Home LiteratureArticle Details
PMID: 20675575 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1.

The Plant cell ·Vol. 22 ·No. 7 ·2010-07-00 ·Pages 2171-83

Ariel F, Diet A, Verdenaud M, Gruber V, Frugier F, Chan R, Crespi M

Abstract

The adaptation of root architecture to environmental constraints is a major agricultural trait, notably in legumes, the third main crop worldwide. This root developmental plasticity depends on the formation of lateral roots (LRs) emerging from primary roots. In the model legume Medicago truncatula, the HD-Zip I transcription factor HB1 is expressed in primary and lateral root meristems and induced by salt stress. Constitutive expression of HB1 in M. truncatula roots alters their architecture, whereas hb1 TILLING mutants showed increased lateral root emergence. Electrophoretic mobility shift assay, promoter mutagenesis, and chromatin immunoprecipitation-PCR assays revealed that HB1 directly recognizes a CAATAATTG cis-element present in the promoter of a LOB-like (for Lateral Organ Boundaries) gene, LBD1, transcriptionally regulated by auxin. Expression of these genes in response to abscisic acid and auxin and their behavior in hb1 mutants revealed an HB1-mediated repression of LBD1 acting during LR emergence. M. truncatula HB1 regulates an adaptive developmental response to minimize the root surface exposed to adverse environmental stresses.

