake and transport in tobacco. Plant Physiol 119:735–741. doi:10.1104/pp.119.2.735
Bellaloui N, Yadavc RC, Chern M-S, Hu H, Gillen AM, Greve C, Dandekar AM, Ronald PC, Brown PH (2003) Transgenically enhanced sorbitol synthesis facilitates phloem-boron mobility in rice. Physiol Plant 117:79–84. doi:10.1034/j.1399-3054.2003.1170110.x
Brown PH, Hu H (1996) Phloem mobility of boron is species dependent: evidence for phloem mobility in sorbitol-rich species. Ann Bot (Lond) 77:497–505. doi:10.1006/anbo.1996.0060
Brown PH, Hu H (1997) Does boron play only a structural role in the growing tissues of higher plants. Plant Soil 196:211–215. doi:10.1023/A:1004245823080
Brown PH, Shelp BJ (1997) Boron mobility in plants. Plant Soil 193:85–101. doi:10.1023/A:1004211925160
Brown PH, Bellaloui N, Hu H, Dandekar A (1999) Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency. Plant Physiol 119:17–20. doi:10.1104/pp.119.1.17
Cakmak I, Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193:71–83. doi:10.1023/A:1004259808322
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. Aust J Plant Physiol 27:397–405
Dannel F, Pfeffer H, Römheld V (2002) Update on boron in higher plants—uptake, primary translocation and compartmentation. Plant Biol 4:193–204. doi:10.1055/s-2002-25730
Delgado A, Benlloch M, Fernández-Escobar R (1994) Mobilization of boron in olive trees during flowering and fruit development. HortScience 29:616–618
Fisher DB, Frame JM (1984) A guide to the use of the exuding-stylet technique in phloem physiology. Planta 161:385–393. doi:10.1007/BF00394567
Flora LL, Madore MA (1993) Stachyose and mannitol transport in olive (Olea europaea L.). Planta 189:484–490. doi:10.1007/BF00198210
Hu H, Brown PH (1994) Localization of boron in cell walls of squash and tobacco and its association with pectin. Evidence for a structural role of boron in the cell wall. Plant Physiol 105:681–689
Hu H, Penn SG, Lebrilla CB, Brown PH (1997) Isolation and characterization of soluble boron complexes in higher plants. Plant Physiol 113:649–655. doi:10.1104/pp.113.2.649
Huang L, Bell RW, Dell B (2008) Evidence of phloem boron transport in response to interrupted boron supply in white lupin (Lupinus albus L. cv. Kiev Mutant) at the reproductive stage. J Exp Bot 59:575–583. doi:10.1093/jxb/erm336
Jiang F, Jeschke WD, Hartung W, Cameron DD (2008) Mobility of boron–polyol complexes in the hemiparasitic association between Rhinanthus minor and Hordeum vulgare: the effects of nitrogen nutrition. Physiol Plant 134:13–21. doi:10.1111/j.1399-3054.2008.01116.x
King RW, Zeevaart JAD (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiol 53:96–103. doi:10.1104/pp.53.1.96
Lehto T, Kallio E, Aphalo PJ (2000) Boron mobility in two coniferous species. Ann Bot (Lond) 86:547–550. doi:10.1006/anbo.2000.1215
Lehto T, Lavola A, Julkunen-Tiitto R, Aphalo PJ (2004a) Boron retranslocation in Scots pine and Norway spruce. Tree Physiol 24:1011–1017
Lehto T, Raisanen M, Lavola A, Julkunen-Tiitto R, Aphalo PJ (2004b) Boron mobility in deciduous forest trees in relation to their polyols. New Phytol 163:333–339. doi:10.1111/j.1469-8137.2004.01105.x
Leite VM, Brown PH, Rosolem CA (2007) Boron translocation in coffee trees. Plant Soil 290:221–229. doi:10.1007/s11104-006-9154-8
Liakopoulos G, Stavrianakou S, Flippou M, Fasseas C, 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 Physiol 25:157–165
Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3:229–239
Matoh T (1997) Boron in plant cell walls. Plant Soil 193:59–70. doi:10.1023/A:1004207824251
Matoh T, Akaike R, Kobayashi M (1997) A sensitive and convenient assay for boron in plant using chromotropic acid and HPLC. Plant Soil 192:115–118. doi:10.1023/A:1004228216749
Matoh T, Ochiai K (2005) Distribution and partitioning of newly taken-up boron in sunflower. Plant Soil 278:351–360. doi:10.1007/s11104-005-0372-2
Penn SG, Hu H, Brown PH, Lebrilla CB (1997) Direct analysis of sugar alcohol borate complexes in plant extracts, by matrix assisted laser desorption Fourier transform mass spectrometry (MALDI-FTMS). Anal Chem 69:2471–2477. doi:10.1021/ac970101o
Perica S, Brown PH, Connell JH, Nyomora AMS, Dordas C, Hu H, Stangoulis J (2001) Foliar boron application improves flower fertility and fruit set of olive. HortScience 36:714–716
Pfeffer H, Dannel F, Römheld V (1999) Isolation of soluble boron complexes and their determination together with free boric acid in higher plants. J Plant Physiol 154:283–288
Power P, Woods WG (1997) The chemistry of boron and its speciation in plants. Plant Soil 193:1–13. doi:10.1023/A:1004231922434
Raven JA (1980) Short- and long-distance transport of boric acid in plants. New Phytol 84:231–249. doi:10.1111/j.1469-8137.1980.tb04424.x
Stangoulis JCR, Brown PH, Bellaloui N, Reid RJ, Graham RD (2001) The efficiency of boron utilization in canola. Aust J Plant Physiol 28:1109–1114
Stavrianakou S, Liakopoulos 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 europaea. Funct Plant Biol 33:189–193. doi:10.1071/FP05097
Acknowledgements
Authors thank Dr. Mariangela N. Fotelli for useful suggestions during manuscript preparation and Mr. G. Kostelenos (Kostelenos Olive Nurseries) for the supply of plant material.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Richard Bell.
Georgios Liakopoulos and Sotiria Stavrianakou have equally contributed to this work
Rights and permissions
About this article
Cite this article
Liakopoulos, G., Stavrianakou, S., Nikolopoulos, D. et al. Quantitative relationships between boron and mannitol concentrations in phloem exudates of Olea europaea leaves under contrasting boron supply conditions. Plant Soil 323, 177–186 (2009). https://doi.org/10.1007/s11104-009-9923-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-009-9923-2