Home LiteratureArticle Details
PMID: 25035400 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

The boron efflux transporter ROTTEN EAR is required for maize inflorescence development and fertility.

The Plant cell ·Vol. 26 ·No. 7 ·2014-07-00 ·Pages 2962-77

Chatterjee M, Tabi Z, Galli M, Malcomber S, Buck A, Muszynski M, Gallavotti A

Abstract

Although boron has a relatively low natural abundance, it is an essential plant micronutrient. Boron deficiencies cause major crop losses in several areas of the world, affecting reproduction and yield in diverse plant species. Despite the importance of boron in crop productivity, surprisingly little is known about its effects on developing reproductive organs. We isolated a maize (Zea mays) mutant, called rotten ear (rte), that shows distinct defects in vegetative and reproductive development, eventually causing widespread sterility in its inflorescences, the tassel and the ear. Positional cloning revealed that rte encodes a membrane-localized boron efflux transporter, co-orthologous to the Arabidopsis thaliana BOR1 protein. Depending on the availability of boron in the soil, rte plants show a wide range of phenotypic defects that can be fully rescued by supplementing the soil with exogenous boric acid, indicating that rte is crucial for boron transport into aerial tissues. rte is expressed in cells surrounding the xylem in both vegetative and reproductive tissues and is required for meristem activity and organ development. We show that low boron supply to the inflorescences results in widespread defects in cell and cell wall integrity, highlighting the structural importance of boron in the formation of fully fertile reproductive organs.

