Convergent responses to stress. Solar ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional responses in field-grown plants of Nicotiana longiflora

Plant Physiology

Volumn 132, Issue 4, 2003, Pages 1755-1767

  Izaguirre, Miriam M ^a   Scopel, Ana L ^a   Baldwin, Ian T ^b   Ballaré, Carlos L ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FATTY ACIDS; GENES; OZONE; PHOTOSYNTHESIS; ULTRAVIOLET RADIATION; UPPER ATMOSPHERE;

STRESSORS;

PLANTS (BOTANY);

EMBRYOPHYTA; EUKARYOTA; INSECTA; MANDUCA SEXTA; NICOTIANA; NICOTIANA LONGIFLORA;

EID: 0041387630     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.103.024323     Document Type: Article

References (68)

1. A.-H.-Mackerness S, Butt PJ, Jordan BR, Thomas B (1996) Amelioration of ultraviolet-B-induced down-regulation of mRNA levels for chloroplast proteins, by high irradiance, is mediated by photosynthesis. J Plant Physiol 148: 100-106.
2. A.-H.-Mackerness S, John CF, Jordan B, Thomas B (2001) Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett 489: 237-242.
3. A.-H.-Mackerness S, Liu LS, Thomas B, Thompson WF, Jordan BR, White MJ (1998) Individual members of the light-harvesting complex II chlorophyll a/b binding protein gene family in pea (Pisum sativum) show differential responses to ultraviolet-B radiation. Physiol Plant 103: 377-384.
4. A.-H.-Mackerness S, Surplus SL, Blake P, John CF, Buchannan-Wollaston V, Jordan BR, Thomas B (1999) Ultraviolet-B-induced stress and changes in gene expression in Arabidopsis thaliana: role of signalling pathways controlled by jasmonlc acid, ethylene and reactive oxygen species. Plant Cell Environ 22: 1413-1423
5. Allen DJ, Nogués S, Baker NR (1998) Ozone depletion and increased UV-B radiation: is there a real threat to photosynthesis? J Exp Bot 49: 1775-1788
6. Baldwin IT, Staszak-Kozinski L, Davidson R (1994) Up in smoke: I. Smoke-derived germination cues for positive annual, Nicotiana attenuata Torr. Ex. Watson. J Chem Ecol 20: 2345-2371
7. Ballaré CL, Barnes PW, Flint SD (1995) Inhibition of hypocotyl elongation by ultraviolet-B radiation in de-etiolating tomato seedlings: I. The photoreceptor. Physiol Plant 93: 584-592
8. Ballaré CL, Scopel A, Mazza C (1999) Effects of solar UV-B radiation on terrestrial ecosystems: case studies from southern South America. In J Rozema, ed, Stratospheric Ozone Depletion: The Effects of Enhanced UV-B Radiation on Terrestrial Ecosystems. Backhuys Publishers, Leiden, The Netherlands, pp 293-311
9. Ballaré CL, Rousseaux MC, Searles PS, Zaller JG, Giordano CV, Robson TM, Caldwell MM, Sala OE, Scopel AL (2001) Impacts of solar ultraviolet-B radiation on terrestrial ecosystems of Tierra del Fuego (southern Argentina): an overview of recent progress. J Photochem Photobiol B Biol 62: 67-77
10. Ballaré CL, Scopel AL, Stapleton AE, Yanovsky MJ (1996) Solar ultraviolet-B radiation affects seedling emergence, DNA integrity, plant morphology, growth rate, and attractiveness to herbivore insects in Datura ferox. Plant Physiol 112: 161-170
11. Beggs C, Wellmann E (1994) Photocontrol of flavonoid biosynthesis. In R Kendrick, G Kronenberg, eds, Photomorphogenesis in Plant. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 733-751
12. Boccalandro HE, Mazza CA, Mazzella MA, Casal JJ, Ballaré CL (2001) Ultraviolet B radiation enhances a phytochrome-B-mediated photomorphogenic response in Arabidopsis. Plant Physiol 126: 780-788
13. Bothwell ML, Sherbot DMJ, Pollock CM (1994) Ecosystem responses to solar ultraviolet-B radiation: influence of trophic-level interactions. Science 265: 97-100
14. Bowler C, Fluhr R (2000) The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci 5: 241-246
15. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
16. Brederode FT, Linthorst HJ, Bol JF (1991) Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol 17: 1117-1125
17. Brosché M, Fant C, Bergkvist SW, Strid H, Svensk A, Olsson O, Strid A (1999) Molecular markers for UV-B stress in plants: alteration of the expression of four classes of genes in Pisum sativum and the formation of high molecular mass RNA adducts. Biochim Biophys Acta 1447: 185-198
18. Brosché M, Schuler MA, Kalbina I, Connor L, Strid A (2002) Gene regulation by low level UV-B radiation: identification by DNA array analysis. Photochem Photobiol Sci 1: 656-664
