Home LiteratureArticle Details
PMID: 19435934 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation.

The Plant cell ·Vol. 21 ·No. 5 ·2009-05-00 ·Pages 1495-511

Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C

Abstract

Plant roots show an impressive degree of plasticity in adapting their branching patterns to ever-changing growth conditions. An important mechanism underlying this adaptation ability is the interaction between hormonal and developmental signals. Here, we analyze the interaction of jasmonate with auxin to regulate lateral root (LR) formation through characterization of an Arabidopsis thaliana mutant, jasmonate-induced defective lateral root1 (jdl1/asa1-1). We demonstrate that, whereas exogenous jasmonate promotes LR formation in wild-type plants, it represses LR formation in jdl1/asa1-1. JDL1 encodes the auxin biosynthetic gene ANTHRANILATE SYNTHASE alpha1 (ASA1), which is required for jasmonate-induced auxin biosynthesis. Jasmonate elevates local auxin accumulation in the basal meristem of wild-type roots but reduces local auxin accumulation in the basal meristem of mutant roots, suggesting that, in addition to activating ASA1-dependent auxin biosynthesis, jasmonate also affects auxin transport. Indeed, jasmonate modifies the expression of auxin transport genes in an ASA1-dependent manner. We further provide evidence showing that the action mechanism of jasmonate to regulate LR formation through ASA1 differs from that of ethylene. Our results highlight the importance of ASA1 in jasmonate-induced auxin biosynthesis and reveal a role for jasmonate in the attenuation of auxin transport in the root and the fine-tuning of local auxin distribution in the root basal meristem.

