Home LiteratureArticle Details
PMID: 14701914 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid.

Plant physiology ·Vol. 134 ·No. 1 ·2004-01-00 ·Pages 420-31

Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H

Abstract

When attacked by a phloem-feeding greenbug aphid (Schizaphis graminum), sorghum (Sorghum bicolor) activates jasmonic acid (JA)- and salicylic acid (SA)-regulated genes, as well as genes outside known wounding and SA signaling pathways. A collection of 672 cDNAs was obtained by differential subtraction with cDNAs prepared from sorghum seedlings infested by greenbug aphids and those from uninfested seedlings. Subsequent expression profiling using DNA microarray and northern-blot analyses identified 82 transcript types from this collection responsive to greenbug feeding, methyl jasmonate (MeJA), or SA application. DNA sequencing analyses indicated that these encoded proteins functioning in direct defense, defense signaling, oxidative burst, secondary metabolism, abiotic stress, cell maintenance, and photosynthesis, as well as proteins of unknown function. In response to insect feeding, sorghum increased transcript abundance of numerous defense genes, with some SA-dependent pathogenesis-related genes responding to greenbug more strongly than to SA. In contrast, only weak induction of MeJA-regulated defense genes was observed after greenbug treatment. However, infestation tests confirmed that JA-regulated pathways were effective in plant defense against greenbugs. Activation of certain transcripts exclusively by greenbug infestation was observed, and may represent unique signal transduction events independent of JA- and SA-regulated pathways. Results indicate that plants coordinately regulate defense gene expression when attacked by phloem-feeding aphids, but also suggest that aphids are able to avoid triggering activation of some otherwise potentially effective plant defensive machinery, possibly through their particular mode of feeding.

