Home LiteratureArticle Details
PMID: 21081694 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Unraveling the evolution of auxin signaling.

Plant physiology ·Vol. 155 ·No. 1 ·2011-01-00 ·Pages 209-21

De Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, Bennett M, Jürgens G, Beeckman T

Abstract

Auxin signaling is central to plant growth and development, yet hardly anything is known about its evolutionary origin. While the presence of key players in auxin signaling has been analyzed in various land plant species, similar analyses in the green algal lineages are lacking. Here, we survey the key players in auxin biology in the available genomes of Chlorophyta species. We found that the genetic potential for auxin biosynthesis and AUXIN1 (AUX1)/LIKE AUX1- and P-GLYCOPROTEIN/ATP-BINDING CASSETTE subfamily B-dependent transport is already present in several single-celled and colony-forming Chlorophyta species. In addition, our analysis of expressed sequence tag libraries from Coleochaete orbicularis and Spirogyra pratensis, green algae of the Streptophyta clade that are evolutionarily closer to the land plants than those of the Chlorophyta clade, revealed the presence of partial AUXIN RESPONSE FACTORs and/or AUXIN/INDOLE-3-ACETIC ACID proteins (the key factors in auxin signaling) and PIN-FORMED-like proteins (the best-characterized auxin-efflux carriers). While the identification of these possible AUXIN RESPONSE FACTOR- and AUXIN/INDOLE-3-ACETIC ACID precursors and putative PIN-FORMED orthologs calls for a deeper investigation of their evolution after sequencing more intermediate genomes, it emphasizes that the canonical auxin response machinery and auxin transport mechanisms were, at least in part, already present before plants "moved" to land habitats.

