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PMID: 23573247 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Regulatory patterns of a large family of defensin-like genes expressed in nodules of Medicago truncatula.

PloS one ·Vol. 8 ·No. 4 ·2013-00-00 ·Pages e60355

Nallu S, Silverstein KA, Samac DA, Bucciarelli B, Vance CP, VandenBosch KA

Abstract

Root nodules are the symbiotic organ of legumes that house nitrogen-fixing bacteria. Many genes are specifically induced in nodules during the interactions between the host plant and symbiotic rhizobia. Information regarding the regulation of expression for most of these genes is lacking. One of the largest gene families expressed in the nodules of the model legume Medicago truncatula is the nodule cysteine-rich (NCR) group of defensin-like (DEFL) genes. We used a custom Affymetrix microarray to catalog the expression changes of 566 NCRs at different stages of nodule development. Additionally, bacterial mutants were used to understand the importance of the rhizobial partners in induction of NCRs. Expression of early NCRs was detected during the initial infection of rhizobia in nodules and expression continued as nodules became mature. Late NCRs were induced concomitantly with bacteroid development in the nodules. The induction of early and late NCRs was correlated with the number and morphology of rhizobia in the nodule. Conserved 41 to 50 bp motifs identified in the upstream 1,000 bp promoter regions of NCRs were required for promoter activity. These cis-element motifs were found to be unique to the NCR family among all annotated genes in the M. truncatula genome, although they contain sub-regions with clear similarity to known regulatory motifs involved in nodule-specific expression and temporal gene regulation.

