Home LiteratureArticle Details
PMID: 16603661 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Transcription analysis of arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence.

Plant physiology ·Vol. 141 ·No. 2 ·2006-06-00 ·Pages 776-92

van der Graaff E, Schwacke R, Schneider A, Desimone M, Flügge UI, Kunze R

Abstract

A comparative transcriptome analysis for successive stages of Arabidopsis (Arabidopsis thaliana) developmental leaf senescence (NS), darkening-induced senescence of individual leaves attached to the plant (DIS), and senescence in dark-incubated detached leaves (DET) revealed many novel senescence-associated genes with distinct expression profiles. The three senescence processes share a high number of regulated genes, although the overall number of regulated genes during DIS and DET is about 2 times lower than during NS. Consequently, the number of NS-specific genes is much higher than the number of DIS- or DET-specific genes. The expression profiles of transporters (TPs), receptor-like kinases, autophagy genes, and hormone pathways were analyzed in detail. The Arabidopsis TPs and other integral membrane proteins were systematically reclassified based on the Transporter Classification system. Coordinate activation or inactivation of several genes is observed in some TP families in all three or only in individual senescence types, indicating differences in the genetic programs for remobilization of catabolites. Characteristic senescence type-specific differences were also apparent in the expression profiles of (putative) signaling kinases. For eight hormones, the expression of biosynthesis, metabolism, signaling, and (partially) response genes was investigated. In most pathways, novel senescence-associated genes were identified. The expression profiles of hormone homeostasis and signaling genes reveal additional players in the senescence regulatory network.

MeSH Terms
Arabidopsis/genetics,growth & development,metabolism Gene Expression Profiling Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Membrane Transport Proteins/genetics Plant Growth Regulators/genetics Plant Leaves/growth & development Transcription, Genetic
Chemicals
Membrane Transport Proteins Plant Growth Regulators
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
van der Graaff Eric
Institute of Botany II, University of Cologne, 50931 Cologne, Germany.
Schwacke Rainer
Schneider Anja
Desimone Marcelo
Flügge Ulf-Ingo
Kunze Reinhard
References (93)
93 references, click to expand
  1. Accumulation and remobilization of amino acids during senescence of detached and attached leaves: in planta analysis of tryptophan levels by recombinant luminescent bacteria.
    J Exp Bot. 2005 Feb;56(412):695-702 PMID: 15611144
  2. Benchmarking the CATMA microarray. A novel tool for Arabidopsis transcriptome analysis.
    Plant Physiol. 2005 Feb;137(2):588-601 PMID: 15710687
  3. Mutations in Arabidopsis acyl-CoA oxidase genes reveal distinct and overlapping roles in beta-oxidation.
    Plant J. 2005 Mar;41(6):859-74 PMID: 15743450
  4. Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades.
    Plant J. 2005 Oct;44(2):314-33 PMID: 16212609
  5. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses.
    Plant Cell. 2002 Mar;14(3):559-74 PMID: 11910004
  6. Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines.
    Plant Physiol. 2001 Jun;126(2):707-16 PMID: 11402199
  7. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana.
    Nature. 2000 Dec 14;408(6814):796-815 PMID: 11130711
  8. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana.
    J Biol Chem. 2002 Sep 6;277(36):33105-14 PMID: 12070171
  9. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis.
    Plant Physiol. 2003 Jun;132(2):530-43 PMID: 12805585
  10. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants.