MeSH Terms
Animals Aphids/pathogenicity Cyclopentanes/metabolism DNA, Complementary/genetics DNA, Plant/genetics Gene Expression Regulation, Plant Genes, Plant Hydrogen Peroxide/metabolism Oxylipins Photosynthesis/genetics Plant Diseases/genetics,parasitology Salicylic Acid/metabolism Signal Transduction Sorghum/genetics,parasitology,physiology Transcription, Genetic
Chemicals
Cyclopentanes DNA, Complementary DNA, Plant Oxylipins jasmonic acid Hydrogen Peroxide Salicylic Acid
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Zhu-Salzman Keyan
Department of Entomology, Texas A&M University, College Station, Texas 77843, USA. ksalzman@tamu.edu
Salzman Ron A
Ahn Ji-Eun
Koiwa Hisashi
References (52)
52 references, click to expand
  1. Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth.
    Plant Physiol. 2000 Nov;124(3):1007-18 PMID: 11080278
  2. Wound signaling in tomato plants. Evidence that aba is not a primary signal for defense gene activation
    Plant Physiol. 1998 Jun;117(2):687-93 PMID: 9625722
  3. 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
  4. Jasmonate and salicylate as global signals for defense gene expression.
    Curr Opin Plant Biol. 1998 Oct;1(5):404-11 PMID: 10066616
  5. Resistance to an herbivore through engineered cyanogenic glucoside synthesis.
    Science. 2001 Sep 7;293(5536):1826-8 PMID: 11474068
  6. 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
  7. Activation of Host Defense Mechanisms by Elevated Production of H2O2 in Transgenic Plants.
    Plant Physiol. 1997 Oct;115(2):427-435 PMID: 12223817
  8. Plant responses to insect herbivory: the emerging molecular analysis.
    Annu Rev Plant Biol. 2002;53:299-328 PMID: 12221978
  9. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis.
    Plant Cell. 2000 May;12(5):707-20 PMID: 10810145
  10. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis.
    Nature. 2002 Sep 26;419(6905):399-403 PMID: 12353036
  11. beta-Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2036-40 PMID: 11607516
  12. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.
    Cell. 1998 Mar 20;92(6):773-84 PMID: 9529253
  13. Salicylic Acid Inhibits Synthesis of Proteinase Inhibitors in Tomato Leaves Induced by Systemin and Jasmonic Acid.
    Plant Physiol. 1995 Aug;108(4):1741-1746 PMID: 12228577
  14. Evidence for Chewing Insect-Specific Molecular Events Distinct from a General Wound Response in Leaves.
    Plant Physiol. 1997 Dec;115(4):1299-1305 PMID: 12223872
  15. Effect of geminivirus infection and Bemisia infestation on accumulation of pathogenesis-related proteins in tomato.
    Arch Insect Biochem Physiol. 2002 Apr;49(4):203-14 PMID: 11921078
  16. Source-sink regulation by sugar and stress.
    Curr Opin Plant Biol. 1999 Jun;2(3):198-206 PMID: 10375568
  17. BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48:355-381 PMID: 15012267
  18. Positional specificity of a phospholipase A activity induced by wounding, systemin, and oligosaccharide elicitors in tomato leaves
    Plant Cell. 1999 Nov;11(11):2249-60 PMID: 10559447
  19. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways.
    Plant Physiol. 2001 Feb;125(2):1074-85 PMID: 11161062
  20. Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):1146-51 PMID: 9927708
  21. 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
  22. Rapid, systemic repression of the synthesis of ribulose 1,5-bisphosphate carboxylase small-subunit mRNA in fungus-infected or elicitor-treated potato leaves.
    Planta. 1990 May;181(2):216-9 PMID: 24196739
  23. Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana.
    Plant J. 1999 Oct;20(2):135-142 PMID: 10571873
  24. Defense activation and enhanced pathogen tolerance induced by H2O2 in transgenic tobacco.
    Proc Natl Acad Sci U S A. 1998 May 12;95(10):5818-23 PMID: 9576968
  25. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  26. Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid.
    Plant J. 2003 Feb;33(4):733-42 PMID: 12609045
  27. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions.
    Arch Insect Biochem Physiol. 2002 Dec;51(4):182-203 PMID: 12432519
  28. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.
    Cell. 1997 Jan 10;88(1):57-63 PMID: 9019406
  29. Reduction of light-induced anthocyanin accumulation in inoculated sorghum mesocotyls. Implications for a compensatory role in the defense response.
    Plant Physiol. 1998 Mar;116(3):979-89 PMID: 9501130
  30. The systemin signaling pathway: differential activation of plant defensive genes.
    Biochim Biophys Acta. 2000 Mar 7;1477(1-2):112-21 PMID: 10708853
  31. Physiological modification of the host feeding site by cereal aphids (Homoptera: Aphididae).
    J Econ Entomol. 2002 Apr;95(2):463-8 PMID: 12020028
  32. RNA commutes to work: regulation of plant gene expression by systemically transported RNA molecules.
    Bioessays. 2001 Dec;23(12):1087-90 PMID: 11746226
  33. The Myriad Plant Responses to Herbivores.
    J Plant Growth Regul. 2000 Jun;19(2):195-216 PMID: 11038228
  34. Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4.
    EMBO J. 2001 Oct 1;20(19):5400-11 PMID: 11574472
  35. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of plant mRNAs in response to insect-derived cues.
    Plant Physiol. 2001 Feb;125(2):701-10 PMID: 11161027
  36. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6531-6 PMID: 9601001
  37. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6523-8 PMID: 10339621
  38. Molecular cloning and functional expression of O-methyltransferases common to isoquinoline alkaloid and phenylpropanoid biosynthesis.
    Plant J. 1999 Feb;17(4):329-39 PMID: 10205892
  39. Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips.
    Plant Mol Biol. 1995 Jun;28(3):473-85 PMID: 7632917
  40. Cloning and molecular characterization of plant aldehyde oxidase.
    J Biol Chem. 1997 Jun 13;272(24):15280-5 PMID: 9182554
  41. De Novo Biosynthesis of Volatiles Induced by Insect Herbivory in Cotton Plants.
    Plant Physiol. 1997 Aug;114(4):1161-1167 PMID: 12223763
  42. Bruchins: insect-derived plant regulators that stimulate neoplasm formation.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):6218-23 PMID: 10811915
  43. Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding.
    Plant Cell. 2000 Aug;12(8):1409-23 PMID: 10948259
  44. Regulation of the Accumulation and Reduction of Nitrate by Nitrogen and Carbon Metabolites in Maize Seedlings.
    Plant Physiol. 1997 Jun;114(2):583-589 PMID: 12223730
  45. Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance.
    J Chem Ecol. 1995 Oct;21(10):1511-30 PMID: 24233680
  46. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate.
    Plant Cell. 2001 Jan;13(1):179-91 PMID: 11158538
  47. Isolation of a cDNA encoding a novel leucine-rich repeat motif from Sorghum bicolor inoculated with fungi.
    Mol Plant Microbe Interact. 1996 Dec;9(9):819-25 PMID: 8969530
  48. Evaluation and optimization of procedures for target labeling and hybridization of cDNA microarrays.
    Mol Vis. 2002 Apr 26;8:130-7 PMID: 12011805
  49. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6553-7 PMID: 10339626
  50. A wound- and systemin-inducible polygalacturonase in tomato leaves.
    Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1756-60 PMID: 9990097
  51. Ethylene production and peroxidase activity in aphid-infested barley.
    J Chem Ecol. 2001 Jan;27(1):53-68 PMID: 11382067
  52. Systemin: a polypeptide signal for plant defensive genes.
    Annu Rev Cell Dev Biol. 1998;14:1-17 PMID: 9891776
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2004-01-00
Epub
2003-00-30
Pages
420-31
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC316321
Subset
IM
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