DICER-like Proteins and Their Role in Plant-herbivore Interactions in Nicotiana attenuata

Journal of Integrative Plant Biology

Volumn 54, Issue 3, 2012, Pages 189-206

  Ahmadovich Bozorov, Tohir ^a   Prakash Pandey, Shree ^a,b   Dinh, Son Truong ^a   Kim, Sang Gyu ^a   Heinrich, Maria ^a   Gase, Klaus ^a   Baldwin, Ian T ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b BIDHAN CHANDRA KRISHI VISWAVIDYALAYA   (India)

Author keywords

Anti herbivore defense; DICER like proteins; Manduca sexta; Nicotiana attenuata; Phytohormone signaling

Indexed keywords

PHYTOHORMONE; RIBONUCLEASE III; TRYPSIN INHIBITOR; VEGETABLE PROTEIN;

GENE EXPRESSION; HERB; HERBIVORE; METABOLITE; PROTEIN; RNA; SHRUB;

ANIMAL; ARTICLE; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; HERBIVORY; HOST PARASITE INTERACTION; LARVA; LEPIDOPTERA; METABOLISM; MUTATION; PARASITOLOGY; PHENOTYPE; PHYSIOLOGY; PLANT GENE; TOBACCO;

ANIMALS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; HERBIVORY; HOST-PARASITE INTERACTIONS; LARVA; MANDUCA; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PLANT GROWTH REGULATORS; PLANT PROTEINS; RIBONUCLEASE III; TOBACCO; TRANSCRIPTION, GENETIC; TRYPSIN INHIBITORS;

MANDUCA SEXTA; NICOTIANA ATTENUATA;

EID: 84863338053     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2012.01104.x     Document Type: Article

References (67)

1. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouche N, Gasciolli V, Vaucheret H (2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16, 927-932.
2. Bartel DP (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
3. Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. USA 92, 8675-8679.
4. Biesgen C, Weiler EW (1999) Structure and regulation of OPR1 and OPR2, two closely related genes encoding 12-oxophytodienoic acid-10, 11-reductases from Arabidopsis thaliana. Planta 208, 155-165.
5. Bouche N, Lauressergues D, Gasciolli V, Vaucheret H (2006) An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25, 3347-3356.
6. Bubner B, Gase K, Baldwin IT (2004) Two-fold differences are the detection limit for determining transgene copy numbers in plants by real-time PCR. BMC Biotechnol. 4, 14.
7. Chen M, Ni M (2006) RED AND FAR-RED INSENSITIVE 2, a RING-domain zinc finger protein, mediates phytochrome-controlled seedling deetiolation responses. Plant Physiol. 140, 457-465.
8. Chen X (2009) Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25, 21-44.
9. Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J. 23, 431-440.
10. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150, 1576-1586.
11. Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F, Alioua A, Himber C, Voinnet O (2010a) An endogenous, systemic RNAi pathway in plants. EMBO J. 29, 1699-1712.
12. Dunoyer P, Himber C, Voinnet O (2005) DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37, 1356-1360.
13. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2010b) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912-916.
14. Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N, Brempelis KJ, Carrington JC (2010) Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell 22, 481-496.
15. Gasciolli V, Mallory AC, Bartel DP, Vaucheret H (2005) Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494-1500.
16. Gase K, Weinhold A, Bozorov T, Schuck S, Baldwin IT (2011) Efficient screening of transgenic plant lines for ecological research. Mol. Ecol. Resour. 11, 890-902.
17. Giri AP, Wunsche H, Mitra S, Zavala JA, Muck A, Svatos A, Baldwin IT (2006) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VII. Changes in the plant's proteome. Plant Physiol. 142, 1621-1641.
18. Heinrich M, Baldwin IT, Wu J (2011) Three MAPK kinases, MEK1, SIPKK and NPK2, are not involved in activation of SIPK after wounding and herbivore feeding but important for accumulation of trypsin proteinase inhibitors. Plant Mol. Rep. DOI:
19. Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J. 36, 794-807.
20. Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) 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. 125, 711-717.
21. Hiraguri A, Itoh R, Kondo N, Nomura Y, Aizawa D, Murai Y, Koiwa H, Seki M, Shinozaki K, Fukuhara T (2005) Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57, 173-188.
22. Jongsma MA, Bakker PL, Stiekema WJ (1993) Quantitative determination of serine proteinase inhibitor activity using a radial diffusion assay. Anal. Biochem. 212, 79-84.
23. Kallenbach M, Alagna F, Baldwin IT, Bonaventure G (2010) Nicotiana attenuata SIPK, WIPK, NPR1, and fatty acid-amino acid conjugates participate in the induction of jasmonic acid biosynthesis by affecting early enzymatic steps in the pathway. Plant Physiol. 152, 96-106.
24. Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18, 3303-3320.
25. Kaur H, Heinzel N, Schottner M, Baldwin IT, Galis I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol. 152, 1731-1747.
26. Kehr J, Buhtz A (2008) Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59, 85-92.
27. Keinanen M, Oldham NJ, Baldwin IT (2001) Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J. Agric. Food Chem. 49, 3553-3558.
28. Kessler A, Baldwin IT (2004) 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. 38, 639-649.
29. Khraiwesh B, Arif MA, Seumel GI, Ossowski S, Weigel D, Reski R, Frank W (2010) Transcriptional control of gene expression by microRNAs. Cell 140, 111-122.
30. Kistner C, Matamoros M (2005) RNA isolation using phase extraction and LiCl precipitation. In: AJ Marquez, ed. Lotus japonicus Handbook. Springer Verlag, Dordrecht, The Netherlands, pp. 123-124.
31. Krügel T, Lim M, Gase K, Halitschke R, Baldwin IT (2002) Agrobacterium-mediated transformation of Nicotiana attenuata, a model ecological expression system. Chemoecology 12, 177-183.
32. La Camera S, Balague C, Gobel C, Geoffroy P, Legrand M, Feussner I, Roby D, Heitz T (2009) The Arabidopsis patatin-like protein 2 (PLP2) plays an essential role in cell death execution and differentially affects biosynthesis of oxylipins and resistance to pathogens. Mol. Plant Microbe. Interact. 22, 469-481.
33. Lackey E, Ng DW, Chen ZJ (2010) RNAi-mediated down-regulation of DCL1 and AGO1 induces developmental changes in resynthesized Arabidopsis allotetraploids. New Phytol. 186, 207-215.
34. Liu Q, Feng Y, Zhu Z (2009a) Dicer-like (DCL) proteins in plants. Funct. Integr. Genomics 9, 277-286.
35. Liu Y, Gao Q, Wu B, Ai T, Guo X (2009b) NgRDR1, an RNA-dependent RNA polymerase isolated from Nicotiana glutinosa, was involved in biotic and abiotic stresses. Plant Physiol. Biochem. 47, 359-368.
36. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22, 1104-1117.
37. McCloud ES, Baldwin IT(1997). Herbivory and caterpillar regurgitants amplify the wound-induced increases in jasmonic acid but not nicotine in Nicotiana sylvestris. Planta 203, 430-435.
38. Meldau S, Wu J, Baldwin IT (2009) Silencing two herbivory-activated MAP kinases, SIPK and WIPK, does not increase Nicotiana attenuata's susceptibility to herbivores in the glasshouse and in nature. New Phytol. 181, 161-173.
39. Moreno JE, Tao Y, Chory J, Ballare CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc. Natl. Acad. Sci. USA 106, 4935-4940.
40. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
41. Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev. 24, 2678-2692.
42. Pandey SP, Baldwin IT (2007) RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. Plant J. 50, 40-53.
43. Pandey SP, Gaquerel E, Gase K, Baldwin IT (2008a) RNA-directed RNA polymerase3 from Nicotiana attenuata is required for competitive growth in natural environments. Plant Physiol. 147, 1212-1224.
44. Pandey SP, Shahi P, Gase K, Baldwin IT (2008b) Herbivory-induced changes in the small-RNA transcriptome and phytohormone signaling in Nicotiana attenuata. Proc. Natl. Acad. Sci. USA 105, 4559-4564.
45. Papp I, Mette MF, Aufsatz W, Daxinger L, Schauer SE, Ray A, van der Winden J, Matzke M, Matzke AJ (2003) Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol. 132, 1382-1390.
46. Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J. 31, 1-12.
47. Paschold A, Halitschke R, Baldwin IT (2007) Co(i)-ordinating defenses: NaCOI1 mediates herbivore- induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J. 51, 79-91.
48. Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett. 581, 3592-3597.
49. Qu F, Ye X, Morris TJ (2008) Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc. Natl. Acad. Sci. USA 105, 14732-14737.
50. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407-3425.
51. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev. 16, 1616-1626.
52. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485-510.
53. Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol. 146, 845-851.
54. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16, 2117-2127.
55. Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for plant protease inhibitors. Ecol. Lett. 10, 499-511.
56. Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine's defensive function in nature. PLoS Biol. 2, E217.
57. Sunkar R, Zhu J (2007) Micro RNAs and short-interfering RNAs in plants. J. Integr. Plant Biol. 49, 817-826.
58. Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, Shinozaki K, Paszkowski J (2002) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J. 21, 6483-6493.
59. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev. 20, 759-771.
60. Voelckel C, Baldwin IT (2004) 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. 38, 650-663.
61. Wang L, Allmann S, Wu J, Baldwin IT (2008) Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-silenced plants reveal that jasmonic acid and jasmonic acid-amino acid conjugates play different roles in herbivore resistance of Nicotiana attenuata. Plant Physiol. 146, 904-915.
62. Wang L, Halitschke R, Kang JH, Berg A, Harnisch F, Baldwin IT (2007) Independently silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine. Planta 226, 159-167.
63. Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19, 1096-1122.
64. Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102, 12984-12989.
65. Xie Z, Johansen LK, Gustafson AM, Kasschau KD, Lellis AD, Zilberman D, Jacobsen SE, Carrington JC (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104.
66. Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y (2004) Plant MAPK phosphatase interacts with calmodulins. J. Biol. Chem. 279, 928-936.
67. Zavala JA, Giri AP, Jongsma MA, Baldwin IT (2008) Digestive duet: Midgut digestive proteinases of Manduca sexta ingesting Nicotiana attenuata with manipulated trypsin proteinase inhibitor expression. PLoS One 3, e2008.