Boron response in wheat is genotype-dependent and related to boron uptake, translocation, allocation, plant phenological development and growth rate
Monika A. Wimmer A D , Elias S. Bassil B , Patrick H. Brown B and André Läuchli CA Institute of Plant Nutrition, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany.
B Department of Pomology, University of California, Davis CA 95616, USA.
C Department of Land, Air and Water Resources, University of California, Davis CA 95616, USA.
D Corresponding author. Email: m.wimmer@uni-bonn.de
Functional Plant Biology 32(6) 507-515 https://doi.org/10.1071/FP04165
Submitted: 10 September 2004 Accepted: 30 March 2005 Published: 15 June 2005
Abstract
Wheat genotypes often differ significantly in their response to low and high boron (B) supply, although the underlying mechanisms for such differences are poorly understood. The stable isotopes 10B and 11B were used to investigate the contribution of root retention, uptake rates, translocation and allocation of B within wheat (Triticum aestivum L.) genotypes known to differ in B response. At high B supply, the tolerant GREEK had reduced B concentrations in main shoot leaves associated with lower uptake rates and increased allocation of B to tillers. The equally tolerant BT-SCHOMBURGK exhibited high uptake rates, but accumulation was low because of rapid development, lower concentrations of soluble B in the cell sap and lower B translocation to the shoot. In WlMMC, high uptake rates, slow development, high translocation and allocation to main shoots resulted in high B accumulation and poor tolerance. Retention in roots was not substantial in any of the genotypes. The results suggest that B tolerance is multi-faceted and genotype specific. Mechanisms contributing to B tolerance include reduced uptake rates and differential translocation and allocation within plants. Additionally, plant growth rate and leaf morphology can influence B response by affecting tissue concentrations and allowing completion of plant maturation before B accumulation impairs growth. These mechanisms are expressed to different extents depending on the genotype.
Keywords: genotypic variation, stable isotopes, Triticum aestivum.
Acknowledgments
This work was supported by the California Agricultural Experiment Station. We thank Mr Anthony McCloskey from the Australian Winter Cereal Collection for providing seeds of the wheat genotypes.
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 |
Blevins DG, Lukaszewski KM
(1998) Boron in plant structure and function. Annual Review of Plant Physiology and Plant Molecular Biology 49, 481–500.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Blumenkrantz N, Asboe-Hansen G
(1973) New method for quantitative determination of uronic acids. Analytical Biochemistry 54, 484–489.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brown PH, Shelp BJ
(1997) Boron mobility in plants. Plant and Soil 193, 85–101.
| 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 |
Cartwright B,
Zarcinas BA, Mayfield AH
(1984) Toxic concentrations of boron in a red-brown earth at Gladstone, South Australia. Australian Journal of Soil Research 22, 261–272.
| Crossref |
Cartwright B,
Zarcinas BA, Spouncer LR
(1986) Boron toxicity in South Australian barley crops. Australian Journal of Agricultural Research 37, 351–359.
| Crossref | GoogleScholarGoogle Scholar |
Dannel F,
Pfeffer H, Römheld V
(1999) Distribution within the plant or compartmentation does not contribute substantially to the detoxification of excess boron in sunflower (Helianthus annuus). Australian 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. 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 |
Goldbach HE
(1997) A critical review on current hypotheses concerning the role of boron in higher plants: suggestions for further research and methodological requirements. Journal of Trace and Microprobe Techniques 15, 51–91.
Hu H,
Brown PH, Labavitch JM
(1996) Species variability in boron requirement is correlated with cell wall pectin. Journal of Experimental Botany 47, 227–232.
Huang C, Graham RD
(1990) Resistance of wheat genotypes to boron toxicity is expressed at the cellular level. Plant and Soil 126, 295–300.
| Crossref | GoogleScholarGoogle Scholar |
Ishii T,
Matsunaga T, Hayashi N
(2001) Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiology 126, 1698–1705.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jefferies SP,
Pallotta MA,
Paull JG,
Karakousis A,
Kretschmer JM,
Manning S,
Islam AKMR,
Langridge P, Chalmers KJ
(2000) Mapping and validation of chromosome regions conferring boron toxicity tolerance in wheat (Triticum aestivum). Theoretical and Applied Genetics 101, 767–777.
| Crossref | GoogleScholarGoogle Scholar |
Kobayashi M,
Matoh T, Azuma J-I
(1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiology 110, 1017–1020.
| PubMed |
Nable RO
(1988) Resistance to boron toxicity amongst several barley and wheat cultivars: a preliminary examination of the resistance mechanism. Plant and Soil 112, 45–52.
