Skip to main content
SpringerLink
Log in

Physiological basis of QTLs for boron efficiency in Arabidopsis thaliana

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

Abstract

Boron (B) is an essential micronutrient for higher plants, but the adaptability of plants to B deficiency varies widely both between and within species. On the basis of quantitative trait loci (QTL) analysis of the B efficiency coefficient (BEC) detected in an Arabidopsis thaliana Ler × Col recombinant inbred (RI) population, B efficiency was evaluated in the original parents (Ler and Col-4) and two F8 lines (1938 and 1961), both of which were selected on the basis of phenotype and genotype of the RI population. The parent Ler and F8 progeny 1938 had higher BEC and B utilization efficiency (BUE) values than those calculated for parent Col-4 and F8 progeny 1961, respectively, when grown in nutrient solutions containing three different concentrations of B. The magnitude of the BEC and BUE-values was correlated closely with the combined phenotypic effect of the corresponding QTLs among the four genotypes. The F8 line, 1938, inherited all four B-efficient QTLs, AtBE1-1, AtBE1-2, AtBE2 and AtBE5, from its two original parents. The four QTLs accounted for 65.2% of the total variation in BEC and 1938 showed the highest BEC (0.74) and BUE (10.5) values among the four genotypes when grown in nutrient solution that contained 0.324 μM B. Only one minor-effect QTL (AtBE1-1) was found in the parent, Col-4. This QTL accounted only for 8.8% of total BEC variation and resulted in the lowest BEC (0.39) and BUE (0.76) in Col-4 when it was grown in nutrient solution that contained 0.324 μM B. Phenotypic profile analysis showed that 1938 not only inherited the B utilization and distribution characteristics found in the silique of Ler, but also acquired the low-B requirement for root and shoot growth from Col-4. As a result, this genotype displayed the strongest tolerance to B deficiency. In addition, both B-efficient genotypes, 1938 and Ler, possessed the QTL (AtBE1-2) and both plants had high-seed yields and high-B distributions in their siliques. Therefore, we hypothesize that QTL AtBE1-2 plays a role in the utilization and/or the distribution of B to the silique when plants suffer from B deficiency. A close correlation between the B-efficient phenotype and the corresponding QTLs indicated that phenotypic differences depend on the genetic variation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

BEC:

Boron efficiency coefficient

BUE:

Boron utilization efficiency

RIL:

Recombinant inbred line

R/S:

Ratio of root/shoot (dry matter basis)

References

  • Alonso-Blanco C, Koornneef M (2000) Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. Trends Plant Sci 5:22-29

    Article  PubMed  CAS  Google Scholar 

  • Asad A, Bell RW, Dell B (2002) A critical comparison of the external and internal boron requirement for contrasting species in boron-buffered solution culture. Plant Soil 233:31–45

    Article  Google Scholar 

  • Blamey FPC, Vermuelen WJ, Chapman J (1984) Inheritance of boron status in sunflower. Crop Sci 24:43–46

    Article  CAS  Google Scholar 

  • Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500

    Article  PubMed  CAS  Google Scholar 

  • Borevitz JO, Chory J (2004) Genomics tools for QTL analysis and gene discovery. Curr Opin Plant Biol 7:132–136

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dell B, Huang L (1997) Physiological response of plants to low boron. Plant Soil 193:103–120

    Article  CAS  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil, vol 347. California Agricultural Experiment Station Circular, University of California, Berkeley, pp 1–32

  • Hu H, Brown PH, Labavitch JM (1996) Species variability in boron requirement is correlated with cell wall pectin. J Exp Bot 47:227–232

    Article  CAS  Google Scholar 

  • Huang L, Pant J, Dell B, Bell RW (2000) Effects of boron deficiency on anther development and floret fertility in wheat (Triticum aestivum L. “Wilgoyne”) Ann Bot 85:493–500

