Advertisement

Molecular Mechanisms of Boron Transport in Plants: Involvement of Arabidopsis NIP5;1 and NIP6;1

  • Kyoko Miwa
  • Mayuki Tanaka
  • Takehiro Kamiya
  • Toru Fujiwara
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 679)

Abstract

Understanding of the molecular mechanisms of boron (B) transport has been greatly advanced in the last decade. BOR1, the first B transporter in living systems, was identified by forward genetics using Arabidopsis mutants. Genes similar to BOR1 have been reported to share different physiological roles in plants. NIP5;1, a member of aquaporins in Arabidopsis, was then identified as a boric acid channel gene responsible for the B uptake into roots. NIP6;1, the most similar gene to NIP5;1, encodes a B channel essential for B distribution to young leaves. In the present chapter, recent advancement of the understanding of molecular mechanisms of B transport and roles of NIP genes are discussed.

Keywords

Transgenic Line Boric Acid Wild Type Plant Pectic Polysaccharide Major Intrinsic Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Warington K. The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot 1923; 37:629–672.Google Scholar
  2. 2.
    Shorrocks VM. The occurrence and correction of boron deficiency. Plant Soil 1997; 193:121–148.CrossRefGoogle Scholar
  3. 3.
    Liu Z, Zhu Q, Tang L et al. Geographical distribution of trace elements-deficient soils in China. Acta Pedol Sin 1982; 19:209–223.Google Scholar
  4. 4.
    Loomis WD, Durst RW. Chemistry and biology of boron. Biofactors 1992; 3:229–239.PubMedGoogle Scholar
  5. 5.
    Marschner H. Mineral Nutritin of Higher Plants, 2nd ed. San Diego: Academic Press, 1995;.Google Scholar
  6. 6.
    Dell B, Huang LB. Physiological response of plants to low boron. Plant Soil 1997; 193:103–120.CrossRefGoogle Scholar
  7. 7.
    Kouchi H, Kumazawa K. Anatomical responses of root tips to boron deficiency. III. Effect of boron deficiency on sub-cellular structure of root tips, particularly on morphology of cell wall and its related organelles. Soil Sci Plant Nutr 1976; 22:53–71.Google Scholar
  8. 8.
    Bolanos L, Lukaszewski K, Bonilla I et al. Why boron? Plant Physiol Biochem 2004; 42:907–912.CrossRefPubMedGoogle Scholar
  9. 9.
    Nable RO, Bañuelos GS, Paull JG. Boron toxicity. Plant Soil 1997; 193:181–198.CrossRefGoogle Scholar
  10. 10.
    Power PP, Woods WG. The chemistry of boron and its speciation in plants. Plant Soil 1997; 193:1–13.CrossRefGoogle Scholar
  11. 11.
    Matoh T, Ishigaki K, Mizutani M et al. Boron nutrition of cultured tobacco BY-2 cells. 1. Requirement for and intracellular localization of boron and selection of boron and selection of cells that tolerate low levels of boron. Plant Cell Physiol 1992; 33:1135–1141.Google Scholar
  12. 12.
    Hu H, Brown PH. 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 1994; 105:681–689.PubMedGoogle Scholar
  13. 13.
    Noguchi K, Dannel F, Heidrun P et al. Defect in root-shoot translocation of boron in Arabidopsis thaliana mutant bor1-1. J Plant Physiol 2000; 156:756–761.Google Scholar
  14. 14.
    Matoh T, Ishigaki KI, Ohno K et al. Isolation and characterization of a boron-polysaccharide complex from radish roots. Plant Cell Physiol 1993; 34:639–642.Google Scholar
  15. 15.
    Kobayashi M, Matoh T, Azuma JI. Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 1996; 110:1017–1020.PubMedGoogle Scholar
  16. 16.