MeSH Terms
Amino Acid Sequence Arabidopsis/genetics Biological Transport Chlamydomonas/genetics Chlorophyta/genetics,metabolism Evolution, Molecular Indoleacetic Acids/metabolism Molecular Sequence Data Phylogeny Promoter Regions, Genetic/genetics Proteins/chemistry,genetics,metabolism Signal Transduction/genetics
Chemicals
Indoleacetic Acids Proteins
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
De Smet Ive
Department of Plant Systems Biology, Flanders Institute for Biotechnology, 9052 Ghent, Belgium. ivsme@psb.vib-ugent.be
Voss Ute
Lau Steffen
Wilson Michael
Shao Ning
Timme Ruth E
Swarup Ranjan
Kerr Ian
Hodgman Charlie
Bock Ralph
Bennett Malcolm
Jürgens Gerd
Beeckman Tom
References (75)
75 references, click to expand
  1. Diversification of P450 genes during land plant evolution.
    Annu Rev Plant Biol. 2010;61:291-315 PMID: 20192745
  2. Evolution of multicellularity in the volvocine algae.
    Curr Opin Plant Biol. 1999 Dec;2(6):496-501 PMID: 10607653
  3. Molecular phylogeny, long-term evolution, and functional divergence of flavin-containing monooxygenases.
    Genetica. 2009 Nov;137(2):173-87 PMID: 19579011
  4. Plant ABC proteins--a unified nomenclature and updated inventory.
    Trends Plant Sci. 2008 Apr;13(4):151-9 PMID: 18299247
  5. Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1.
    Plant Cell. 2004 Nov;16(11):3069-83 PMID: 15486104
  6. Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus.
    Plant Physiol. 2010 May;153(1):128-44 PMID: 20200071
  7. Auxin: a trigger for change in plant development.
    Cell. 2009 Mar 20;136(6):1005-16 PMID: 19303845
  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. The evolution of nuclear auxin signalling.
    BMC Evol Biol. 2009 Jun 03;9:126 PMID: 19493348
  10. Exploring plant biodiversity: the Physcomitrella genome and beyond.
    Trends Plant Sci. 2008 Oct;13(10):542-9 PMID: 18762443
  11. An outlook on microalgal biofuels.
    Science. 2010 Aug 13;329(5993):796-9 PMID: 20705853
  12. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation.
    Proc Natl Acad Sci U S A. 2007 May 1;104(18):7705-10 PMID: 17460045
  13. Synthesis of phytohormones by plant-associated bacteria.
    Crit Rev Microbiol. 1995;21(1):1-18 PMID: 7576148
  14. Indole-3-acetamide-dependent auxin biosynthesis: a widely distributed way of indole-3-acetic acid production?
    Eur J Cell Biol. 2010 Dec;89(12):895-905 PMID: 20701997
  15. Mechanism of auxin-regulated gene expression in plants.
    Annu Rev Genet. 2009;43:265-85 PMID: 19686081
  16. The evolving complexity of the auxin pathway.
    Plant Cell. 2008 Jul;20(7):1738-46 PMID: 18647826
  17. New insight into the biochemical mechanisms regulating auxin transport in plants.
    Biochem J. 2007 Feb 1;401(3):613-22 PMID: 17209803
  18. Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis.
    Dev Cell. 2006 Feb;10(2):265-70 PMID: 16459305
  19. Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification.
    PLoS One. 2009 Jun 08;4(6):e5791 PMID: 19503786
  20. The Relationship between auxin transport and maize branching.
    Plant Physiol. 2008 Aug;147(4):1913-23 PMID: 18550681
  21. Green algae and the origin of land plants.
    Am J Bot. 2004 Oct;91(10):1535-56 PMID: 21652308
  22. Engineering algae for biohydrogen and biofuel production.
    Curr Opin Biotechnol. 2009 Jun;20(3):264-71 PMID: 19560336
  23. Indole as an intercellular signal in microbial communities.
    FEMS Microbiol Rev. 2010 Jul;34(4):426-44 PMID: 20070374
  24. Plant ATP-binding cassette transporters.
    Annu Rev Plant Biol. 2007;58:347-75 PMID: 17263663
  25. The Chlamydomonas genome reveals the evolution of key animal and plant functions.
    Science. 2007 Oct 12;318(5848):245-50 PMID: 17932292
  26. The role of local biosynthesis of auxin and cytokinin in plant development.
    Curr Opin Plant Biol. 2008 Feb;11(1):16-22 PMID: 18409210
  27. Local, efflux-dependent auxin gradients as a common module for plant organ formation.
    Cell. 2003 Nov 26;115(5):591-602 PMID: 14651850
  28. Auxin biosynthesis and its role in plant development.
    Annu Rev Plant Biol. 2010;61:49-64 PMID: 20192736
  29. The PIN-FORMED (PIN) protein family of auxin transporters.
    Genome Biol. 2009;10(12):249 PMID: 20053306
  30. The ABC of auxin transport: the role of p-glycoproteins in plant development.
    FEBS Lett. 2006 Feb 13;580(4):1094-102 PMID: 16359667
  31. Molecular and cellular aspects of auxin-transport-mediated development.
    Trends Plant Sci. 2007 Apr;12(4):160-8 PMID: 17369077
  32. High-affinity auxin transport by the AUX1 influx carrier protein.
    Curr Biol. 2006 Jun 6;16(11):1123-7 PMID: 16677815
  33. Indole-3-acetic acid in microbial and microorganism-plant signaling.
    FEMS Microbiol Rev. 2007 Jul;31(4):425-48 PMID: 17509086
  34. An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development.
    Plant Cell. 2005 Oct;17(10):2693-704 PMID: 16169896
  35. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter.
    Nature. 2009 Jun 25;459(7250):1136-40 PMID: 19506555
  36. Uncovering the evolutionary origin of plant molecular processes: comparison of Coleochaete (Coleochaetales) and Spirogyra (Zygnematales) transcriptomes.
    BMC Plant Biol. 2010 May 25;10:96 PMID: 20500869
  37. The auxin influx carrier LAX3 promotes lateral root emergence.
    Nat Cell Biol. 2008 Aug;10(8):946-54 PMID: 18622388