MeSH Terms
Base Sequence Chromosome Mapping Conserved Sequence Defensins/genetics,metabolism Gene Expression Regulation, Plant Medicago truncatula/genetics,metabolism,microbiology Molecular Sequence Data Plant Proteins/genetics,metabolism Plant Root Nodulation Promoter Regions, Genetic Rhizobium/physiology Root Nodules, Plant/genetics,metabolism,microbiology Sequence Deletion Transcriptome
Chemicals
Defensins Plant Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Nallu Sumitha
Department of Plant Biology, University of Minnesota, Saint Paul, Minnesota, United States of America.
Silverstein Kevin A T
Samac Deborah A
Bucciarelli Bruna
Vance Carroll P
VandenBosch Kathryn A
References (67)
67 references, click to expand
  1. Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis.
    Plant J. 2010 Feb 1;61(3):482-94 PMID: 19912567
  2. The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties.
    Nucleic Acids Res. 2004 Mar 12;32(5):1710-20 PMID: 15020707
  3. Expression of coordinately regulated defence response genes and analysis of their role in disease resistance in Medicago truncatula.
    Mol Plant Pathol. 2011 Oct;12(8):786-98 PMID: 21726379
  4. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription.
    Science. 2005 Jun 17;308(5729):1789-91 PMID: 15961669
  5. Symbiotic Nitrogen Fixation.
    Plant Cell. 1995 Jul;7(7):869-885 PMID: 12242391
  6. Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATRE-BS2* of the Sesbania rostrata leghemoglobin glb3 promoter.
    Plant Cell. 1994 Mar;6(3):317-32 PMID: 8180496
  7. Symbiotic induction of a MADS-box gene during development of alfalfa root nodules.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5273-7 PMID: 7777496
  8. Transcription reprogramming during root nodule development in Medicago truncatula.
    PLoS One. 2011 Jan 27;6(1):e16463 PMID: 21304580
  9. Combining evidence using p-values: application to sequence homology searches.
    Bioinformatics. 1998;14(1):48-54 PMID: 9520501
  10. The Medicago genome provides insight into the evolution of rhizobial symbioses.
    Nature. 2011 Nov 16;480(7378):520-4 PMID: 22089132
  11. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti Nod factors.
    Science. 1992 May 15;256(5059):998-1000 PMID: 10744524
  12. Spatio-temporal expression patterns of Arabidopsis thaliana and Medicago truncatula defensin-like genes.
    PLoS One. 2013;8(3):e58992 PMID: 23527067
  13. Peptide antibiotics and their role in innate immunity.
    Annu Rev Immunol. 1995;13:61-92 PMID: 7612236
  14. Controlling the reproductive fate of rhizobia: how universal are legume sanctions?
    New Phytol. 2009;183(4):967-979 PMID: 19594691
  15. A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs.
    Plant Physiol. 2003 May;132(1):161-73 PMID: 12746522
  16. Cloning of nodule-specific cDNAs of Galega orientalis.
    Physiol Plant. 2002 Apr;114(4):588-593 PMID: 11975733
  17. DNA binding properties of two Arabidopsis MADS domain proteins: binding consensus and dimer formation.
    Plant Cell. 1996 Jan;8(1):81-94 PMID: 8597661
  18. Genome organization of more than 300 defensin-like genes in Arabidopsis.
    Plant Physiol. 2005 Jun;138(2):600-10 PMID: 15955924
  19. Recent Advances in Medicago truncatula Genomics.
    Int J Plant Genomics. 2008;2008:256597 PMID: 18288239
  20. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis.
    Plant Cell. 1998 Dec;10(12):2103-13 PMID: 9836748
  21. Diversity and similarity among recognition sequences of Dof transcription factors.
    Plant J. 1999 Jan;17(2):209-14 PMID: 10074718
  22. Isolation and expression in transgenic tobacco and rice plants, of the cassava vein mosaic virus (CVMV) promoter.
    Plant Mol Biol. 1996 Sep;31(6):1129-39 PMID: 8914529
  23. Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation.
    New Phytol. 2010 Jul;187(2):508-520 PMID: 20456052
  24. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis.
    Science. 2010 Feb 26;327(5969):1126-9 PMID: 20185723
  25. A defensin from tomato with dual function in defense and development.
    Plant Mol Biol. 2009 Sep;71(1-2):131-43 PMID: 19533379
  26. Nitrogen Fixation, Nodule Development, and Vegetative Regrowth of Alfalfa (Medicago sativa L.) following Harvest.
    Plant Physiol. 1979 Jul;64(1):1-8 PMID: 16660893
  27. A gene expression atlas of the model legume Medicago truncatula.
    Plant J. 2008 Aug;55(3):504-13 PMID: 18410479
  28. Transcript analysis of early nodulation events in Medicago truncatula.
    Plant Physiol. 2006 Jan;140(1):221-34 PMID: 16377745
  29. Nitrogen fixation mutants of Medicago truncatula fail to support plant and bacterial symbiotic gene expression.
    Plant Physiol. 2006 Feb;140(2):671-80 PMID: 16407449
  30. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development.
    Genes Dev. 1993 Aug;7(8):1485-97 PMID: 8393417
  31. Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis.
    Plant Physiol. 2004 Feb;134(2):595-604 PMID: 14739349
  32. Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches.
    PLoS One. 2010 Mar 04;5(3):e9519 PMID: 20209049