    Ishii T, Matsunaga T. Isolation and characterization of a boron-rhamnogalacturonan-II complex from cell walls of sugar beet pulp. Carbohydr Res 1996; 284:1–9.CrossRefGoogle Scholar
  17. 17.
    Pellerin P, Doco T, Vidal S et al. Structural characterization of red wine rhamnogalacturonan II. Carbohydr Res 1996; 290:183–197.CrossRefPubMedGoogle Scholar
  18. 18.
    O’Neill MA, Warrenfeltz D, Kates K et al. Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester. In vitro conditions for the formation and hydrolysis of the dimer. J Biol Chem 1996; 271:22923–22930.CrossRefPubMedGoogle Scholar
  19. 19.
    O’Neill MA, Ishii T, Albersheim P et al. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 2004; 55:109–139.CrossRefPubMedGoogle Scholar
  20. 20.
    Ishii T, Matsunaga T, Pellerin P et al. The plant cell wall polysaccharide rhamnogalacturonan II self-assembles into a covalently cross-linked dimer. J Biol Chem 1999; 274:13098–13104.CrossRefPubMedGoogle Scholar
  21. 21.
    Kobayashi M, Nakagawa H, Asaka T et al. Borate-rhamnogalacturonan II bonding reinforced by Ca2+ retains pectic polysaccharides in higher-plant cell walls. Plant Physiol 1999; 119:199–204.CrossRefPubMedGoogle Scholar
  22. 22.
    Iwai H, Usui M, Hoshino H et al. Analysis of sugars in squash xylem sap. Plant Cell Physiol 2003; 44:582–587.CrossRefPubMedGoogle Scholar
  23. 23.
    Ishii T, Matsunaga T, Hayashi N. Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiol 2001; 126:1698–1705.CrossRefPubMedGoogle Scholar
  24. 24.
    O’Neill MA, Eberhard S, Albersheim P et al. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 2001; 294:846–849.CrossRefPubMedGoogle Scholar
  25. 25.
    Bonin CP, Potter I, Vanzin GF et al. The MUR1 gene of Arabidopsis thaliana encodes an isoform of GDP-D-mannose-4,6-dehydratase, catalyzing the first step in the de novo synthesis of GDP-L-fucose. Proc Natl Acad Sci USA 1997; 94:2085–2090.CrossRefPubMedGoogle Scholar
  26. 26.
    Zablackis E, York WS, Pauly M et al. Substitution of L-fucose by L-galactose in cell walls of Arabidopsis mur1. Science 1996; 272:1808–1810.CrossRefPubMedGoogle Scholar
  27. 27.
    Reuhs BL, Glenn J, Stephens SB et al. L-Galactose replaces L-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the L-fucose-deficient mur1 Arabidopsis mutant. Planta 2004; 219:147–157.CrossRefPubMedGoogle Scholar
  28. 28.
    Vanzin GF, Madson M, Carpita NC et al. The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1 Proc Natl Acad Sci USA 2002; 99:3340–3345.CrossRefPubMedGoogle Scholar
  29. 29.
    Ryden P, Sugimoto-Shirasu K, Smith AC et al. Tensile properties of Arabidopsis cell walls depend on both a xyloglucan cross-linked microfibrillar network and rhamnogalacturonan II-borate complexes. Plant Physiol 2003; 132:1033–1040.CrossRefPubMedGoogle Scholar
  30. 30.
    Baluska F, Hlavacka A, Samaj J et al. F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol 2002; 130:422–431.CrossRefPubMedGoogle Scholar
  31. 31.
    Yu Q, Hlavacka A, Matoh T et al. Short-term boron deprivation inhibits endocytosis of cell wall pectins in meristematic cells of maize and wheat root apices. Plant Physiol 2002; 130:415–421.CrossRefPubMedGoogle Scholar
  32. 32.
    Matsunaga T, Ishii T, Matsumoto S et al. Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 2004; 134:339–351.CrossRefPubMedGoogle Scholar
  33. 33.
    Bassil E, Hu H, Brown PH. Use of phenylboronic acids to investigate boron function in plants. Possible role of boron in transvacuolar cytoplasmic strands and cell-to-wall adhesion. Plant Physiol 2004; 136:3383–3395.CrossRefPubMedGoogle Scholar