MeSH Terms
Acetates/metabolism,pharmacology Anthranilate Synthase/genetics,metabolism,pharmacology Arabidopsis/drug effects,metabolism,physiology Arabidopsis Proteins/genetics,metabolism,pharmacology,physiology Biological Transport/drug effects Cyclopentanes/metabolism,pharmacology Ethylenes/pharmacology Indoleacetic Acids/metabolism Mutation Oxylipins/metabolism,pharmacology Plant Roots/drug effects,genetics,growth & development,metabolism
Chemicals
Acetates Arabidopsis Proteins Cyclopentanes Ethylenes Indoleacetic Acids Oxylipins methyl jasmonate ethylene ASA1 protein, Arabidopsis Anthranilate Synthase
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Sun Jiaqiang
State Key Laboratory of Plant Genomics, National Centre for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
Xu Yingxiu
Ye Songqing
Jiang Hongling
Chen Qian
Liu Fang
Zhou Wenkun
Chen Rong
Li Xugang
Tietz Olaf
Wu Xiaoyan
Cohen Jerry D
Palme Klaus
Li Chuanyou
References (74)
74 references, click to expand
  1. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility.
    Science. 1998 May 15;280(5366):1091-4 PMID: 9582125
  2. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis.
    Development. 2007 Feb;134(4):681-90 PMID: 17215297
  3. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis.
    Genes Dev. 2006 Jul 1;20(13):1790-9 PMID: 16818609
  4. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  5. Gravity-regulated differential auxin transport from columella to lateral root cap cells.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2987-91 PMID: 12594336
  6. Jasmonate: an oxylipin signal with many roles in plants.
    Vitam Horm. 2005;72:431-56 PMID: 16492478
  7. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators.
    Science. 1993 Oct 22;262(5133):539-44 PMID: 8211181
  8. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
    Plant Cell. 1997 Nov;9(11):1963-71 PMID: 9401121
  9. Bestatin, an inhibitor of aminopeptidases, provides a chemical genetics approach to dissect jasmonate signaling in Arabidopsis.
    Plant Physiol. 2006 Aug;141(4):1400-13 PMID: 16798948
  10. Auxin-mediated cell cycle activation during early lateral root initiation.
    Plant Cell. 2002 Oct;14(10):2339-51 PMID: 12368490
  11. A high-throughput method for the quantitative analysis of indole-3-acetic acid and other auxins from plant tissue.
    Anal Biochem. 2008 Jan 15;372(2):177-88 PMID: 17889819
  12. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis.
    Plant Cell. 2007 Jul;19(7):2225-45 PMID: 17616737
  13. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal.
    Nat Cell Biol. 2005 Nov;7(11):1057-65 PMID: 16244669
  14. Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana.
    Plant J. 2008 Jul;55(2):175-87 PMID: 18363780
  15. Specialized zones of development in roots.
    Plant Physiol. 1995;109:725-7 PMID: 11539165
  16. Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression.
    Development. 2005 Oct;132(20):4521-31 PMID: 16192309
  17. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex.
    Genes Dev. 2001 Oct 15;15(20):2648-53 PMID: 11641271
  18. Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis.
    Plant J. 2002 Jan;29(2):153-68 PMID: 11862947
  19. Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you.
    Plant Physiol. 2000 Jul;123(3):795-805 PMID: 10889228
  20. Branching out in new directions: the control of root architecture by lateral root formation.
    New Phytol. 2008;179(3):595-614 PMID: 18452506
  21. Organization and cell differentiation in lateral roots of Arabidopsis thaliana.
    Development. 1997 Jan;124(1):33-44 PMID: 9006065
  22. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration.
    Methods Mol Biol. 1998;82:259-66 PMID: 9664431
  23. 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
  24. Auxin transport promotes Arabidopsis lateral root initiation.
    Plant Cell. 2001 Apr;13(4):843-52 PMID: 11283340
  25. Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings.
    Plant J. 2002 Feb;29(3):325-32 PMID: 11844109
  26. Auxin is a positive regulator for ethylene-mediated response in the growth of Arabidopsis roots.
    Plant Cell Physiol. 2001 Mar;42(3):301-7 PMID: 11266581
  27. Lateral root initiation or the birth of a new meristem.
    Plant Mol Biol. 2006 Apr;60(6):871-87 PMID: 16724258
  28. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root.
    Cell. 1999 Nov 24;99(5):463-72 PMID: 10589675
  29. Local, efflux-dependent auxin gradients as a common module for plant organ formation.
    Cell. 2003 Nov 26;115(5):591-602 PMID: 14651850
  30. Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana.
    Plant J. 2008 Jul;55(2):335-47 PMID: 18435826
  31. Mutations in Arabidopsis thaliana genes involved in the tryptophan biosynthesis pathway affect root waving on tilted agar surfaces.
    Plant J. 1998 Oct;16(2):145-54 PMID: 9839461
  32. Auxin distribution and plant pattern formation: how many angels can dance on the point of PIN?
    Cell. 2005 Jun 17;121(6):819-22 PMID: 15960970