19. Caldwell MM (1971) Solar UV irradiation and the growth and development of higher plants. In AC Giese, ed, Photophysiology, Vol 6. Academic Press, New York, pp 131-177
20. Caldwell MM, Flint SD (1997) Uses of biological weighting functions and the need of scaling for the ozone reduction problem. Plant Ecol 128: 66-76
21. Conconi A, Smerdon MJ, Howe GA, Ryan CA (1996) The octadecanoid signalling pathway in plants mediates a response to ultraviolet radiation. Nature 383: 826-829
22. Ernst D, Bodemann A, Schmelzer E, Langebartels C, Sandermann H (1996) β-1,3-Glucanase mRNA is locally, but not systematically induced in Nicotiana tabacum L. cv Bel W3 after ozone fumigation. J Plant Physiol 148: 215-221
23. Ernst D, Schraudner M, Langebartels C, Sandermann HJ (1992) Ozone-induced changes of mRNA levels of beta-1,3-glucanase, chitinase and "pathogenesis-related" protein 1b in tobacco plants. Plant Mol Biol 20: 673-682
24. Fiscus EL, Booker FL (1995) Is increased UV-B a threat to crop photosynthesis and productivity? Photosynth Res 43: 81-92
25. + and stimulates gene expression in transgenic parsley cell cultures. Plant J 20: 109-117
26. Gatehouse JA (2002) Plant resistance towards insect herbivores: a dynamic interaction. New Phytol 156: 145-169
27. Green R, Fluhr R (1995) UV-B-induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203-212
28. Halitschke R, Gase C, Hui D, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuate: VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 131: 1894-1902
29. Hermsmeier D, Schittko U, Baldwin IT (2001) 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 125: 683-700
30. Hideg É, Barta C, Kálai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43: 1154-1164
31. Hideg É, Kálai T, Hideg K, Vass I (2000) Do oxidative stress conditions impairing photosynthesis in the light manifest as photoinhibition? Philos Trans R Soc Lond B Biol Sci 355: 1511-1516
32. Hui D, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: V. Microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131: 1877-1893
33. Jongsma MA, Bakker PL, Stiekema WJ (1993) Quantitative determination of serine proteinase inhibitor activity using a radial diffusion assay. Anal Biochem 212: 79-84
34. Jongsma MA, Bakker PL, Visser B, Stiekema WJ (1994) Trypsin inhibitor activity in mature tobacco and tomato plants is mainly induced locally in response to insect attack, wounding and virus infection. Planta 195: 29-35
35. Jordan BR, Chow HJ, Anderson JM (1992) Changes in mRNA levels and polypeptide subunits of ribulose 1:5-bisphosphate carboxylase in response to supplementary ultraviolet-B radiation. Plant Cell Environ 15: 91-98
36. Kalbin G, Hidema J, Brosché M, Kumagai T, Bornman JF, Strid Å (2001) UV-B-induced DNA damage and expression of defence genes under UV-B stress: tissue-specific molecular marker analysis in leaves. Plant Cell Environ 24: 983-990
37. Karban R, Baldwin IT (1997) Induced Responses to Herbivory. Chicago University Press, Chicago
38. Krizek DT, Britz SJ, Mirecki RM (1998) Inhibitory effects of ambient levels of solar UV-A and UV-B radiation on growth of cv. New Red Fire lettuce. Physiol Plant 103: 1-7
39. Malanga G, Puntarulo S (1995) Oxidative responses and antloxidant content in Chlorella vulgaris after exposure to ultraviolet-B radiation. Physiol Plant 94: 672-679
40. Mazza CA, Battista D, Zima A, Szwarcberg-Bracchitta M, Giordano CV, Acevedo A, Scopel AL, Ballare CL (1999a) The effects of solar UV-B radiation on the growth and yield of barley are accompanied by increased DNA damage and antioxidant responses. Plant Cell Environ 22: 61-67
41. Mazza CA, Boccalandro HE, Giordano CV, Battista D, Scopel AL, Ballaré CL (2000) Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops. Plant Physiol 122: 117-125
42. Mazza CA, Izaguirre M, Zavala J, Scopel A, Ballaré C (2002) Insect perception of ambient ultraviolet-B radiation. Ecol Lett 5: 722-726
43. Mazza CA, Zavala J, Scopel AL, Ballaré CL (1999b) Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications. Proc Natl Acad Sci USA 96: 980-985
44. Montoya T, Nomura T, Farrar K, Kaneta T, Yokota T, Bishop GJ (2002) Cloning the tomato Curl3 gene highlights the putative dual role of the leucine-rich repeat receptor kinase tBRI1/SR160 in plant steroid hormone and peptide hormone signaling. Plant Cell 14: 3163-3176
