Poplar defense against insects: Genome analysis, full-length cDNA cloning, and transcriptome and protein analysis of the poplar Kunitz-type protease inhibitor family

New Phytologist

Volumn 184, Issue 4, 2009, Pages 865-884

  Philippe, Ryan N ^a,b   Ralph, Steven G ^c   Külheim, Carsten ^a   Jancsik, Sharon I ^a   Bohlmann, Jörg ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Choristoneura rosaceana (oblique banded leaf roller); Malacosoma disstria (forest tent caterpillar); Plant defense; Plant herbivore interaction; Populus trichocarpa (cottonwood); Tree genomics

Indexed keywords

COMPLEMENTARY DNA; PEPTIDE; PROTEINASE INHIBITOR; VEGETABLE PROTEIN;

DECIDUOUS TREE; DNA; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; GENOMICS; INHIBITOR; PHYLOGENY; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; PLANT-INSECT INTERACTION; POLYMERASE CHAIN REACTION; PROTEIN; PROTEOMICS; REAL TIME;

ANIMAL; ARTICLE; ASPEN; EXPRESSED SEQUENCE TAG; GENE DUPLICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; LEPIDOPTERA; METABOLISM; MICROARRAY ANALYSIS; MOLECULAR CLONING; MULTIGENE FAMILY; PHYLOGENY; PLANT DISEASE; PLANT GENE; PLANT GENOME; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; EXPRESSED SEQUENCE TAGS; GENE DUPLICATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENES, PLANT; GENOME, PLANT; LEPIDOPTERA; MICROARRAY ANALYSIS; MULTIGENE FAMILY; PEPTIDES; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; POPULUS; PROTEASE INHIBITORS; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

CHORISTONEURA ROSACEANA; HEXAPODA; MALACOSOMA DISSTRIA; POPULUS; POPULUS TRICHOCARPA; TORTRICIDAE;

EID: 70449363862     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.03028.x     Document Type: Article

References (59)