  34. 34.
    Raven JA. Short-and long-distance transport of boric acid in plants. New Phytol 1980; 84:231–249.CrossRefGoogle Scholar
  35. 35.
    Dordas C, Brown PH. Permeability of boric acid across lipid bilayers and factors affecting it. J Membr Biol 2000; 175:95–105.CrossRefPubMedGoogle Scholar
  36. 36.
    Dordas C, Chrispeels MJ, Brown PH. Permeability and channel-mediated transport of boric acid across membrane vesicles isolated from squash roots. Plant Physiol 2000; 124:1349–1362.CrossRefPubMedGoogle Scholar
  37. 37.
    Stangoulis JC, Reid RJ, Brown PH et al. Kinetic analysis of boron transport in Chara. Planta 2001; 213:142–146.CrossRefPubMedGoogle Scholar
  38. 38.
    Dannel F, Pfeffer H, Römheld V. Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotope 10B and 11B. Aust J Plant Physiol 2000; 156:756–761.Google Scholar
  39. 39.
    Dordas C, Brown PH. Expression of the major intrinsic protein (MIP) PIP1 in Xenopus laevis oocytes. Evidence for channel mediated transport of boric acid in squash (Cucurbita pepo). Plant Soil 2001; 235:95–103.CrossRefGoogle Scholar
  40. 40.
    Dannel F, Pfeffer H, Walch-Liu P et al. Plant nutrition-Food security and sustainability of afro-ecosystems, Kluwer Academic Publishers, Dordrecht, 2001;162–163.Google Scholar
  41. 41.
    Hayes JE, Reid RJ. Boron tolerance in barley is mediated by efflux of boron from the roots. Plant Physiol 2004; 136:3376–3382.CrossRefPubMedGoogle Scholar
  42. 42.
    Sutton T, Baumann U, Hayes J et al. Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 2007; 318:1446–1449.CrossRefPubMedGoogle Scholar
  43. 43.
    Noguchi K, Yasumori M, Imai T et al. Bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron. Plant Physiol 1997; 115:901–906.CrossRefPubMedGoogle Scholar
  44. 44.
    Takano J, Yamagami M, Noguchi K et al. Preferential translocation of boron to young leaves in Arabidopsis thaliana regulated by the BOR1 gene. Soil Sci Plant Nutr 2001; 47:345–357.Google Scholar
  45. 45.
    Noguchi K, Ishii T, Matsunaga T et al. Biochemical properties of the cell wall in the Arabidopsis mutant bor1-1 in relation to boron nutrition. J Plant Nutr Soil Sci 2003; 166:175–178.CrossRefGoogle Scholar
  46. 46.
    Takano J, Noguchi K, Yasumori M et al. Arabidopsis boron transporter for xylem loading. Nature 2002; 420:337–340.CrossRefPubMedGoogle Scholar
  47. 47.
    Nozawa A, Takano J, Kobayashi M et al. Roles of BOR1, DUR3 and FPS1 in boron transport and tolerance in Saccharomyces cerevisiae. FEMS Microbiol Lett 2006; 262:216–222.CrossRefPubMedGoogle Scholar
  48. 48.
    Park M, Li Q, Shcheynikov N et al. NaBC1 is a ubiquitous electrogenic Na+-coupled borate transporter essential for cellular boron homeostasis and cell growth and proliferation. Mol Cell 2004; 16:331–341.CrossRefPubMedGoogle Scholar
  49. 49.
    Takano J, Miwa K, Yuan L et al. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 2005a; 102:12276–12281.CrossRefPubMedGoogle Scholar
  50. 50.
    Takano J, Miwa K, von Wiren N et al. Regulation of the boron transporter AtBOR1 by boron availability. In Plant nutrition for food security, human health and environmental protection, (Li CJ et al, eds). Beijing, China: Tsinghua University Press, 2005b;138–139.Google Scholar
  51. 51.
    Miwa K, Takano J, Fujiwara T. Roles of BOR1 paralog in boron transport in Arabidpsis thaliana. Plant nutrition for food security, human health and environmental protection. (Li CJ et al, eds). Beijing, China: Tsinghua University Press, 2005;124–125.Google Scholar