    Plant Cell. 2001 Jul;13(7):1499-510 PMID: 11449047
  11. Identification of a promoter region responsible for the senescence-specific expression of SAG12.
    Plant Mol Biol. 1999 Sep;41(2):181-94 PMID: 10579486
  12. COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence.
    Plant Cell. 2004 May;16(5):1132-42 PMID: 15075400
  13. PGP4, an ATP binding cassette P-glycoprotein, catalyzes auxin transport in Arabidopsis thaliana roots.
    Plant Cell. 2005 Nov;17(11):2922-39 PMID: 16243904
  14. MIPS Arabidopsis thaliana Database (MAtDB): an integrated biological knowledge resource for plant genomics.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D373-6 PMID: 14681437
  15. Open source clustering software.
    Bioinformatics. 2004 Jun 12;20(9):1453-4 PMID: 14871861
  16. N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana.
    J Biol Chem. 2004 Nov 12;279(46):47822-32 PMID: 15342621
  17. AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana.
    Development. 2005 Oct;132(20):4563-74 PMID: 16176952
  18. BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis.
    Development. 2004 Nov;131(21):5341-51 PMID: 15486337
  19. One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated.
    Plant Mol Biol. 2001 Jul;46(4):447-57 PMID: 11485201
  20. An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana.
    Plant Mol Biol. 2004 Mar;54(5):713-25 PMID: 15356390
  21. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes.
    Nucleic Acids Res. 2004 Oct 14;32(18):5539-45 PMID: 15486203
  22. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene.
    Plant Physiol. 2002 Jul;129(3):1181-93 PMID: 12114572
  23. Mitotic and postmitotic senescence in plants.
    Sci Aging Knowledge Environ. 2003 Sep 24;2003(38):RE7 PMID: 14508060
  24. Cloning and characterization of a receptor-like protein kinase gene associated with senescence.
    Plant Physiol. 2000 Nov;124(3):1305-14 PMID: 11080306
  25. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana.
    Plant J. 2005 May;42(4):535-46 PMID: 15860012
  26. Combinatorial microarray analysis revealing arabidopsis genes implicated in cytokinin responses through the His->Asp Phosphorelay circuitry.
    Plant Cell Physiol. 2005 Feb;46(2):339-55 PMID: 15695462
  27. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members.
    Plant Physiol. 2004 Oct;136(2):2982-3000 PMID: 15466221
  28. Plant immunity: the EDS1 regulatory node.
    Curr Opin Plant Biol. 2005 Aug;8(4):383-9 PMID: 15939664
  29. A senescence-associated gene of Arabidopsis thaliana is distinctively regulated during natural and artificially induced leaf senescence.
    Plant Mol Biol. 1996 Feb;30(4):739-54 PMID: 8624406
  30. The plant-specific database. Classification of Arabidopsis proteins based on their phylogenetic profile.
    Plant Physiol. 2004 Aug;135(4):1888-92 PMID: 15326280
  31. Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes.
    Plant Mol Biol. 1999 May;40(2):267-78 PMID: 10412905
  32. Identification of brassinosteroid-related genes by means of transcript co-response analyses.
    Nucleic Acids Res. 2005 May 12;33(8):2685-96 PMID: 15891113
  33. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense.
    Plant Cell. 2003 Jan;15(1):165-78 PMID: 12509529
  34. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin.
    Plant Physiol. 2000 Dec;124(4):1706-17 PMID: 11115887
  35. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment.
    Plant Mol Biol. 1998 Jun;37(3):455-69 PMID: 9617813
  36. Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis.
    Plant Mol Biol. 2004 Sep;56(2):271-83 PMID: 15604743
  37. Phylogenetic profiling of the Arabidopsis thaliana proteome: what proteins distinguish plants from other organisms?
    Genome Biol. 2004;5(8):R53 PMID: 15287975
  38. Differential expression of senescence-associated mRNAs during leaf senescence induced by different senescence-inducing factors in Arabidopsis.
    Plant Mol Biol. 1998 Jun;37(3):445-54 PMID: 9617812
  39. Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis.
    Plant J. 2003 Apr;34(1):13-26 PMID: 12662305
  40. Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway.
    Plant J. 2002 Feb;29(4):393-403 PMID: 11846873
  41. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression.
    Plant Cell. 2000 Mar;12(3):393-404 PMID: 10715325
  42. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis.