    Article  CAS  Google Scholar 

  • Iwai H, Hokura A, Oishi M, Chida H, Ishii T, Sakai Sh, Satoh S (2006) The gene responsible for borate cross-linking of pectin Rhamnogalacturonan-II is required for plant reproductive tissue development and fertilization. Proc Natl Acad Sci USA 103:16592–16597

    Article  PubMed  CAS  Google Scholar 

  • Jannink J, Bink MCAM, Jansen RC (2001) Using complex plant pedigrees to map valuable genes. Trends Plant Sci 6:337–342

    Article  PubMed  CAS  Google Scholar 

  • John MK (1975) Acid extraction of plant boron. J Sci Food Agric 26:1911–1915

    Article  CAS  Google Scholar 

  • Juenger T, Pérez-Pérez JM, Bernal S, Micol JL (2005) Quantitative trait loci mapping of floral and leaf morphology traits in Arabidopsis thaliana: evidence for modular genetic architecture. Evol Dev 7:259–271

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi M, Mutoh T, Matoh T (2004) Boron nutrition of cultured tobacco BY-2 cells. IV. genes induced under low boron supply. J Exp Bot 55:1441–1443

    Article  PubMed  CAS  Google Scholar 

  • Koelewijn HP (2004) Rapid change in relative growth rate between the vegetative and reproductive stage of the life cycle in Plantago coronopus. New Phytol 163:67–76

    Article  Google Scholar 

  • Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172

    Article  PubMed  CAS  Google Scholar 

  • Ling HQ, Bauer P, Bereczky Z, Keller B, Ganal M (2002) The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc Natl Acad Sci USA 99:13938–13943

    Article  PubMed  CAS  Google Scholar 

  • Lister C, Dean C (1993) Recombinant inbred lines for mapping RFLP and phenotypic markers in Arabidopsis thaliana. Plant J 4:745–750

    Article  CAS  Google Scholar 

  • Mailer AP, Lope FD, Saino N (1995) Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations. J Evol Biol 8:671–687

    Article  Google Scholar 

  • Maloof JN (2003) Genomic approaches to analyzing natural variation in Arabidopsis thaliana. Curr Opin Genet Dev 13:576–582

    Article  PubMed  CAS  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, London, pp 379–392

    Google Scholar 

  • Matoh T, Kawagochi S, Kobayashi M (1996) Ubiquity of a borate rhamnogalacturonan II complex in the cell walls of higher plants. Plant Cell Physiol 37:636–640

    CAS  Google Scholar 

  • Meyer RC, Törjék O, Becher M, Altmann T (2004) Heterosis of biomass production in Arabidopsis. establishment during early development. Plant Physiol 134:1813–1823

    Article  PubMed  CAS  Google Scholar 

  • Nachiangmai D, Dell B, Bell RW, Huang L, Rerkasem B (2004) Enhanced boron transport into the ear of wheat as a mechanism for boron efficiency. Plant Soil 264:141–147

    Article  CAS  Google Scholar 

  • O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139

    Article  PubMed  CAS  Google Scholar 

  • Rasmuson M (2002) The genotype-phenotype link. Hereditas 136:1–6

    Article  PubMed  Google Scholar 

  • Rerkasem B, Jamjod S (1997) Genotypic variation in plant response to low boron and implications for plant breeding. Plant Soil 193:169–180

    Article  CAS  Google Scholar 

  • Richard-Molard C, Wuillème S, Scheel C, Gresshoff PM, Morot-Gaudry JF, Limami AM (1999) Nitrogen-induced changes in morphological development and bacterial susceptibility of Belgian endive (Cichorium intybus L.) are genotype-dependent. Planta 209:389–398

    Article  PubMed  CAS  Google Scholar 

  • Sachs T (1999) Node counting: an internal control of balanced vegetative and reproductive development. Plant Cell Environ 22:757–766

    Article  Google Scholar 

  • Srivastava SP, Bhandari TMS, Yadav CR, Joshi M, Erskine W (2000) Boron deficiency in lentil: yield loss and geographic distribution in a germplasm collection. Plant Soil 219:147–151

