Skip to main content
Log in

Analysis of genetic factors that control shoot mineral concentrations in rapeseed (Brassica napus) in different boron environments

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Mineral nutrients are essential for plant cell function, and understanding the genetic and physiological basis of mineral concentration is therefore important for the development of nutrient-efficient crop varieties that can cope with a shortage of mineral resources. In the present study, we investigated the profiles of B, Ca, Fe, Cu, Mg, P and Zn concentrations in shoots and analyzed the genetic variation in a rapeseed (Brassica napus) double haploid population at normal and deficient boron (B) levels in hydroponic conditions. Significant correlations between the concentrations of different minerals, such as Ca and Mg, Ca and P, and Cu and Fe, existed in both B environments. A total of 35 quantitative trait loci (QTL) and 74 epistatic interaction pairs for mineral concentrations were identified by whole genome analysis of QTL and epistatic interactions. The individual phenotypic contributions of the QTL ranged from 4.4% to 19.0%, and the total percentage of genetic variance that was due to QTL and epistatic interactions varied from 10.4% to 82.4%. Most of these QTL corresponded specifically to one of the two B conditions except for one stable main-effect P-QTL across the B environments. Three QTL for Ca and Mg were found to co-localize under normal B condition. These results revealed that genetic factors control mineral homeostasis in plants and multigenes involving ion transport are required to regulate mineral balance in plants under conditions of diverse nutrient stress. In addition, 26 genes involved in ion uptake and transport in Arabidopsis thaliana were in silico mapped onto the QTL intervals of B. napus by comparative genomic analysis. These candidate orthologous genes in B. napus allowed the selection of genes involved in the controlling mineral concentration that may account for the identified QTL.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251 doi:10.1105/tpc.104.030452

    Article  PubMed  CAS  Google Scholar 

  • Bentsink L, Yuan K, Koornneef M, Vreugdenhil D (2003) The genetics of phytate and phosphate accumulation in seeds and leaves of Arabidopsis thaliana, using natural variation. Theor Appl Genet 106:1234–1243

    PubMed  CAS  Google Scholar 

  • Broadley MR, Hammond JP, King GJ, Astley D, Bowen HC, Meacham MC, Mead A, Pink DAC, Teakle GR, Hayden RM, Spracklen WP, White PJ (2008) Shoot calcium (Ca) and magnesium (Mg) concentrations differ between subtaxa, are highly heritable, and associate with potentially pleiotropic loci in Brassica oleracea. Plant Physiol 146:1707–1720 doi:10.1104/pp.107.114645

    Article  PubMed  CAS  Google Scholar 

  • Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Romheld V (2002) Boron in plant biology. Plant Biol 4:205–223 doi:10.1055/s-2002-25740

    Article  CAS  Google Scholar 

  • Camacho-Cristobal JJ, Gonzalez-Fontes A (2007) Boron deficiency decreases plasmalemma H+-ATPase expression and nitrate uptake, and promotes ammonium assimilation into asparagine in tobacco roots. Planta 226:443–451 doi:10.1007/s00425-007-0494-2

    Article  PubMed  CAS  Google Scholar 

  • Churchill GA, Doerge RW (1994) Emprical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212:475–486 doi:10.1007/s004250000458

    Article  PubMed  CAS  Google Scholar 

  • Coic Y, Lesaint C, Le Roux F (1962) Effects of ammonium and nitrate nutrition and a change of ammonium and nitrate supply on the metabolism of anions and cations in tomatoes. Ann Physiol Veg 4:117–125

    CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2006) Put the metal to the petal: Metal uptake and transport throughout plants. Curr Opin Plant Biol 9:322–330 doi:10.1016/j.pbi.2006.03.015

    Article  PubMed  CAS  Google Scholar 

  • Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213

    PubMed  CAS  Google Scholar 

  • DiDonato RJ, Roberts LA, Sanderson T, Eisley RB, Walker EL (2004) Arabidopsis Yellow Stripe-Like2 (YSL2): A metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes. Plant J 39:403–414 doi:10.1111/j.1365-313X.2004.02128.x

    Article  PubMed  CAS  Google Scholar 

  • Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294

    PubMed  CAS  Google Scholar 

  • Goldbach HE, Wimmer MA (2007) Boron in plants and animals: Is there a role beyond cell-wall structure? J Plant Nutr Soil SC 170:39–48 doi:10.1002/jpln.200625161