  33. BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:355-381 PMID: 15012267
  34. 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
  35. Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6837-40 PMID: 11607311
  36. Hormone interactions during lateral root formation.
    Plant Mol Biol. 2009 Mar;69(4):437-49 PMID: 18982413
  37. Intrinsic and environmental response pathways that regulate root system architecture.
    Plant Cell Environ. 2005 Jan;28(1):67-77 PMID: 16021787
  38. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux.
    Cell. 2007 Sep 21;130(6):1044-56 PMID: 17889649
  39. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics.
    Plant Cell. 1995 Jul;7(7):921-34 PMID: 7640526
  40. Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana.
    Plant Cell. 2004 Jul;16(7):1898-911 PMID: 15208397
  41. An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1.
    Plant Physiol. 2002 Oct;130(2):887-94 PMID: 12376653
  42. A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana.
    Plant J. 2002 Apr;30(1):95-106 PMID: 11967096
  43. IAR3 encodes an auxin conjugate hydrolase from Arabidopsis.
    Plant Cell. 1999 Mar;11(3):365-76 PMID: 10072397
  44. The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light.
    Plant Cell. 2004 May;16(5):1191-205 PMID: 15100399
  45. A pathway for lateral root formation in Arabidopsis thaliana.
    Genes Dev. 1995 Sep 1;9(17):2131-42 PMID: 7657165
  46. Dissecting Arabidopsis lateral root development.
    Trends Plant Sci. 2003 Apr;8(4):165-71 PMID: 12711228
  47. The auxin influx carrier LAX3 promotes lateral root emergence.
    Nat Cell Biol. 2008 Aug;10(8):946-54 PMID: 18622388
  48. Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth.
    Plant Cell. 2007 Jan;19(1):148-62 PMID: 17237352
  49. Auxin-mediated lateral root formation in higher plants.
    Int Rev Cytol. 2007;256:111-37 PMID: 17241906
  50. Jasmonate signaling: toward an integrated view.
    Plant Physiol. 2008 Apr;146(4):1459-68 PMID: 18390489
  51. AXR4 is required for localization of the auxin influx facilitator AUX1.
    Science. 2006 May 26;312(5777):1218-20 PMID: 16690816
  52. Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway.
    Plant Cell. 1992 Jun;4(6):721-33 PMID: 1392592
  53. The SCF(COI1) ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis.
    Plant Cell. 2002 Aug;14(8):1919-35 PMID: 12172031
  54. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis.
    Cell. 2002 Mar 8;108(5):661-73 PMID: 11893337
  55. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution.
    Plant Cell. 2007 Jul;19(7):2197-212 PMID: 17630274
  56. Flavonoids act as negative regulators of auxin transport in vivo in arabidopsis.
    Plant Physiol. 2001 Jun;126(2):524-35 PMID: 11402184
  57. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation.
    Plant Cell. 2007 Jul;19(7):2186-96 PMID: 17630275
  58. Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development.
    Cell Mol Life Sci. 2006 Dec;63(23):2738-54 PMID: 17013565
  59. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  60. Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects.
    Plant Cell. 1997 May;9(5):745-57 PMID: 9165751
  61. Sites and regulation of auxin biosynthesis in Arabidopsis roots.
    Plant Cell. 2005 Apr;17(4):1090-104 PMID: 15772288
  62. Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana.
    Planta. 2001 Nov;214(1):30-6 PMID: 11762168
  63. Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein.
    Plant J. 1999 Nov;20(4):503-8 PMID: 10607302
  64. Cell cycle: the key to plant growth control?
    Trends Plant Sci. 2003 Apr;8(4):154-8 PMID: 12711226
  65. The jasmonate signal pathway.
    Plant Cell. 2002;14 Suppl:S153-64 PMID: 12045275
  66. Plant immunity to insect herbivores.
    Annu Rev Plant Biol. 2008;59:41-66 PMID: 18031220
  67. Cytokinins act directly on lateral root founder cells to inhibit root initiation.
    Plant Cell. 2007 Dec;19(12):3889-900 PMID: 18065686
  68. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development.
    Ann Bot. 2007 Oct;100(4):681-97 PMID: 17513307
  69. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.
    Nature. 2005 Jan 6;433(7021):39-44 PMID: 15635403
  70. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis.
    Science. 1999 Jun 25;284(5423):2148-52 PMID: 10381874
  71. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling.
    Plant Cell. 2002 Mar;14(3):589-97 PMID: 11910006
  72. Auxin: regulation, action, and interaction.
    Ann Bot. 2005 Apr;95(5):707-35 PMID: 15749753
  73. A Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis.
    Plant Cell. 2005 Aug;17(8):2230-42 PMID: 15980261
  74. Isolation and Identification of a Senescence-promoting Substance from Wormwood (Artemisia absinthium L.).
    Plant Physiol. 1980 Aug;66(2):246-9 PMID: 16661414
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2009-05-00
Epub
2009-00-12
Pages
1495-511
Language
English
Region
England
NLM ID
9208688
PMCID
PMC2700526
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