    Article  CAS  Google Scholar 

  • 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 Soil 225:243–251

    Article  CAS  Google Scholar 

  • Subedi KD, Gregory PJ, Gooding MJ (1999) Boron content and partitioning in wheat cultivars with contrasting tolerance to boron deficiency. Plant Soil 214:141–152

    Article  CAS  Google Scholar 

  • Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102:12276–12281

    Article  PubMed  CAS  Google 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

    Article  PubMed  CAS  Google Scholar 

  • 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. Plant Cell 18:1498–1509

    Article  PubMed  Google Scholar 

  • Thomson MJ, Edwards JD, Septiningsih EM, Harrington SE, McCouch SR (2006) Substitution mapping of dth1.1, a flowering-time quantitative trait locus (QTL) associated with transgressive variation in rice, reveals multiple sub-QTL. Genetics 172:2501–2514

    Article  PubMed  CAS  Google Scholar 

  • Tomas MA, Carrera AD, Poverene M (2000) Is there any genetic differentiation among populations of Piptochaetium napostaense (Speg.) Hack (Poaceae) with different grazing histories? Plant Ecol 147:227–235

    Article  Google Scholar 

  • Tonsor SJ, Alonso-Blanco C, Koornneef M (2005) Gene function beyond the single trait: natural variation, gene effects, and evolutionary ecology in Arabidopsis thaliana. Plant Cell Environ 28:2–20

    Article  CAS  Google Scholar 

  • Wang L, Zhao J, Xu F, Liu R, Meng J (2002) Integration of DNA clones related to important economic traits of Brassica napus onto Arabidopsis genetic map. Acta Genet Sin 29:741–746

    PubMed  CAS  Google Scholar 

  • Wang S, Basten CJ, Zeng Z (2004) Windows QTL Cartographer, Version 2.0. Department of Statistics, North Carolina State University, Raleigh, NC

    Google Scholar 

  • Wayne ML, McIntyre LM (2002) Combining mapping and arraying: an approach to candidate gene identification. Proc Natl Acad Sci USA 99:14903–14906

    Article  PubMed  CAS  Google Scholar 

  • Wimmer MA, Goldbach HE (1999) A miniaturized curcumin method for the determination of boron in solutions and biological samples. J Plant Nutr Soil Sci 162:15–18

    Article  CAS  Google Scholar 

  • Xu F, Wang Y, Meng J (2001) Mapping boron efficiency gene(s) in Brassica napus using RFLP and AFLP markers. Plant Breed 120:319–325

    Article  CAS  Google Scholar 

  • Xue J, Lin M, Bell RW, Graham RD, Yang X, Yang Yu (1998) Differential response of oilseed rape (Brassica napus L.) cultivars to low boron supply. Plant Soil 204:155–163

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors sincerely thank Dr. Yanlai Han for her work in the Arabidopsis RIL population culture and phenotype investigation of B efficiency. The authors are also grateful to Prof. Dr. Heiner Goldbach, Dr. Longbin Huang, Dr. Paul Edward Bilsborrow and Dr. Lei Shi for their valuable comments and the correction of manuscript. This study was supported by the National Natural Science Foundation of China (No. 30471041) and the Program for New Century Excellent Talents in University (No. NCET-05-0666).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Changying Zeng, Fangsen Xu & Jinling Meng

  2. Microelement Research Centre, Huazhong Agricultural University, Wuhan, 430070, China

    Changying Zeng, Fangsen Xu, Yunhua Wang & Chengxiao Hu

Authors
  1. Changying Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fangsen Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunhua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chengxiao Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinling Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fangsen Xu.

Additional information

Responsible Editor: Richard W. Bell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeng, C., Xu, F., Wang, Y. et al. Physiological basis of QTLs for boron efficiency in Arabidopsis thaliana . Plant Soil 296, 187–196 (2007). https://doi.org/10.1007/s11104-007-9309-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-007-9309-2

Keywords

Search

Navigation