Home LiteratureArticle Details
PMID: 16912118 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots.

Schwachtje J, Minchin PE, Jahnke S, van Dongen JT, Schittko U, Baldwin IT

Abstract

Herbivore attack elicits costly defenses that are known to decrease plant fitness by using resources that are normally slated for growth and reproduction. Additionally, plants have evolved mechanisms for tolerating attack, which are not understood on a molecular level. Using 11C-photosynthate labeling as well as sugar and enzyme measurements, we found rapid changes in sink-source relations in the annual Nicotiana attenuata after simulated herbivore attacks, which increased the allocation of sugars to roots. This herbivore-induced response is regulated by the beta-subunit of an SnRK1 (SNF1-related kinase) protein kinase, GAL83, transcripts of which are rapidly down-regulated in source leaves after herbivore attack and, when silenced, increase assimilate transport to roots. This C diversion response is activated by herbivore-specific elicitors and is independent of jasmonate signaling, which regulates most of the plant's defense responses. Herbivore attack during early stages of development increases root reserves, which, in turn, delays senescence and prolongs flowering. That attacked GAL83-silenced plants use their enhanced root reserves to prolong reproduction demonstrates that SnRK1 alters resource allocation so that plants better tolerate herbivory. This tolerance mechanism complements the likely defensive value of diverting resources to a less vulnerable location within the plant.

MeSH Terms
Animals Carbon/metabolism Feeding Behavior Molecular Sequence Data Plant Roots/growth & development,metabolism Plants, Genetically Modified Protein Serine-Threonine Kinases/genetics,metabolism Tobacco/enzymology,genetics,growth & development,metabolism
Chemicals
Carbon Protein Serine-Threonine Kinases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Schwachtje Jens
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
Minchin Peter E H
Jahnke Sigfried
van Dongen Joost T
Schittko Ursula
Baldwin Ian T
References (29)
29 references, click to expand
  1. The ecology and evolution of plant tolerance to herbivory.
    Trends Ecol Evol. 1999 May;14(5):179-185 PMID: 10322530
  2. Source-sink regulation by sugar and stress.
    Curr Opin Plant Biol. 1999 Jun;2(3):198-206 PMID: 10375568
  3. Genetic Constraints and Selection Acting on Tolerance to Herbivory in the Common Morning Glory Ipomoea purpurea.
    Am Nat. 1999 Dec;154(6):700-716 PMID: 10600614
  4. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore.
    Planta. 2000 Jan;210(2):336-42 PMID: 10664141
  5. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs.
    Plant Physiol. 2001 Feb;125(2):683-700 PMID: 11161026
  6. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses.
    Plant Physiol. 2001 Feb;125(2):711-7 PMID: 11161028
  7. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-Induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts.
    Plant Physiol. 2001 Apr;125(4):2189-202 PMID: 11299398
  8. Subcellular localization of the Snf1 kinase is regulated by specific beta subunits and a novel glucose signaling mechanism.
    Genes Dev. 2001 May 1;15(9):1104-14 PMID: 11331606
  9. Co-evolution and plant resistance to natural enemies.
    Nature. 2001 Jun 14;411(6839):857-64 PMID: 11459070
  10. An ecologically motivated analysis of plant-herbivore interactions in native tobacco.
    Plant Physiol. 2001 Dec;127(4):1449-58 PMID: 11743088
  11. Induction of Male Sterility in Wheat by Meiotic-Stage Water Deficit Is Preceded by a Decline in Invertase Activity and Changes in Carbohydrate Metabolism in Anthers.
    Plant Physiol. 1996 May;111(1):137-145 PMID: 12226280
  12. Molecular interactions between the specialist herbivore Manduca sexta (lepidoptera, sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates.
    Plant Physiol. 2003 Apr;131(4):1894-902 PMID: 12692348
  13. QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments.
    Mol Ecol. 2003 May;12(5):1153-63 PMID: 12694279
  14. Evolutionary genetics of resistance and tolerance to natural herbivory in Arabidopsis thaliana.
    Evolution. 2003 Jun;57(6):1270-80 PMID: 12894935
  15. Antisense repression of StubGAL83 affects root and tuber development in potato.
    Plant J. 2003 Jan;33(1):139-47 PMID: 12943548
  16. Highly conserved protein kinases involved in the regulation of carbon and amino acid metabolism.
    J Exp Bot. 2004 Jan;55(394):35-42 PMID: 14645392
  17. Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata.
    Plant J. 2003 Dec;36(6):794-807 PMID: 14675445
  18. Constitutive and inducible trypsin proteinase inhibitor production incurs large fitness costs in Nicotiana attenuata.
    Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1607-12 PMID: 14757829
  19. Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata.
    Plant J. 2004 May;38(4):639-49 PMID: 15125770
  20. Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations.
    Plant J. 2004 May;38(4):650-63 PMID: 15125771
  21. Silencing the jasmonate cascade: induced plant defenses and insect populations.
    Science. 2004 Jul 30;305(5684):665-8 PMID: 15232071
  22. Individual variability in herbivore-specific elicitors from the plant's perspective.
    Mol Ecol. 2004 Aug;13(8):2421-33 PMID: 15245414
  23. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin.
    Science. 2005 Dec 9;310(5754):1642-6 PMID: 16308421
  24. Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2994-9 PMID: 16481625
  25. Herbivore-induced ethylene burst reduces fitness costs of jasmonate- and oral secretion-induced defenses in Nicotiana attenuata.
    Oecologia. 2001 Apr;127(2):274-280 PMID: 24577660
  26. Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata.
    Oecologia. 2000 Aug;124(3):408-417 PMID: 28308780
  27. Overexpression of pyrophosphatase leads to increased sucrose degradation and starch synthesis, increased activities of enzymes for sucrose-starch interconversions, and increased levels of nucleotides in growing potato tubers.
    Planta. 1998 Jul;205(3):428-37 PMID: 9640668
  28. Jasmonate-induced responses are costly but benefit plants under attack in native populations.
    Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8113-8 PMID: 9653149
  29. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell?
    Annu Rev Biochem. 1998;67:821-55 PMID: 9759505
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2006-08-22
Epub
2006-00-15
Pages
12935-40
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1568949
Subset
IM
Databases
GENBANK
AY460336
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