Home LiteratureArticle Details
PMID: 24114060 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Roles of BOR2, a boron exporter, in cross linking of rhamnogalacturonan II and root elongation under boron limitation in Arabidopsis.

Plant physiology ·Vol. 163 ·No. 4 ·2013-12-00 ·Pages 1699-709

Miwa K, Wakuta S, Takada S, Ide K, Takano J, Naito S, Omori H, Matsunaga T, Fujiwara T

Abstract

Boron (B) is required for cross linking of the pectic polysaccharide rhamnogalacturonan II (RG-II) and is consequently essential for the maintenance of cell wall structure. Arabidopsis (Arabidopsis thaliana) BOR1 is an efflux B transporter for xylem loading of B. Here, we describe the roles of BOR2, the most similar paralog of BOR1. BOR2 encodes an efflux B transporter localized in plasma membrane and is strongly expressed in lateral root caps and epidermis of elongation zones of roots. Transfer DNA insertion of BOR2 reduced root elongation by 68%, whereas the mutation in BOR1 reduced it by 32% under low B availability (0.1 µm), but the reduction in shoot growth was not as obvious as that in the BOR1 mutant. A double mutant of BOR1 and BOR2 exhibited much more severe growth defects in both roots and shoots under B-limited conditions than the corresponding single mutants. All single and double mutants grew normally under B-sufficient conditions. These results suggest that both BOR1 and BOR2 are required under B limitation and that their roles are, at least in part, different. The total B concentrations in roots of BOR2 mutants were not significantly different from those in wild-type plants, but the proportion of cross-linked RG-II was reduced under low B availability. Such a reduction in RG-II cross linking was not evident in roots of the BOR1 mutant. Thus, we propose that under B-limited conditions, transport of boric acid/borate by BOR2 from symplast to apoplast is required for effective cross linking of RG-II in cell wall and root cell elongation.

MeSH Terms
Anion Transport Proteins/metabolism Arabidopsis/drug effects,genetics,growth & development,metabolism Arabidopsis Proteins/metabolism Biological Transport/drug effects Boron/pharmacology Cell Size/drug effects DNA, Bacterial/genetics Dimerization Models, Biological Molecular Sequence Data Mutagenesis, Insertional/genetics Mutation/genetics Organ Specificity/drug effects Pectins/metabolism Plant Epidermis/cytology,drug effects Plant Roots/drug effects,growth & development,metabolism Plants, Genetically Modified Saccharomyces cerevisiae/drug effects,metabolism Subcellular Fractions/drug effects,metabolism
Chemicals
Anion Transport Proteins Arabidopsis Proteins BOR2 protein, Arabidopsis DNA, Bacterial T-DNA rhamnogalacturonan II Pectins Boron
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Miwa Kyoko
Creative Research Institution, Hokkaido University, Sapporo 001-0021, Japan.
Wakuta Shinji
Takada Shigeki
Ide Koji
Takano Junpei
Naito Satoshi
Omori Hiroyuki
Matsunaga Toshiro
Fujiwara Toru
References (32)
32 references, click to expand
  1. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation.
    Plant Cell. 2006 Jun;18(6):1498-509 PMID: 16679457
  2. Cell-type specificity of the expression of Os BOR1, a rice efflux boron transporter gene, is regulated in response to boron availability for efficient boron uptake and xylem loading.
    Plant Cell. 2007 Aug;19(8):2624-35 PMID: 17675406
  3. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  4. Plants tolerant of high boron levels.
    Science. 2007 Nov 30;318(5855):1417 PMID: 18048682
  5. Saccharomyces cerevisiae Bor1p is a boron exporter and a key determinant of boron tolerance.
    FEMS Microbiol Lett. 2007 Feb;267(2):230-5 PMID: 17166224
  6. Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia.
    Plant Physiol. 1992 May;99(1):263-8 PMID: 16668860
  7. Characterization of Arabidopsis CTP:3-deoxy-D-manno-2-octulosonate cytidylyltransferase (CMP-KDO synthetase), the enzyme that activates KDO during rhamnogalacturonan II biosynthesis.
    Plant Cell Physiol. 2011 Oct;52(10):1832-43 PMID: 21893514
  8. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability.
    Proc Natl Acad Sci U S A. 2005 Aug 23;102(34):12276-81 PMID: 16103374
  9. Rhamnogalacturonan II structure shows variation in the side chains monosaccharide composition and methylation status within and across different plant species.
    Plant J. 2013 Oct;76(1):61-72 PMID: 23802881
  10. The plant cell wall polysaccharide rhamnogalacturonan II self-assembles into a covalently cross-linked dimer.
    J Biol Chem. 1999 May 7;274(19):13098-104 PMID: 10224062
  11. Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants.
    Biosci Biotechnol Biochem. 2007 Aug;71(8):2095-100 PMID: 17690442
  12. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  13. Arabidopsis boron transporter for xylem loading.
    Nature. 2002 Nov 21;420(6913):337-40 PMID: 12447444
  14. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set.
    Plant J. 2009 Jul;59(1):169-78 PMID: 19309456
  15. An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics.
    Plant Mol Biol. 2003 Sep;53(1-2):247-59 PMID: 14756321
  16. The endosomal system of plants: charting new and familiar territories.
    Plant Physiol. 2008 Aug;147(4):1482-92 PMID: 18678740
  17. 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 Sep 13;271(37):22923-30 PMID: 8798473
  18. Chemistry and biology of boron.
    Biofactors. 1992 Apr;3(4):229-39 PMID: 1605832
  19. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways.
    Proc Natl Acad Sci U S A. 2010 Mar 16;107(11):5220-5 PMID: 20194745
  20. High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana.
    J Biol Chem. 2011 Feb 25;286(8):6175-83 PMID: 21148314
  21. Two Chains of Rhamnogalacturonan II Are Cross-Linked by Borate-Diol Ester Bonds in Higher Plant Cell Walls.
    Plant Physiol. 1996 Mar;110(3):1017-1020 PMID: 12226238
  22. Getting started with yeast.
    Methods Enzymol. 1991;194:3-21 PMID: 2005794
  23. A gateway cloning vector set for high-throughput functional analysis of genes in planta.
    Plant Physiol. 2003 Oct;133(2):462-9 PMID: 14555774
  24. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots.
    Plant J. 2002 Feb;29(4):475-86 PMID: 11846880
  25. Borate cross-linked/total rhamnogalacturonan II ratio in cell walls for the biochemical diagnosis of boron deficiency in hydroponically grown pumpkin.
    Anal Sci. 2006 Aug;22(8):1125-7 PMID: 16896255
  26. bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron.
    Plant Physiol. 1997 Nov;115(3):901-6 PMID: 9390427
  27. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide.
    Annu Rev Plant Biol. 2004;55:109-39 PMID: 15377216
  28. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis.
    Science. 1999 Aug 6;285(5429):901-6 PMID: 10436161
  29. Boron transport in plants: co-ordinated regulation of transporters.
    Ann Bot. 2010 Jun;105(7):1103-8 PMID: 20228086
  30. NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis.
    Plant Cell. 2008 Oct;20(10):2860-75 PMID: 18952773
  31. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth.
    Science. 2001 Oct 26;294(5543):846-9 PMID: 11679668
  32. Permeability of boric acid across lipid bilayers and factors affecting it.
    J Membr Biol. 2000 May 15;175(2):95-105 PMID: 10811971
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2013-12-00
Epub
2013-00-10
Pages
1699-709
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3850200
Subset
IM
Databases
GENBANK
GU971377, GU971378
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]