1. Araújo APU, Hansen D, Vieira DF, de Oliveira C, Santana LA, Beltramini LM, Sampaio CAM, Sampaio MU, Oliva MLV. 2005. Kunitz-type Bauhinia bauhinioides inhibitors devoid of disulfide bridges: isolation of the cDNAs, heterologous expression and structural studies. Biological Chemistry 386 : 561 568.
2. Bode W, Huber R. 1992. Natural protein proteinase inhibitors and their interaction with proteinases. European Journal of Biochemistry 204 : 433 451.
3. Bolter CJ, Jongsma MA. 1995. Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. Journal of Insect Physiology 41 : 1071 1078.
4. Bown DP, Wilkinson HS, Gatehouse JA. 1997. Differentially regulated inhibitor-sensitive and insensitive protease genes from the phytophagous insect pest, Helicoverpa armigera, are members of complex multigene families. Insect Biochemistry and Molecular Biology 27 : 625 638.
5. Bown DP, Wilkinson HS, Gatehouse JA. 2004. Regulation of expression of genes encoding digestive proteases in the gut of a polyphagous lepidopteran larva in response to dietary protease inhibitors. Physiological Entomology 29 : 278 290.
6. Bradshaw HD, Hollick JB, Parsons TJ, Clarke HR, Gordon MP. 1990. Systemically wound-responsive genes in poplar trees encode proteins similar to sweet potato sporamins and legume Kunitz trypsin inhibitors. Plant Molecular Biology 14 : 51 59.
7. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC et al. 2001. Minimum information about a microarray experiment (MIAME) - toward standards for microarray data. Nature Genetics 29 : 365 371.
8. Broadway RM. 1995. Are insects resistant to plant proteinase inhibitors? Journal of Insect Physiology 41 : 107 116.
9. Broadway RM. 1997. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. Journal of Insect Physiology 43 : 855 874.
10. Broadway RM, Duffey SS. 1986. Plant proteinase inhibitors: mechanism of action and effect on the growth and digestive physiology of larval Heliothis zea and Spodoptera exigua. Journal of Insect Physiology 32 : 827 833.
11. Cavalcanti MDSM, Oliva MLV, Fritz H, Jochum M, Mentele R, Sampaio M, Coelho LCBB, Batista IFC, Sampaio CAM. 2002. Characterization of a Kunitz trypsin inhibitor with one disulfide bridge purified from Swartzia pickellii. Biochemical and Biophysical Research Communications 291 : 635 639.
12. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA. 2005. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proceedings of the National Academy of Sciences, USA 102 : 19237 19242.
13. Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA. 2007. Stability of plant defense proteins in the gut of insect herbivores. Plant Physiology 143 : 1954 1967.
14. Christopher ME, Miranda M, Major IT, Constabel CP. 2004. Gene expression profiling of systemically wound-induced defenses in hybrid poplar. Planta 219 : 936 947.
15. Dibella FP, Liener IE. 1969. Soybean trypsin inhibitor - cleavage and identification of a disulfide bridge not essential for activity. Journal of Biological Chemistry 244 : 2824 2829.
16. Downing WL, Mauxion F, Fauvarque MO, Reviron MP, Devienne D, Vartanian N, Giraudat J. 1992. A Brassica napus transcript encoding a protein related to the Kunitz protease inhibitor family accumulates upon water-stress in leaves, not in seeds. Plant Journal 2 : 685 693.
17. Felsenstein J. 1993. PHYLIP (Phylogeny Inference Package). Version 3.5c, Washington, WA, USA : University of Washington, Seattle.
18. Garcia VA, Freire MDGM, Novello JC, Marangoni S, Macedo MLR. 2004. Trypsin inhibitor from Poecilanthe parviflora seeds: purification, characterization, and activity against pest proteases. Protein Journal 23 : 343 350.
19. Gascuel O. 1997. BIONJ: An improved version of the NJ algorithm based on a simple model of sequence data. Molecular Biology and Evolution 14 : 685 695.
20. Gatehouse LN, Shannon AL, Burgess EPJ, Christeller JT. 1997. Characterization of major midgut proteinase cDNAs from Helicoverpa armigera larvae and changes in gene expression in response to four proteinase inhibitors in the diet. Insect Biochemistry and Molecular Biology 27 : 929 944.
21. Green TR, Ryan CA. 1973. Wound-induced proteinase inhibitor in tomato leaves - some effects of light and temperature on wound response. Plant Physiology 51 : 19 21.
22. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52 : 696 704.
23. Haruta M, Major IT, Christopher ME, Patton JJ, Constabel CP. 2001. A Kunitz trypsin inhibitor gene family from trembling aspen (Populus tremuloides Michx.): cloning, functional expression, and induction by wounding and herbivory. Plant Molecular Biology 46 : 347 359.
24. Huang X, Madan A. 1999. CAP3: a DNA sequence assembly program. Genome Research 9 : 868 877.
25. Ingvarsson PK. 2005. Molecular population genetics of herbivore-induced protease inhibitor genes in European Aspen (Populus tremula L., Salicaceae). Molecular Biology and Evolution 22 : 1802 1812.
26. Jones DT, Taylor WR, Thornton JM. 1992. The rapid enumeration of mutation data matrices from protein sequences. Computer Applications in the Biosciences 8 : 275 282.
27. Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ. 1995. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of the National Academy of Sciences, USA 92 : 8041 8045.
28. Kolosova N, Miller B, Ralph S, Ellis BE, Douglas C, Ritland K, Bohlmann J. 2004. Isolation of high-quality RNA from gymnosperm and angiosperm trees. BioTechniques 36 : 821 824.
29. Kumar M, Thammannagowda S, Bulone V, Chiang V, Han KH, Joshi CP, Mansfield SD, Mellerowicz E, Sundberg B, Teeri T et al. 2009. An update on the nomenclature for the cellulose synthase genes in Populus. Trends in Plant Science 14 : 248 254.
30. Kunitz M. 1945. Crystallization of a trypsin inhibitor from soybean. Science 101 : 668 669.