  38. Over-expression of an Arabidopsis gene encoding a glucosyltransferase of indole-3-acetic acid: phenotypic characterisation of transgenic lines.
    Plant J. 2002 Nov;32(4):573-83 PMID: 12445128
  39. Arabidopsis IAR4 modulates auxin response by regulating auxin homeostasis.
    Plant Physiol. 2009 Jun;150(2):748-58 PMID: 19395411
  40. TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development.
    Cell. 2008 Apr 4;133(1):177-91 PMID: 18394997
  41. 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
  42. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas.
    Science. 2009 Apr 10;324(5924):268-72 PMID: 19359590
  43. Charophyte algae and land plant origins.
    Trends Ecol Evol. 2004 Dec;19(12):661-6 PMID: 16701329
  44. Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis.
    Plant J. 2004 Mar;37(5):770-7 PMID: 14871316
  45. Early embryo development in Fucus distichus is auxin sensitive.
    Plant Physiol. 2002 Sep;130(1):292-302 PMID: 12226509
  46. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism.
    Science. 1996 Aug 16;273(5277):948-50 PMID: 8688077
  47. Auxin influx activity is associated with Frankia infection during actinorhizal nodule formation in Casuarina glauca.
    Plant Physiol. 2007 Aug;144(4):1852-62 PMID: 17556507
  48. Progressive sequence alignment as a prerequisite to correct phylogenetic trees.
    J Mol Evol. 1987;25(4):351-60 PMID: 3118049
  49. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis.
    Nature. 2003 Nov 13;426(6963):147-53 PMID: 14614497
  50. Approaching cellular and molecular resolution of auxin biosynthesis and metabolism.
    Cold Spring Harb Perspect Biol. 2010 Jan;2(1):a001594 PMID: 20182605
  51. Differentiation of germinal and somatic cells in Volvox carteri.
    Curr Opin Microbiol. 2003 Dec;6(6):608-13 PMID: 14662357
  52. Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe.
    Plant J. 2009 Jul;59(1):179-91 PMID: 19309458
  53. The Chlamydomonas Sourcebook. A Comprehensive Guide to Biology and Laboratory Use. Elizabeth H. Harris. Academic Press, San Diego, CA, 1989. xiv, 780 pp., illus. $145.
    Science. 1989 Dec 15;246(4936):1503-4 PMID: 17756009
  54. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants.
    Science. 2008 Jan 4;319(5859):64-9 PMID: 18079367
  55. Streptophyte algae and the origin of embryophytes.
    Ann Bot. 2009 May;103(7):999-1004 PMID: 19273476
  56. Auxin signaling in algal lineages: fact or myth?
    Trends Plant Sci. 2009 Apr;14(4):182-8 PMID: 19285905
  57. Volvox carteri as a model for studying the genetic and cytological control of morphogenesis.
    Dev Growth Differ. 2001 Dec;43(6):621-31 PMID: 11737143
  58. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex.
    Plant Cell. 2010 Sep;22(9):2943-55 PMID: 20852019
  59. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features.
    Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11647-52 PMID: 16868079
  60. Use of an inducible reporter gene system for the analysis of auxin distribution in the moss Physcomitrella patens.
    Plant Cell Rep. 2003 Aug;21(12):1143-52 PMID: 12789498
  61. Evolutionary patterns in auxin action.
    Plant Mol Biol. 2002 Jun-Jul;49(3-4):319-38 PMID: 12036257
  62. 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
  63. A role for flavin monooxygenase-like enzymes in auxin biosynthesis.
    Science. 2001 Jan 12;291(5502):306-9 PMID: 11209081
  64. Auxin: regulation, action, and interaction.
    Ann Bot. 2005 Apr;95(5):707-35 PMID: 15749753
  65. Identification and biochemical characterization of an Arabidopsis indole-3-acetic acid glucosyltransferase.
    J Biol Chem. 2001 Feb 9;276(6):4350-6 PMID: 11042207
  66. AUXIN BINDING PROTEIN 1: functional and evolutionary aspects.
    Trends Plant Sci. 2010 Aug;15(8):436-46 PMID: 20605513
  67. The Ectocarpus genome and the independent evolution of multicellularity in brown algae.
    Nature. 2010 Jun 3;465(7298):617-21 PMID: 20520714
  68. Auxin transport routes in plant development.
    Development. 2009 Aug;136(16):2675-88 PMID: 19633168
  69. A bright future for Chlamydomonas.
    Genome Biol. 2006;7(9):327 PMID: 16973002
  70. Auxin biosynthesis by the YUCCA genes in rice.
    Plant Physiol. 2007 Mar;143(3):1362-71 PMID: 17220367
  71. PIN proteins perform a rate-limiting function in cellular auxin efflux.
    Science. 2006 May 12;312(5775):914-8 PMID: 16601150
  72. A codon-optimized luciferase from Gaussia princeps facilitates the in vivo monitoring of gene expression in the model alga Chlamydomonas reinhardtii.
    Curr Genet. 2008 Jun;53(6):381-8 PMID: 18408930
  73. Unraveling the evolution of cytokinin signaling.
    Plant Physiol. 2009 Oct;151(2):782-91 PMID: 19675156
  74. Higher plant glycosyltransferases.
    Genome Biol. 2001;2(2):REVIEWS3004 PMID: 11182895
  75. Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots.
    Evol Dev. 2008 Mar-Apr;10(2):176-86 PMID: 18315811
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
DOI
10.1104/pp.110.168161
Email
ivsme@psb.vib-ugent.be
Published
2011-01-00
Epub
2010-00-16
Pages
209-21
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3075796
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/D019613/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/G023972/1 · United Kingdom
External Links
PubMed source DOI: 10.1104/pp.110.168161 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