    Plant J. 2005 May;42(4):567-85 PMID: 15860015
  43. The ABC of auxin transport: the role of p-glycoproteins in plant development.
    FEBS Lett. 2006 Feb 13;580(4):1094-102 PMID: 16359667
  44. Molecular cloning and characterization of an amidase from Arabidopsis thaliana capable of converting indole-3-acetamide into the plant growth hormone, indole-3-acetic acid.
    Phytochemistry. 2003 Feb;62(3):293-300 PMID: 12620340
  45. ARAMEMNON, a novel database for Arabidopsis integral membrane proteins.
    Plant Physiol. 2003 Jan;131(1):16-26 PMID: 12529511
  46. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1.
    Genes Dev. 1998 Dec 1;12(23):3703-14 PMID: 9851977
  47. Identification of a transcription factor specifically expressed at the onset of leaf senescence.
    Planta. 2001 Jul;213(3):469-73 PMID: 11506370
  48. AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator.
    Plant J. 2005 Jul;43(1):29-46 PMID: 15960614
  49. The Arabidopsis XET-related gene family: environmental and hormonal regulation of expression.
    Plant J. 1996 Jun;9(6):879-89 PMID: 8696366
  50. The Arabidopsis thaliana isogene NIT4 and its orthologs in tobacco encode beta-cyano-L-alanine hydratase/nitrilase.
    J Biol Chem. 2001 Jan 26;276(4):2616-21 PMID: 11060302
  51. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases.
    Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10763-8 PMID: 11526204
  52. The use of abscisic acid analogues to analyse the substrate selectivity of UGT71B6, a UDP-glycosyltransferase of Arabidopsis thaliana.
    FEBS Lett. 2005 Aug 15;579(20):4454-8 PMID: 16083885
  53. Auxin gradient theory of abscission regulation.
    Science. 1955 Apr 29;121(3148):644-5 PMID: 14372971
  54. Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence.
    Plant Physiol. 2002 Mar;128(3):876-84 PMID: 11891244
  55. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses.
    Plant Cell. 2004 Jul;16(7):1925-37 PMID: 15208394
  56. Inhibition of leaf senescence by autoregulated production of cytokinin.
    Science. 1995 Dec 22;270(5244):1986-8 PMID: 8592746
  57. Changes in gene expression in response to altered SHL transcript levels.
    Plant Mol Biol. 2003 Dec;53(6):805-20 PMID: 15082927
  58. Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis.
    Plant Mol Biol. 2003 Sep;53(1-2):61-74 PMID: 14756307
  59. Cloning of two gibberellin-regulated cDNAs from Arabidopsis thaliana by subtractive hybridization: expression of the tonoplast water channel, gamma-TIP, is increased by GA3.
    Plant Mol Biol. 1994 Feb;24(4):603-15 PMID: 8155880
  60. Transcriptome profiling of the response of Arabidopsis suspension culture cells to Suc starvation.
    Plant Physiol. 2004 Aug;135(4):2330-47 PMID: 15310832
  61. Molecular cloning and functional expression of gibberellin 2- oxidases, multifunctional enzymes involved in gibberellin deactivation.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4698-703 PMID: 10200325
  62. The Control of Apical Bud Growth and Senescence by Auxin and Gibberellin in Genetic Lines of Peas.
    Plant Physiol. 1997 Feb;113(2):631-637 PMID: 12223631
  63. Contrasting modes of diversification in the Aux/IAA and ARF gene families.
    Plant Physiol. 2004 Jul;135(3):1738-52 PMID: 15247399
  64. The IUBMB-endorsed transporter classification system.
    Mol Biotechnol. 2004 Jul;27(3):253-62 PMID: 15247498
  65. Expression profiling of cytokinin action in Arabidopsis.
    Plant Physiol. 2003 Aug;132(4):1998-2011 PMID: 12913156
  66. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid.
    Plant Cell. 2005 Feb;17(2):616-27 PMID: 15659623
  67. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice.
    Plant Cell. 2004 May;16(5):1220-34 PMID: 15105442
  68. Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5961-6 PMID: 9159183
  69. Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species.