31. Larson PR, Isebrands JG. 1971. The plastochron index as applied to developmental studies of cottonwood. Canadian Journal of Forest Research 1 : 1 11.
32. Lawrence SD, Novak NG. 2001. A rapid method for the production and characterization of recombinant insecticidal proteins in plants. Molecular Breeding 8 : 139 146.
33. Lawrence SD, Novak NG, Blackburn MB. 2007. Inhibition of proteinase inhibitor transcripts by Leptinotarsa decemlineata regurgitant in Solanum lycopersicum. Journal of Chemical Ecology 33 : 1041 1048.
34. Lu S, Sun Y-H, Chiang VL. 2008. Stress-responsive microRNAs in Populus. Plant Journal 55 : 131 151.
35. Macedo MLR, Freire MDGM, Martins LTDM, Martinez DST, Gomes VM, Smolka MB, Toyama MH, Marangoni S, Coelho LCBB. 2004. Novel protein from Labramia bojeri A. DC. seeds homologue to Kunitz-type trypsin inhibitor with lectin-like properties. Journal of Agricultural Food Chemistry 52 : 7548 7554.
36. Macedo MLR, Garcia VA, Freire MDGM, Richardson M. 2007. Characterization of a Kunitz trypsin inhibitor with a single disulfide bridge from seeds of Inga laurina (SW.) Willd. Phytochemistry 68 : 1104 1111.
37. Major IT, Constabel CP. 2006. Molecular analysis of poplar defense against herbivory: comparison of wound- and insect elicitor-induced gene expression. New Phytologist 172 : 617 635.
38. Major IT, Constabel CP. 2008. Functional analysis of the Kunitz trypsin inhibitor family in poplar reveals biochemical diversity and multiplicity in defense against herbivores. Plant Physiology 146 : 888 903.
39. Mazumdar-Leighton S, Broadway RM. 2001a. Transcriptional induction of diverse midgut trypsins in larval Agrotis ipsilon and Helicoverpa zea feeding on the soybean trypsin inhibitor. Insect Biochemistry and Molecular Biology 31 : 645 657. (Pubitemid 32373911)
40. Mazumdar-Leighton S, Broadway RM. 2001b. Identification of six chymotrypsin cDNAs from larval midguts of Helicoverpa zea and Agrotis ipsilon feeding on the soybean (Kunitz) trypsin inhibitor. Insect Biochemistry and Molecular Biology 31 : 633 644. (Pubitemid 32373910)
41. de Meester P, Brick P, Lloyd LF, Blow DM, Onesti S. 1998. Structure of the Kunitz-type soybean trypsin inhibitor (STI): implication for the interactions between members of the STI family and tissue-plasminogen activator. Acta Crystallographica Section D - Biological Crystallography 54 : 589 597.
42. Miranda M, Christopher ME, Constabel CP. 2004. The variable nature of herbivore defense: evidence for rapidly diverging Kunitz trypsin inhibitor genes in Populus. In : Cronk QC, Whitton J, Ree RH, Taylor IEP, eds. Proceedings of an international workshop on plant adaptation: molecular biology and ecology: 11-13 December 2002, Vancouver. Ottawa, Canada : NRC Research Press, 153 158.
43. Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP. 2007. The transcriptional response of hybrid poplar (Populus trichocarpa × deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Molecular Plant-Microbe Interactions 20 : 816 831.
44. Morgenstern B, Frech K, Dress A, Werner T. 1998. DIALIGN: Finding local similarities by multiple sequence alignment. Bioinformatics 14 : 290 294.
45. Page RDM. 1996. TreeView: an application to display phylogenetics trees on personal computers. Computer Applications in the Biosciences 12 : 357 358.
46. Pandey SP, Shahi P, Gase K, Baldwin IT. 2008. Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proceedings of the National Academy of Sciences, USA 105 : 4559 4564.
47. Philippe RN, Bohlmann J. 2007. Poplar defense against insect herbivores. Canadian Journal of Botany 85 : 1111 1126.
48. Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N, Philippe RN, Aeschliman D, White R, Huber D et al. 2006. Genomics of hybrid poplar (Populus trichocarpa × deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Molecular Ecology 15 : 1275 1297.
49. Ralph SG, Chun HJE, Cooper D, Kirkpatrick R, Kolosova N, Gunter L, Tuskan GA, Douglas CJ, Holt RA, Jones SJM et al. 2008. Analysis of 4,664 high-quality sequence-finished poplar full-length cDNA clones and their utility for the discovery of genes responding to insect feeding. BMC Genomics 9 : 57.
50. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339 : 62 66.
51. Ravichandran S, Sen U, Chakrabarti C, Dattagupta JK. 1999. Cryocrystallography of a Kunitz-type serine protease inhibitor: the 90 K structure of winged bean chymotrypsin inhibitor (WCI) at 2.13 angstrom resolution. Acta Crystallographica Section D - Biological Crystallography 55 : 1814 1821.
52. Richardson M. 1977. Proteinase-inhibitors of plants and microorganisms. Phytochemistry 16 : 159 169.
53. Ryan CA. 1973. Proteolytic enzymes and their inhibitors in plants. Annual Review of Plant Physiology and Plant Molecular Biology 24 : 173 196.
54. Schittko U, Hermsmeier D, Baldwin IT. 2001. Molecular interaction 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 Physiology 125 : 701 710. (Pubitemid 32169877)
55. Song HK, Suh SW. 1998. Kunitz-type soybean trypsin inhibitor revisited: refined structure of its complex with porcine trypsin reveals an insight into the interaction between a homologous inhibitor from Erythrina caffra and tissue-type plasminogen activator. Journal of Molecular Biology 275 : 347 363.
56. Talyzina NM, Ingvarsson PK. 2006. Molecular evolution of a small gene family of wound inducible Kunitz trypsin inhibitors in Populus. Journal of Molecular Evolution 63 : 108 119.
57. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al. 2006. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313 : 1596 1604.
58. Volpicella M, Ceci LR, Cordewener J, America T, Gallerani R, Bode W, Jongsma MA, Beekwilder J. 2003. Properties of purified gut trypsin from Helicoverpa zea, adapted to proteinase inhibitors. European Journal of Biochemistry 270 : 10 19.
59. Wang J, Constabel CP. 2004. Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220 : 87 96.