MeSH Terms
Amino Acid Sequence Chromatin Immunoprecipitation Electrophoretic Mobility Shift Assay Medicago truncatula/growth & development,metabolism Molecular Sequence Data Plant Roots/growth & development Polymerase Chain Reaction Promoter Regions, Genetic Sequence Homology, Amino Acid Transcription Factors/chemistry,metabolism
Chemicals
Transcription Factors
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Ariel Federico
Instituto de Agrobiotecnología del Litoral, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional del Litoral, CP 3000 Santa Fe, Argentina.
Diet Anouck
Verdenaud Marion
Gruber Véronique
Frugier Florian
Chan Raquel
Crespi Martin
References (58)
58 references, click to expand
  1. Estimating genome conservation between crop and model legume species.
    Proc Natl Acad Sci U S A. 2004 Oct 26;101(43):15289-94 PMID: 15489274
  2. Lateral root emergence: a difficult birth.
    J Exp Bot. 2009;60(13):3637-43 PMID: 19635746
  3. A novel plant leucine-rich repeat receptor kinase regulates the response of Medicago truncatula roots to salt stress.
    Plant Cell. 2009 Feb;21(2):668-80 PMID: 19244136
  4. The true story of the HD-Zip family.
    Trends Plant Sci. 2007 Sep;12(9):419-26 PMID: 17698401
  5. Survival of the flexible: hormonal growth control and adaptation in plant development.
    Nat Rev Genet. 2009 May;10(5):305-17 PMID: 19360022
  6. A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula.
    Plant J. 2010 Apr 1;62(1):100-12 PMID: 20088899
  7. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor.
    Plant Cell. 2008 Dec;20(12):3258-72 PMID: 19106375
  8. Expression of sunflower homeodomain containing proteins in Escherichia coli: purification and functional studies.
    Protein Expr Purif. 1998 Jun;13(1):97-103 PMID: 9631521
  9. Identification of a Rhizobium meliloti pSym2011 region controlling the host specificity of root hair curling and nodulation.
    J Bacteriol. 1985 Dec;164(3):1200-10 PMID: 4066612
  10. De novo organ formation from differentiated cells: root nodule organogenesis.
    Sci Signal. 2008 Dec 09;1(49):re11 PMID: 19066400
  11. A novel role for abscisic acid emerges from underground.
    Trends Plant Sci. 2006 Sep;11(9):434-9 PMID: 16890475
  12. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties.
    Cell. 1992 Jul 24;70(2):351-64 PMID: 1638635
  13. The lateral organ boundaries gene defines a novel, plant-specific gene family.
    Plant Physiol. 2002 Jun;129(2):747-61 PMID: 12068116
  14. Conserved and diverse mechanisms in root development.
    Curr Opin Plant Biol. 2008 Feb;11(1):70-4 PMID: 18006363
  15. Identification of regulatory pathways involved in the reacquisition of root growth after salt stress in Medicago truncatula.
    Plant J. 2007 Jul;51(1):1-17 PMID: 17488237
  16. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.
    Genome Biol. 2002 Jun 18;3(7):RESEARCH0034 PMID: 12184808
  17. Response of root branching to abscisic acid is correlated with nodule formation both in legumes and nonlegumes.
    Am J Bot. 2005 Oct;92(10):1675-83 PMID: 21646084
  18. Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype.
    Plant J. 2000 Jul;23(1):97-114 PMID: 10929105
  19. Three sequenced legume genomes and many crop species: rich opportunities for translational genomics.
    Plant Physiol. 2009 Nov;151(3):970-7 PMID: 19759344
  20. The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid.
    Plant J. 1996 Aug;10(2):375-81 PMID: 8771791
  21. Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula.
    Plant Cell. 2008 Oct;20(10):2681-95 PMID: 18931020
  22. ARL1, a LOB-domain protein required for adventitious root formation in rice.
    Plant J. 2005 Jul;43(1):47-56 PMID: 15960615
  23. Organization and cell differentiation in lateral roots of Arabidopsis thaliana.
    Development. 1997 Jan;124(1):33-44 PMID: 9006065
  24. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19.
    Plant Cell. 2005 Feb;17(2):444-63 PMID: 15659631
  25. Arabidopsis lateral root development: an emerging story.
    Trends Plant Sci. 2009 Jul;14(7):399-408 PMID: 19559642
  26. The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis.
    Plant Mol Biol. 2004 Jul;55(5):663-77 PMID: 15604708
  27. Identification of transcription factors involved in root apex responses to salt stress in Medicago truncatula.
    Mol Genet Genomics. 2009 Jan;281(1):55-66 PMID: 18987888
  28. Abscisic acid rescues the root meristem defects of the Medicago truncatula latd mutant.
    Dev Biol. 2007 Apr 1;304(1):297-307 PMID: 17239844
  29. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula.
    Plant Cell. 2009 Feb;21(2):545-57 PMID: 19252081
  30. ProtTest: selection of best-fit models of protein evolution.
    Bioinformatics. 2005 May 1;21(9):2104-5 PMID: 15647292
  31. REMORA: a pilot in the ocean of BioMoby web-services.
    Bioinformatics. 2006 Apr 1;22(7):900-1 PMID: 16423924
  32. An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis.
    Plant J. 2003 Feb;33(3):543-55 PMID: 12581312
  33. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells.
    Proc Natl Acad Sci U S A. 2008 Jun 24;105(25):8790-4 PMID: 18559858
  34. Hormone interactions during lateral root formation.
    Plant Mol Biol. 2009 Mar;69(4):437-49 PMID: 18982413
  35. Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships.
    Plant Physiol. 2005 Sep;139(1):509-18 PMID: 16055682
  36. Tendril-less regulates tendril formation in pea leaves.
    Plant Cell. 2009 Feb;21(2):420-8 PMID: 19208900
  37. The Medicago truncatula ortholog of Arabidopsis EIN2, sickle, is a negative regulator of symbiotic and pathogenic microbial associations.
    Plant J. 2008 Aug;55(4):580-95 PMID: 18435823
  38. The auxin influx carrier LAX3 promotes lateral root emergence.
    Nat Cell Biol. 2008 Aug;10(8):946-54 PMID: 18622388
  39. 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
  40. ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis.
    Plant J. 2001 Dec;28(6):655-62 PMID: 11851911
  41. Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis.
    Plant Cell. 2009 Nov;21(11):3567-84 PMID: 19933203
  42. Bayesian inference of phylogeny and its impact on evolutionary biology.
    Science. 2001 Dec 14;294(5550):2310-4 PMID: 11743192
  43. Legume transcription factors: global regulators of plant development and response to the environment.
    Plant Physiol. 2007 Jun;144(2):538-49 PMID: 17556517
  44. MView: a web-compatible database search or multiple alignment viewer.
    Bioinformatics. 1998;14(4):380-1 PMID: 9632837
  45. The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis.
    Plant J. 2003 Apr;34(1):67-75 PMID: 12662310
  46. GATEWAY vectors for Agrobacterium-mediated plant transformation.
    Trends Plant Sci. 2002 May;7(5):193-5 PMID: 11992820
  47. Two ABREs, two redundant root-specific and one W-box cis-acting elements are functional in the sunflower HAHB4 promoter.
    Plant Physiol Biochem. 2008 Oct;46(10):860-7 PMID: 18586510
  48. LATERAL ORGAN BOUNDARIES defines a new family of DNA-binding transcription factors and can interact with specific bHLH proteins.
    Nucleic Acids Res. 2007;35(19):6663-71 PMID: 17913740
  49. Optimizing TILLING populations for reverse genetics in Medicago truncatula.
    Plant Biotechnol J. 2009 Jun;7(5):430-41 PMID: 19490506
  50. LBD18/ASL20 regulates lateral root formation in combination with LBD16/ASL18 downstream of ARF7 and ARF19 in Arabidopsis.
    Plant Physiol. 2009 Nov;151(3):1377-89 PMID: 19717544
  51. Expression patterns of novel genes encoding homeodomain leucine-zipper proteins in Arabidopsis thaliana.
    Plant Mol Biol. 1994 Oct;26(1):145-54 PMID: 7948864
  52. Recent developments in the MAFFT multiple sequence alignment program.
    Brief Bioinform. 2008 Jul;9(4):286-98 PMID: 18372315
  53. Differential expression of the Arabidopsis cytochrome c genes Cytc-1 and Cytc-2. Evidence for the involvement of TCP-domain protein-binding elements in anther- and meristem-specific expression of the Cytc-1 gene.
    Plant Physiol. 2005 Sep;139(1):88-100 PMID: 16113211
  54. The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti.
    Plant Cell. 2006 Oct;18(10):2680-93 PMID: 17028204
  55. Hidden branches: developments in root system architecture.
    Annu Rev Plant Biol. 2007;58:93-113 PMID: 17177637
  56. The LATD gene of Medicago truncatula is required for both nodule and root development.
    Mol Plant Microbe Interact. 2005 Jun;18(6):521-32 PMID: 15986921
  57. Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic Acid.
    Plant Physiol. 2006 Nov;142(3):1065-74 PMID: 16963523
  58. Calmodulin interacts with and regulates the RNA-binding activity of an Arabidopsis polyadenylation factor subunit.
    Plant Physiol. 2006 Apr;140(4):1507-21 PMID: 16500995
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
DOI
10.1105/tpc.110.074823
Published
2010-07-00
Epub
2010-00-30
Pages
2171-83
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2929095
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.110.074823 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2