  33. Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
    Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36 PMID: 7584402
  34. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti.
    J Bacteriol. 1998 Oct;180(19):5183-91 PMID: 9748453
  35. Interaction of a nodule specific, trans-acting factor with distinct DNA elements in the soybean leghaemoglobin Ibc(3) 5' upstream region.
    EMBO J. 1988 May;7(5):1265-71 PMID: 16453839
  36. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies.
    Nucleic Acids Res. 2003 Oct 1;31(19):5654-66 PMID: 14500829
  37. Rhizobium genetics.
    Annu Rev Genet. 1989;23:483-506 PMID: 2694941
  38. Direct ligand-receptor complex interaction controls Brassica self-incompatibility.
    Nature. 2001 Oct 4;413(6855):534-8 PMID: 11586363
  39. Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula.
    Plant Physiol. 2002 Oct;130(2):519-37 PMID: 12376622
  40. Auxin-responsive gene expression: genes, promoters and regulatory factors.
    Plant Mol Biol. 2002 Jun-Jul;49(3-4):373-85 PMID: 12036261
  41. Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis.
    PLoS Biol. 2011 Oct;9(10):e1001169 PMID: 21990963
  42. Insights into symbiotic nitrogen fixation in Medicago truncatula.
    Mol Plant Microbe Interact. 2006 Mar;19(3):330-41 PMID: 16570662
  43. Plant peptides govern terminal differentiation of bacteria in symbiosis.
    Science. 2010 Feb 26;327(5969):1122-6 PMID: 20185722
  44. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants.
    Plant J. 2007 Jul;51(2):262-80 PMID: 17565583
  45. Molecular analysis of SCARECROW genes expressed in white lupin cluster roots.
    J Exp Bot. 2010 Mar;61(5):1351-63 PMID: 20167612
  46. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells.
    Nature. 2009 Mar 19;458(7236):357-61 PMID: 19295610
  47. Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1.
    PLoS Biol. 2010 Jun 01;8(6):e1000388 PMID: 20532241
  48. Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations.
    Mol Plant Microbe Interact. 2001 Jun;14(6):695-700 PMID: 11386364
  49. Ultrastructural analysis of ineffective alfalfa nodules formed by nif::Tn5 mutants of Rhizobium meliloti.
    J Bacteriol. 1983 Jul;155(1):367-80 PMID: 6575011
  50. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?
    Nat Rev Microbiol. 2005 Mar;3(3):238-50 PMID: 15703760
  51. Sequential induction of nodulin gene expression in the developing pea nodule.
    Plant Cell. 1990 Aug;2(8):687-700 PMID: 2152123
  52. The male determinant of self-incompatibility in Brassica.
    Science. 1999 Nov 26;286(5445):1697-700 PMID: 10576728
  53. A small family of nodule specific genes from soybean.
    Nucleic Acids Res. 1987 Feb 25;15(4):1507-19 PMID: 3822835
  54. Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus.
    Nature. 2005 Oct 13;437(7061):975-80 PMID: 16222292
  55. Micropylar pollen tube guidance and burst: adapted from defense mechanisms?
    Curr Opin Plant Biol. 2009 Dec;12(6):773-80 PMID: 19896414
  56. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules.
    J Bacteriol. 1990 Aug;172(8):4295-306 PMID: 2376562
  57. Plant defensins.
    Planta. 2002 Dec;216(2):193-202 PMID: 12447532
  58. Detection of functional DNA motifs via statistical over-representation.
    Nucleic Acids Res. 2004 Feb 26;32(4):1372-81 PMID: 14988425
  59. STAMP: a web tool for exploring DNA-binding motif similarities.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W253-8 PMID: 17478497
  60. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis.
    Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5230-5 PMID: 16547129
  61. Identification of new potential regulators of the Medicago truncatula-Sinorhizobium meliloti symbiosis using a large-scale suppression subtractive hybridization approach.
    Mol Plant Microbe Interact. 2007 Mar;20(3):321-32 PMID: 17378435
  62. Plant cis-acting regulatory DNA elements (PLACE) database: 1999.
    Nucleic Acids Res. 1999 Jan 1;27(1):297-300 PMID: 9847208
  63. Analysis of Medicago truncatula nodule expressed sequence tags.
    Mol Plant Microbe Interact. 2000 Jan;13(1):62-71 PMID: 10656586
  64. Computational identification and characterization of novel genes from legumes.
    Plant Physiol. 2004 Jul;135(3):1179-97 PMID: 15266052
  65. Plant gene expression in effective and ineffective root nodules of alfalfa (Medicago sativa).
    Plant Mol Biol. 1987 Sep;9(5):469-78 PMID: 24277133
  66. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model.
    Nat Rev Microbiol. 2007 Aug;5(8):619-33 PMID: 17632573
  67. Plant defensins and virally encoded fungal toxin KP4 inhibit plant root growth.
    Planta. 2008 Jan;227(2):331-9 PMID: 17849147
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
DOI
10.1371/journal.pone.0060355
Published
2013-00-00
Epub
2013-00-01
Pages
e60355
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3613412
Subset
IM
Databases
GEO
GSE34803
External Links
PubMed source DOI: 10.1371/journal.pone.0060355 PMC Full Text View journal details
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