    Article  CAS  Google Scholar 

  • Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe and Zn homeostasis in plants. BBA-Mol Cell Res 1763:595–608

    CAS  Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: Integrating root responses to phosphorus starvation. J Exp Bot 59:93–109 doi:10.1093/jxb/erm221

    Article  PubMed  CAS  Google Scholar 

  • Harada H, Leigh RA (2006) Genetic mapping of natural variation in potassium concentrations in shoots of Arabidopsis thaliana. J Exp Bot 57:953–960 doi:10.1093/jxb/erj081

    Article  PubMed  CAS  Google Scholar 

  • Hirschi KD (2003) Strike while the ionome is hot: Making the most of plant genomic advances. Trends Biotechnol 21:520–521 doi:10.1016/j.tibtech.2003.09.013

    Article  PubMed  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agriculture Experimental Station circular 347.

  • Kirkby EA (1968) Influence of ammonium and nitrate nutrition on the cation-anion balance and nitrogen and carbohydrate metabolism of white mustard plants grown in dilute nutrient solutions. Soil Sci 105:133–141 doi:10.1097/00010694-196803000-00001

    Article  CAS  Google Scholar 

  • Lahner B, Gong JM, Mahmoudian M, Smith EL, Abid KB, Rogers EE, Guerinot ML, Harper JF, Ward JM, McIntyre L, Schroeder JI, Salt DE (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotechnol 21:1215–1221 doi:10.1038/nbt865

    Article  PubMed  CAS  Google Scholar 

  • Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Park BS, Choi SR, Lim YP, Meng J (2007) Flowering time quantitative trait loci analysis of oilseed Brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177:2433–2444

    PubMed  CAS  Google Scholar 

  • Lopez-Lefebre LR, Rivero RM, Garcia PC, Sanchez E, Ruiz JM, Romero L (2002) Boron effect on mineral nutrients of tobacco. J Plant Nutr 25:509–522 doi:10.1081/PLN-120003379

    Article  CAS  Google Scholar 

  • Loudet O, Chaillou S, Merigout P, Talbotec J, Daniel-Vedele F (2003) Quantitative trait loci analysis of nitrogen use efficiency in Arabidopsis. Plant Physiol 131:345–358 doi:10.1104/pp.102.010785

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London, UK

    Google Scholar 

  • Mauricio R (2001) Mapping quantitative trait loci in plants: Uses and caveats for evolutionary biology. Nat Rev Genet 2:370–381 doi:10.1038/35072085

    Article  PubMed  CAS  Google Scholar 

  • Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427 doi:10.1093/jxb/erm190

    Article  PubMed  CAS  Google Scholar 

  • Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781 doi:10.1534/genetics.105.042093

    Article  PubMed  CAS  Google Scholar 

  • Payne KA, Bowen HC, Hammond JP, Hampton CR, Lynn JR, Mead A, Swarup K, Bennett MJ, White PJ, Broadley MR (2004) Natural genetic variation in caesium (Cs) accumulation by Arabidopsis thaliana. New Phytol 162:535–548 doi:10.1111/j.1469-8137.2004.01026.x

    Article  CAS  Google Scholar 

  • Peleman JD, Wye C, Zethof J, Sorensen AP, Verbakel H, van Oeveren J, Gerats T, van der Voort JR (2005) Quantitative trait locus (QTL) isogenic recombinant analysis: A method for high-resolution mapping of QTL within a single population. Genetics 171:1341–1352 doi:10.1534/genetics.105.045963

    Article  PubMed  CAS  Google Scholar 

  • Price CA, Carell EF (1964) Control by iron of chlorophyll formation and growth in Euglena gracilis. Plant Physiol 39:862–868 doi:10.1104/pp.39.5.862

    Article  PubMed  CAS  Google Scholar 

  • Qiu D, Morgan C, Shi J, Long Y, Liu J, Li R, Zhuang X, Wang Y, Tan X, Dietrich E, Weihmann T, Everett C, Vanstraelen S, Beckett P, Fraser F, Trick M, Barnes S, Wilmer J, Schmidt R, Li J, Li D, Meng J, Bancroft I (2006) A comparative linkage map of oilseed rape and its use for QTL analysis of seed oil and erucic acid content. Theor Appl Genet 114:67–80 doi:10.1007/s00122-006-0411-2