Nable RO
(1991) Distribution of boron within barley genotypes with differing susceptibilities to boron toxicity. Journal of Plant Nutrition 14, 453–461.
Nable RO,
Paull JG, Cartwright B
(1990) Problems associated with the use of foliar analysis for diagnosing boron toxicity in barley. Plant and Soil 128, 225–232.
| Crossref | GoogleScholarGoogle Scholar |
Nable RO,
Banuelos GS, Paull JG
(1997) Boron toxicity. Plant and Soil 193, 181–198.
| Crossref | GoogleScholarGoogle Scholar |
O'Neill MA,
Warrenfeltz D,
Kates K,
Pellerin P,
Doco T,
Darvill AG, Albersheim P
(1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. Journal of Biological Chemistry 271, 22923–22930.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Paull JG,
Cartwright B, Rathjen AJ
(1988) Responses of wheat and barley genotypes to toxic concentrations of soil boron. Euphytica 39, 137–144.
| Crossref | GoogleScholarGoogle Scholar |
Paull JG,
Rathjen AJ, Cartwright B
(1991) Tolerance to high concentrations of boron for the amphiploid of Triticum aestivum × Agropyron elongatum. Plant and Soil 133, 297–299.
| Crossref | GoogleScholarGoogle Scholar |
Paull JG,
Nable RO, Rathjen AJ
(1992a) Physiological and genetic control of the tolerance of wheat to high concentrations of boron and implications for plant breeding. Plant and Soil 146, 251–260.
| Crossref | GoogleScholarGoogle Scholar |
Paull JG,
Nable RO,
Lake AWH,
Materne MA, Rathjen AJ
(1992b) Response of annual medics (Medicago spp.) and field peas (Pisum sativum) to high concentrations of boron: genetic variation and the mechanism of tolerance. Australian Journal of Agricultural Research 43, 203–213.
| Crossref | GoogleScholarGoogle Scholar |
Raven JA
(1980) Short- and long-distance transport of boric acid in plants. New Phytologist 84, 231–249.
Rerkasem B, Jamjod S
(1997a) Boron deficiency induced male sterility in wheat (Triticum aestivum L.) and implications for plant breeding. Euphytica 96, 257–262.
| Crossref | GoogleScholarGoogle Scholar |
Rerkasem B, Jamjod S
(1997b) Genotypic variation in plant response to low boron and implications for plant breeding. Plant and Soil 193, 169–180.
| Crossref | GoogleScholarGoogle Scholar |
Reuhs BL,
Glenn J,
Stephens SB,
Kim JS,
Christie BD,
Glushka JG,
Zablackis E,
Albersheim P,
Darvill AG, O’Neill MA
(2004)
l-Galactose replaces l-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the l-fucose-deficient mur1 Arabidopsis mutant. Planta 219, 147–157.
| Crossref | l-Galactose replaces l-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the l-fucose-deficient mur1 Arabidopsis mutant.&journal=Planta&volume=219&pages=147-157&publication_year=2004&author=MA%20O%E2%80%99Neill&hl=en&doi=10.1007/s00425-004-1205-x" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |
Shelp BJ,
Marentes E,
Kitheka AM, Vivekanandan P
(1995) Boron mobility in plants. Physiologia Plantarum 94, 356–361.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Stangoulis JCR,
Brown PH,
Bellaloui N,
Reid RJ, Graham RD
(2001) The efficiency of boron utilisation in canola. Australian Journal of Plant Physiology 28, 1109–1114.
Williams RF
(1948) The effect of phosphorus supply on the rate of intake of phosphorus and nitrogen and upon certain aspects of phosphorus metabolism in gramineous plants. Australian Journal of Scientific Research B1, 333–361.
Wimmer MA,
Mühling KH,
Läuchli A,
Brown PH, Goldbach HE
(2003) The interaction between salinity and boron toxicity affects the subcellular distribution of ions and proteins in wheat leaves. Plant, Cell & Environment 26, 1267–1274.
| Crossref | GoogleScholarGoogle Scholar |
Zadok JC,
Chang TT, Konzak CF
(1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–420.