45. Orozco-Cárdenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octade-canoid pathway. Proc Natl Acad Sci USA 96: 6553-6557
46. Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) 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 13: 179-191
47. Pohlon E, Baldwin IT (2001) Artificial diets "capture" the dynamics of jasmonate-induced defenses in plants. Entomol Exp Appl 100: 127-130
48. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B and ozone-induced biochemical changes in an antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110: 125-136
49. Rousseaux MC, Ballaré CL, Scopel AL, Searles PS, Caldwell MM (1998) Solar ultraviolet-B radiation affects plant-insect interactions in a natural ecosystem of Tierra del Fuego (southern Argentina). Oecologia 116: 528-535
50. Rousseaux MC, Scopel AL, Searles PS, Caldwell MM, Sala OE, Ballaré CL (2001) Responses to solar ultraviolet-B radiation in a shrub-dominated natural ecosystem of Tierra del Fuego (southern Argentina). Global Change Biol 7: 467-478
51. Ryan CA (2000) The systemin signaling pathway: differential activation of plant defensive genes. Biochim Biophys Acta 1477: 112-121
52. Sävenstrand H, Brosché M, Strid A (2002) Regulation of gene expression by low levels of ultraviolet-B radiation in Pisum sativum: isolation of novel genes by suppression subtractive hybridisation. Plant Cell Physiol 43: 402-410
53. Schittko U, Hermsmeier D, Baldwin IT (2001) 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 125: 701-710
54. Stratmann J, Scheer J, Ryan CA (2000a) Suramin inhibits initiation of defense signaling by systemin, chitosan, and a β-glucan elicitor in suspension-cultured Lycopersicon peruvianum cells. Proc Natl Acad Sci USA 97: 8862-8867
55. Stratmann J, Stelmach B, Weiler E, Ryan C (2000b) UVB/UVA radiation activates a 48 kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves. Photochem Photobiol 71: 116-123
56. Strid A, Chow W, Anderson JM (1996) Changes in the relaxation of electronic shifts of photosynthetic pigments and in the levels of mRNA transcripts in leaves of Pisum Sativum as a result of exposure to supplementary UV-B radiation: the dependency on the intensity of the photo-synthetically active radiation. Plant Cell Physiol 37: 61-67
57. Surplus SL, Jordan BR, Murphy AM, Carr JP, Thomas B, A.-H.-Mackerness S (1998) Ultraviolet-B-induced responses in Arabidopsis thaliana: role of salicylic acid and reactive oxygen species in the regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins. Plant Cell Environ 21: 685-694
58. Thalmair M, Bauw G, Thiel S, Döhring T, Langebartels C, Sandermann H (1996) Ozone and ultraviolet-B effects on the defense-related proteins β-1,3-glucanase and chitinase in tobacco. J Plant Physiol 148: 222-228
59. van Dam NM, Horn M, Mares M, Baldwin IT (2001) Ontogeny constrains the systemic protease inhibitor response in Nicotiana attenuata. J Chem Ecol 27: 547-568
60. Voelckel C, Baldwin IT (2003) Detecting herbivore-specific transcriptional responses in plants with multiple DDRT-PCR and subtractive library procedures. Physiol Plant 118: 240-252
61. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19: 195-216
62. Weber H (2002) Fatty acid-derived signals in plants Trends Plant Sci 7: 217-224
63. Willekens H, Camp WV, Montagu MV, Inzé D, Langebartels C, Sandermann JH (1994) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol 106: 1007-1014
64. Yalamanchili RD, Stratmann JW (2002) Ultraviolet-B activates components of the systemin signaling pathway in Lycopersicon peruvianum suspension-cultured cells. J Biol Chem 277: 28424-28430
65. Yalpani N, Enyedi AJ, Leon J, Raskin I (1994) UV light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193: 372-376
66. Yang T, Poovaiah BW (2002) A calmodulin-binding/CGCG Box DNA-binding protein family involved in multiple signaling pathways in plants. J Biol Chem 277: 45049-45058
67. Zavala J, Scopel A, Ballaré C (2001) Effects of solar UV-B radiation on soybean crops: Impact on leaf herbivory by Anticarsia gemmatalis. Plant Ecol 156: 121-130
68. Ziegler J, Keinanen M, Baldwin IT (2001) Herbivore-induced allene oxide synthase transcripts and jasmonic acid in Nicotiana attenuata. Phytochemistry 58: 729-738.