  52. 52.
    Takano J, Wada M, Ludewig U et al. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 2006; 18:1498–1509.CrossRefPubMedGoogle Scholar
  53. 53.
    Tyerman SD, Niemietz CM, Bramley H. Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 2002; 25:173–194.CrossRefPubMedGoogle Scholar
  54. 54.
    Danielson JAH, Johanson U. Unexpected complexity of the aquaporin gene family in the moss Physcomitrella patens. BMC Plant Biol 2008; 8:45.CrossRefPubMedGoogle Scholar
  55. 55.
    Wallace IS, Choi WG, Roberts DM. The structure, function and regulation of the nodulin 26-like intrinsic protein family of plant aquaglyceroporins. Biochim Biophys Acta 2006; 1758:1165–1175.CrossRefPubMedGoogle Scholar
  56. 56.
    Ma JF, Tamai K, Yamaji N et al. A silicon transporter in rice. Nature 2006; 440:688–691.CrossRefPubMedGoogle Scholar
  57. 57.
    Ma JF, Yamaji N, Mitani N et al. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 2008; 105:9931–9935.CrossRefPubMedGoogle Scholar
  58. 58.
    Kamiya T, Tanaka M, Mitani N et al. NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 2009; 284:2114–2120.CrossRefPubMedGoogle Scholar
  59. 59.
    Kamiya T, Fujiwara T. Arabidopsis NIP1;1 transports antimonite and determines the antimonite sensitivity. Plant Cell Physiol 2009; Plant Cell Physiol 2009; 50:1977–1981.CrossRefPubMedGoogle Scholar
  60. 60.
    Tanaka M, Wallace IS, Takano J et al. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 2008; 20:2860–2875.CrossRefPubMedGoogle Scholar
  61. 61.
    Tao R, Uratsu SL, Dandekar AM. Sorbitol synthesis in transgenic tobacco with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant Cell Physiol 1995; 36:525–532.PubMedGoogle Scholar
  62. 62.
    Brown PH, Bellaloui N, Hu H et al. Transgenically enhanced sorbitol synthesis facilitates phloem boron transport and increases tolerance of tobacco to boron deficiency. Plant Physiol 1999; 119:17–20.CrossRefPubMedGoogle Scholar
  63. 63.
    Bellaloui N, Brown PH, Dandekar AM. Manipulation of in vivo sorbitol production alters boron uptake and transport in tobacco. Plant Physiol 1999; 119:735–742.CrossRefPubMedGoogle Scholar
  64. 64.
    Bellaloui N, Yadavc RC, Chern MS et al. Transgenically enhanced sorbitol synthesis facilitates phloem-boron mobility in rice. Physiol Plant 2003; 117:79–84.CrossRefGoogle Scholar
  65. 65.
    Deguchi M, Koshita Y, Gao M et al. Engineered sorbitol accumulation induces dwarfism in Japanese persimmon. J Plant Physiol 2004; 161:1177–1184.CrossRefPubMedGoogle Scholar
  66. 66.
    Sheveleva EV, Marquez S, Chmara W et al. Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. High amounts of sorbitol lead to necrotic lesions. Plant Physiol 1998; 117:831–839.CrossRefPubMedGoogle Scholar
  67. 67.
    Miwa K, Takano J, Fujiwara T. Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana. Plant J 2006; 46:1084–1091.CrossRefPubMedGoogle Scholar
  68. 68.
    Miwa K, Takano J, Omori H et al. Plants tolerant of high boron levels. Science 2007; 318:1417.CrossRefPubMedGoogle Scholar
  69. 69.
    Kato Y, Miwa K, Takano J et al. Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant Cell Physiol 2009; 50:58–66.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2010

Authors and Affiliations

  • Kyoko Miwa
    • 1
  • Mayuki Tanaka
    • 1
  • Takehiro Kamiya
    • 1
  • Toru Fujiwara
    • 1
  1. 1.Biotechnology Research CenterThe University of TokyoJapan

Personalised recommendations