    Article  PubMed  CAS  Google Scholar 

  • Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annu Rev Plant Biol 59:709–733 doi:10.1146/annurev.arplant.59.032607.092942

    Article  PubMed  CAS  Google Scholar 

  • Sancenon V, Puig S, Mira H, Thiele DJ, Penarrubia L (2003) Identification of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51:577–587 doi:10.1023/A:1022345507112

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69 doi:10.1146/annurev.arplant.58.032806.103750

    Article  PubMed  CAS  Google Scholar 

  • Shaul O (2002) Magnesium transport and function in plants: The tip of the iceberg. Biometals 15:309–323 doi:10.1023/A:1016091118585

    Article  PubMed  CAS  Google Scholar 

  • Shelp BJ (1988) Boron mobility and nutrition in Broccoli (Brassica oleracea var. italica). Ann Bot (Lond) 61:83–91

    CAS  Google Scholar 

  • Shi L, Nian FZ, Zhao H, Xu FS, Meng JL, Wang YH (2004) Responses to boron deficiency in 7 varieties of rape (Brassica napus L.). Chin J Oil Crop Sci 26:47–50

    Google Scholar 

  • Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825 doi:10.1007/s00239-006-0048-4

    Article  PubMed  CAS  Google Scholar 

  • Vreugdenhil D, Aarts MGM, Koornneef M, Nelissen H, Ernst WHO (2004) Natural variation and QTL analysis for cationic mineral content in seeds of Arabidopsis thaliana. Plant Cell Environ 27:828–839 doi:10.1111/j.1365-3040.2004.01189.x

    Article  CAS  Google Scholar 

  • Wang DL, Zhu J, Li ZK, Paterson AH (1999) Mapping QTLs with epistatic effects and QTL×environment interactions by mixed linear model approaches. Theor Appl Genet 99:1255–1264 doi:10.1007/s001220051331

    Article  Google Scholar 

  • Wang SC, Bastern J, Zeng ZB (2006) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)

  • Waters BM, Grusak MA (2008) Quantitative trait locus mapping for seed mineral concentrations in two Arabidopsis thaliana recombinant inbred populations. New Phytol 179:1033–1047 doi:10.1111/j.1469-8137.2008.02544.x

    Article  PubMed  CAS  Google Scholar 

  • White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899 doi:10.1093/jexbot/52.358.891

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Yuan YX, Zhang XW, Zhao JJ, Song XF, Li Y, Li XN, Sun RF, Koornneef M, Aarts MGM, Wang XW (2008) Mapping QTLs for mineral accumulation and shoot dry biomass under different Zn nutritional conditions in Chinese cabbage (Brassica rapa L. ssp pekinensis). Plant Soil 310:25–40 doi:10.1007/s11104-008-9625-1

    CAS  Google Scholar 

  • Xu FS, Wang YH, Meng J (2001) Mapping boron efficiency gene(s) in Brassica napus using RFLP and AFLP markers. Plant Breed 120:319–324 doi:10.1046/j.1439-0523.2001.00583.x

    Article  CAS  Google Scholar 

  • Yamauchi T, Hara T, Sonoda Y (1986) Effects of boron deficiency and calcium supply on the calcium metabolism in tomato plant. Plant Soil 93:223–230 doi:10.1007/BF02374224

    Article  CAS  Google Scholar 

  • Zeng CY, Xu FS, Wang YH, Hu CX, Meng JL (2007) Physiological basis of QTLs for boron efficiency in Arabidopsis thaliana. Plant Soil 296:187–196 doi:10.1007/s11104-007-9309-2

    Article  CAS  Google Scholar 

  • Zeng ZB (1994) Precision mapping of quatitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank sincerely Dr. Jinming Zhu at Pennsylvania State University for his kind help in data analysis of phenotype. This work was supported by the Ministry of Science and Technology (2005CB120905 / 2007AA10Z117) and the National Natural Science Foundation (30771283) of China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fangsen Xu.

Additional information

Responsible Editor: Jian Feng Ma.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM Table 1

Epistatic interactions (P ≤ 0.005) that affect mineral concnetrations in the shoots of the TN DH population (DOC 176 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, J., Yang, J., Li, R. et al. Analysis of genetic factors that control shoot mineral concentrations in rapeseed (Brassica napus) in different boron environments. Plant Soil 320, 255–266 (2009). https://doi.org/10.1007/s11104-009-9891-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-009-9891-6

Keywords

Navigation