MeSH Terms
Antiporters/genetics Arabidopsis/drug effects,genetics,metabolism Arabidopsis Proteins/genetics Biological Transport Boron/metabolism Cell Wall/drug effects Chromosome Mapping Cloning, Molecular Fertility Gene Expression Regulation, Plant Inflorescence/drug effects,genetics,growth & development,ultrastructure Membrane Transport Proteins/genetics,metabolism Meristem/drug effects,genetics,growth & development,ultrastructure Mutation Phenotype Phylogeny Plant Proteins/genetics,metabolism Plant Roots/drug effects,genetics,growth & development,ultrastructure Plants, Genetically Modified Reproduction Xylem/drug effects,genetics,growth & development,ultrastructure Zea mays/drug effects,genetics,growth & development,ultrastructure
Chemicals
Antiporters Arabidopsis Proteins BOR1 protein, Arabidopsis Membrane Transport Proteins Plant Proteins Boron
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Chatterjee Mithu
Waksman Institute, Rutgers University, Piscataway, New Jersey 08854-8020.
Tabi Zara
Section of Cell and Developmental Biology, University of California San Diego, La Jolla, California 92093-0116.
Galli Mary
Waksman Institute, Rutgers University, Piscataway, New Jersey 08854-8020.
Malcomber Simon
Department of Biological Sciences, California State University Long Beach, Long Beach, California 90840 Division of Environmental Biology, National Science Foundation, Arlington, Virginia 22230.
Buck Amy
Section of Cell and Developmental Biology, University of California San Diego, La Jolla, California 92093-0116.
Muszynski Michael
Department of Genetics, Development, and Cell Biology, Iowa State University, Iowa 50011-2156.
Gallavotti Andrea
Waksman Institute, Rutgers University, Piscataway, New Jersey 08854-8020 Department of Plant Biology and Pathology, Rutgers University, New Brunswick, New Jersey 08901 agallavotti@waksman.rutgers.edu.
References (60)
60 references, click to expand
  1. Identification of boron transporter genes likely to be responsible for tolerance to boron toxicity in wheat and barley.
    Plant Cell Physiol. 2007 Dec;48(12):1673-8 PMID: 18003669
  2. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  3. High-throughput genetic mapping of mutants via quantitative single nucleotide polymorphism typing.
    Genetics. 2010 Jan;184(1):19-26 PMID: 19884313
  4. Assessing the effects of low boron diets on embryonic and fetal development in rodents using in vitro and in vivo model systems.
    Biol Trace Elem Res. 1998 Winter;66(1-3):271-98 PMID: 10050925
  5. MrBayes 3: Bayesian phylogenetic inference under mixed models.
    Bioinformatics. 2003 Aug 12;19(12):1572-4 PMID: 12912839
  6. Roles of BOR2, a boron exporter, in cross linking of rhamnogalacturonan II and root elongation under boron limitation in Arabidopsis.
    Plant Physiol. 2013 Dec;163(4):1699-709 PMID: 24114060
  7. 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
  8. Boron is required for zebrafish embryogenesis
    J Exp Biol. 1999 Jun;202 (Pt 12):1649-54 PMID: 10333510
  9. Structural identification of a bacterial quorum-sensing signal containing boron.
    Nature. 2002 Jan 31;415(6871):545-9 PMID: 11823863
  10. Arabidopsis boron transporter for xylem loading.
    Nature. 2002 Nov 21;420(6913):337-40 PMID: 12447444
  11. Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana.
    Plant J. 2006 Jun;46(6):1084-91 PMID: 16805739
  12. Boron transport mechanisms: collaboration of channels and transporters.
    Trends Plant Sci. 2008 Aug;13(8):451-7 PMID: 18603465
  13. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport.
    Plant Cell. 2010 Apr;22(4):1129-42 PMID: 20407025
  14. 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
  15. A developmental framework for endodermal differentiation and polarity.
    Proc Natl Acad Sci U S A. 2010 Mar 16;107(11):5214-9 PMID: 20142472
  16. The gene responsible for borate cross-linking of pectin Rhamnogalacturonan-II is required for plant reproductive tissue development and fertilization.
    Proc Natl Acad Sci U S A. 2006 Oct 31;103(44):16592-7 PMID: 17053077
  17. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  18. Boron deficiency and transcript level changes.
    Plant Sci. 2011 Aug;181(2):85-9 PMID: 21683871
  19. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides.
    Carbohydr Res. 2009 Sep 28;344(14):1879-900 PMID: 19616198
  20. Depletion of UDP-D-apiose/UDP-D-xylose synthases results in rhamnogalacturonan-II deficiency, cell wall thickening, and cell death in higher plants.
    J Biol Chem. 2006 May 12;281(19):13708-13716 PMID: 16549428
  21. The Sorghum bicolor genome and the diversification of grasses.
    Nature. 2009 Jan 29;457(7229):551-6 PMID: 19189423
  22. Boron deficiency disables Xenopus laevis oocyte maturation events.
    Biol Trace Elem Res. 2002 Feb;85(2):157-69 PMID: 11899023
  23. Review: mechanisms for boron deficiency-mediated changes in plant water relations.
    Plant Sci. 2013 Apr;203-204:25-32 PMID: 23415325
  24. Chemistry and biology of boron.