    J Plant Res. 2003 Jun;116(3):241-52 PMID: 12721786
  70. Quantitation of the rapid electron donors to P700, the functional plastoquinone pool, and the ratio of the photosystems in spinach chloroplasts.
    J Biol Chem. 1984 Nov 25;259(22):14003-10 PMID: 6389539
  71. Salicylic acid has a role in regulating gene expression during leaf senescence.
    Plant J. 2000 Sep;23(5):677-85 PMID: 10972893
  72. Delayed Leaf Senescence in Tobacco Plants Transformed with tmr, a Gene for Cytokinin Production in Agrobacterium.
    Plant Cell. 1991 Jul;3(7):647-656 PMID: 12324608
  73. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy.
    Plant Cell. 2004 Nov;16(11):2967-83 PMID: 15494556
  74. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana.
    Plant J. 1997 Sep;12(3):527-35 PMID: 9351240
  75. Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants.
    Plant Physiol. 2001 Nov;127(3):876-86 PMID: 11706170
  76. Reliability of gene expression ratios for cDNA microarrays in multiconditional experiments with a reference design.
    Nucleic Acids Res. 2004 Feb 13;32(3):e29 PMID: 14966261
  77. Two-component signal transduction pathways in Arabidopsis.
    Plant Physiol. 2002 Jun;129(2):500-15 PMID: 12068096
  78. BRASSINOSTEROIDS: Essential Regulators of Plant Growth and Development.
    Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:427-451 PMID: 15012241
  79. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family.
    Plant Cell. 2002 Jan;14(1):275-86 PMID: 11826312
  80. Auxin: regulation, action, and interaction.
    Ann Bot. 2005 Apr;95(5):707-35 PMID: 15749753
  81. Targets of AtWRKY6 regulation during plant senescence and pathogen defense.
    Genes Dev. 2002 May 1;16(9):1139-49 PMID: 12000796
  82. The molecular analysis of leaf senescence--a genomics approach.
    Plant Biotechnol J. 2003 Jan;1(1):3-22 PMID: 17147676
  83. A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype.
    Plant Cell. 2000 Mar;12(3):443-55 PMID: 10715329
  84. Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence.
    Plant J. 2002 Oct;32(1):51-63 PMID: 12366800
  85. Senescence-related gene expression profiles of rosette leaves of Arabidopsis thaliana: leaf age versus plant age.
    Plant Biol (Stuttg). 2004 Mar-Apr;6(2):178-83 PMID: 15045669
  86. Genetic analysis of indole-3-butyric acid responses in Arabidopsis thaliana reveals four mutant classes.
    Genetics. 2000 Nov;156(3):1323-37 PMID: 11063705
  87. Molecular events in senescing Arabidopsis leaves.
    Plant J. 2004 Aug;39(4):612-28 PMID: 15272878
  88. Cross talk between gibberellin and cytokinin: the Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling.
    Plant Cell. 2005 Jan;17(1):92-102 PMID: 15608330
  89. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways.
    Plant Physiol. 2005 Aug;138(4):2097-110 PMID: 16040659
  90. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.
    Plant Cell. 2003 Nov;15(11):2532-50 PMID: 14555694
  91. Starvation-induced expression of autophagy-related genes in Arabidopsis.
    Biol Cell. 2006 Jan;98(1):53-67 PMID: 16354162
  92. Nitrogen metabolism and remobilization during senescence.
    J Exp Bot. 2002 Apr;53(370):927-37 PMID: 11912235
  93. A functional-phylogenetic classification system for transmembrane solute transporters.
    Microbiol Mol Biol Rev. 2000 Jun;64(2):354-411 PMID: 10839820
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
DOI
10.1104/pp.106.079293
Published
2006-06-00
Epub
2006-00-07
Pages
776-92
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC1475451
Subset
IM
External Links
PubMed source DOI: 10.1104/pp.106.079293 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