    Biofactors. 1992 Apr;3(4):229-39 PMID: 1605832
  25. Distribution of boron in the environment.
    Biol Trace Elem Res. 1998 Winter;66(1-3):131-43 PMID: 10050915
  26. Polar localization and endocytic degradation of a boron transporter, BOR1, is dependent on specific tyrosine residues.
    Plant Signal Behav. 2012 Jan;7(1):46-9 PMID: 22301967
  27. 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
  28. Ionomics: studying the social network of mineral nutrients.
    Curr Opin Plant Biol. 2009 Jun;12(3):381-6 PMID: 19481970
  29. ramosa2 encodes a LATERAL ORGAN BOUNDARY domain protein that determines the fate of stem cells in branch meristems of maize.
    Plant Cell. 2006 Mar;18(3):574-85 PMID: 16399802
  30. 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
  31. 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
  32. Membrane-associated, boron-interacting proteins isolated by boronate affinity chromatography.
    Plant Cell Physiol. 2009 Jul;50(7):1292-304 PMID: 19478072
  33. Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue.
    Plant Physiol. 2001 Aug;126(4):1698-705 PMID: 11500567
  34. Plasma membrane-cell wall contacts.
    Plant Physiol. 2000 Sep;124(1):31-8 PMID: 10982419
  35. Boron bridging of rhamnogalacturonan-II, monitored by gel electrophoresis, occurs during polysaccharide synthesis and secretion but not post-secretion.
    Plant J. 2014 Feb;77(4):534-46 PMID: 24320597
  36. Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin.
    PLoS One. 2013;8(3):e57813 PMID: 23554870
  37. bor1-1, an Arabidopsis thaliana mutant that requires a high level of boron.
    Plant Physiol. 1997 Nov;115(3):901-6 PMID: 9390427
  38. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide.
    Annu Rev Plant Biol. 2004;55:109-39 PMID: 15377216
  39. Gateway-compatible vectors for plant functional genomics and proteomics.
    Plant J. 2006 Feb;45(4):616-29 PMID: 16441352
  40. Pectin structure and biosynthesis.
    Curr Opin Plant Biol. 2008 Jun;11(3):266-77 PMID: 18486536
  41. A pectin glucuronyltransferase gene is essential for intercellular attachment in the plant meristem.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16319-24 PMID: 12451175
  42. Plants tolerant of high boron levels.
    Science. 2007 Nov 30;318(5855):1417 PMID: 18048682
  43. VvBOR1, the grapevine ortholog of AtBOR1, encodes an efflux boron transporter that is differentially expressed throughout reproductive development of Vitis vinifera L.
    Plant Cell Physiol. 2012 Feb;53(2):485-94 PMID: 22247248
  44. MUSCLE: a multiple sequence alignment method with reduced time and space complexity.
    BMC Bioinformatics. 2004 Aug 19;5:113 PMID: 15318951
  45. Boron transport in plants: co-ordinated regulation of transporters.
    Ann Bot. 2010 Jun;105(7):1103-8 PMID: 20228086
  46. Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl).
    Curr Opin Plant Biol. 2009 Jun;12(3):259-66 PMID: 19524482
  47. Boron nutrition of tobacco BY-2 cells. V. oxidative damage is the major cause of cell death induced by boron deprivation.
    Plant Cell Physiol. 2009 Jan;50(1):26-36 PMID: 19054807
  48. Boron-toxicity tolerance in barley arising from efflux transporter amplification.
    Science. 2007 Nov 30;318(5855):1446-9 PMID: 18048688
  49. A novel protein family mediates Casparian strip formation in the endodermis.
    Nature. 2011 May 19;473(7347):380-3 PMID: 21593871
  50. 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
  51. BARREN STALK FASTIGIATE1 is an AT-hook protein required for the formation of maize ears.
    Plant Cell. 2011 May;23(5):1756-71 PMID: 21540434
  52. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis.
    Curr Biol. 2011 Oct 25;21(20):1720-6 PMID: 21982593
  53. The boron requirement and cell wall properties of growing and stationary suspension-cultured chenopodium album L. cells
    Plant Physiol. 1998 Aug;117(4):1401-10 PMID: 9701596
  54. Signal integration in the control of shoot branching.
    Nat Rev Mol Cell Biol. 2011 Apr;12(4):211-21 PMID: 21427763
  55. EFFECT OF BORON DEFICIENCY UPON THE STRUCTURE OF ZEA MAYS.
    Plant Physiol. 1936 Oct;11(4):765-78 PMID: 16653384
  56. A floret by any other name: control of meristem identity in maize.
    Trends Plant Sci. 2000 Feb;5(2):61-6 PMID: 10664615
  57. The Pore Size of Non-Graminaceous Plant Cell Walls Is Rapidly Decreased by Borate Ester Cross-Linking of the Pectic Polysaccharide Rhamnogalacturonan II.
    Plant Physiol. 1999 Nov;121(3):829-838 PMID: 10557231
  58. Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants.
    Plant Physiol. 2004 Jan;134(1):339-51 PMID: 14671014
  59. 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
  60. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth.
    Science. 2001 Oct 26;294(5543):846-9 PMID: 11679668
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2014-07-00
Epub
2014-00-17
Pages
2962-77
Language
English
Region
England
NLM ID
9208688
PMCID
PMC4145125
Subset
IM
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: product@genelibs.com