Interactions between metal ion toxicity and defences against biotic stress: Glucosinolates and benzoxazinoids as case studies

Forest Snow and Landscape Research

Volumn 80, Issue 2, 2006, Pages 149-160

  Poschenrieder, Charlotte ^a   Tolrà, Roser ^a   Barceló, Juan ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Biotic stress; Chemical defence; Heavy metal toxicity; Herbivores; Resistance; Signalling

Indexed keywords

ANTIHERBIVORE DEFENSE; CHEMICAL DEFENSE; ENVIRONMENTAL STRESS; HEAVY METAL; TOXICITY;

THLASPI; THLASPI CAERULESCENS; ZEA MAYS;

EID: 33749424919     PISSN: 14245108     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (74)

1. ASSUNÇÃO, A.G.L.; SCHAT, H.; AARTS, M.G.M., 2003: Thlaspi caerulescens, an attractive model species to study heavy metal hyperaccumulation in plants. New Phytol. 159: 351-360.
2. BAK, S.; TAX, F.E., FELDMANN, K.A., GALBRAIT, D.W.; FEYEREISEN, R., 2001: CYP83B1, a cytochrome P 450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13: 101-111.
3. BARCELÓ, J.; POSCHENRIEDER, C. 2002: Fast root growth responses, root exudates, and internal detoxification as clues to the mechansims of aluminium toxicity and resistance: a review. Environ. Exp. Bot. 48: 75-92.
4. BEHMER, ST.; LLOYD, C.M.; RAUBENHEIMER, D.; STEWART-CLARK, J.; KNIGHT, J.; LEIGHTON, R.S.; HARPER, F.A.; SMITH, J.A.C., 2005: Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores. Funct. Ecol. 19: 55-66.
5. BOLLER, T., 1995: Chemoperception of microbial signals in plant cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46: 189-214.
6. BOYD, R.S.; MARTENS, S.N., 1992: The raison d'être for metal hyperaccumulation in plants. In: BAKER, A.J.M., PROCTOR, J.; REEVES, R.D. (eds) The Vegetation of Ultramafic (Serpentine) Soils. Andover, UK, Intercept. 279-289.
7. BOYD, R.S.; MARTENS, S.N., 1998: Nickel hyperaccumulation by Thlaspi montanum var. montanum (Brassicaceae) a constitutive trait. Am. J. Bot. 85: 259-265.
8. BOYD, R.S.; DAVIS, M,A.; WALL, M.A.; BALKWILL, K., 2002. Nickel defends the South African nickel hyperaccumulator Senecio coronatus (Asteraceae) against Helix aspersa (Mollusca: Pulmonidae). Chemoecology 12: 91-97.
9. CELENZA, J.L.; QUIEL, J.A.; SMOLEN, G.A.; MERRIKH, H.; SILVESTRO, A.R.; NORMANLY, J.; BENDER, J., 2005: The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol. 137: 253-262.
10. CHAPPLE, C., 1998: Molecular-genetic analysis of plant cytochrome P450-dependent monooxygenases. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 311-343.
11. COBBETT, L.S., 2000: Phytochelatin biosynthesis and function in heavy metal detoxification. Curr. Opin. Plant Biol. 3: 211-216.
12. COOLONG, T.W.; RANDLE, W.M.; TOLER, H.D., 2004: Zinc availability in hydroponic culture influences glucosinolate concentrations in Brassica rapa. Hortscience 39: 84-86.
13. DE KNECHT, J.A.; KOEVOETS, P.L.M.; VERKLEIJ, J.A.C.; ERNST, W.H.O., 1992: Evidence against a role for phytochelatins in naturally selected increased cadmium tolerance in Silene vulgaris (Moench) Garcke. New Phytol. 122: 681-688.
14. 2+ homeostasis. Plant Physiol. 136: 3712-3723.
15. ERNST, W.H.O.; VERKLEIJ, J.A.C.; SCHAT, H., 1992: Metal tolerance in plants. Acta Bot. Neerl. 41: 229-248.
16. FARMER, E.E.; ALMÉROS, E.; KRISHNAMURTHY, V., 2003: Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant Biol. 6: 372-378.
17. FLOR, H.H., 1971: Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9: 275-296.
18. FREEMAN, J.L.; GARCÍA, D.; KIM, D.G.; HOPF, A.; SALT, D.E., 2005: Constitutively elevated salicylic acid signals glutathione-mediated nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Physiol. 137: 1082-1091.
19. FREY, M.; CHOMET, P.; GLAWISCHNIG, E.; STETTNER, C.; GRÜN, S.; WINKLMAIR, A.; EISENREICH, W.; BACHER, A.; MEELEY, R.; BRIGGS, S.; SIMCOX, K.; GIERL, A., 1997: Analysis of a Chemical Plant Defense Mechanism in Grasses. Science 277: 696-699.
20. GLOMBITZA, S.; DUBUIS, P.H.; THULKE, O.; WELZL, G.; BOVET, L.; GOTZ, M.; AFFENZELLER, M.; GEIST, B.; HEHN, A.; ASNAGHI, C.; ERNST, D.; SEIDLITZ, H.K.; GUNDLACH, H.; MAYER, K.F.; MARTINOIA, E.; WERCK-REICHHART, D.; MAUCH, F.; SCHAFFNER, A.R., 2004: Crosstalk and differential response to abiotic and biotic stressors reflected at the transcriptional level of effector genes from secondary metabolism. Plant Mol. Biol. 54: 817-835.
21. GÓMEZ-GÓMEZ, L.; BOLLER, T., 2002: Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7: 251-256.
22. GRATAO, P.L.; POLLE, A.; LEA, P.J.; ACEVEDO, R.A., 2005: Making the life of heavy metal stressed plants a little easier. Funct. Plant Biol. 32: 487-494.
23. HALL, J.L.; WILLIAMS, L.E., 2003: Transition metal transporters in plants. J. Exp. Bot. 54: 2601-2613.
24. HAMMOND, J.P.; BOWEN, H.C.; WHITE, P.J.; MILLS, V., PYKE, K.A., BAKER, A.J.M., WHITING, S.N.; MAY, S.T.; BROADLEY, M.R., 2006: A comparison of the Thlaspi caerulescens and Thlaspi arvense shoot transcriptomes. New Phytol. 170: 239-260.
25. HANSON, B.; GARRIFULLINA, G.F., LINDBLOM, S.D.; WANGELINE, A.; ACKLEY, A., KRAMER, K.; NORTON, A.P.; LAWRENCE, C.B., PILON-SMITS, E.A.H., 2003: Selenium accumulation protects Brassica juncea from invertebrate herbivory and fungal infection. New Phytol. 159: 461-469.
26. HE, Z-H.; HE, D.; KOHORN, B.D., 1998: Requirement of the induced expression of cell wall associated receptor kinase for survival during the pathogen response. Plant J. 14: 55-63.
27. HEATH, M., 2000: Nonhost resistance and nonspecific plant defenses. Curr. Opin. Plant Biol. 3: 315-319.
28. HUITSON, S.B.; MACNAIR, M.R., 2003: Does zinc protect the zinc hyperaccumulator Arabidopsis halleri from herbivory by snails? New Phytol. 159: 453-159.
29. - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. U.S.A. 94: 4800-4805.
30. JHEE, E.M.; DANDRIDGE, K.; CHRYSTY, JR, A.M., POLLARD, A.J., 1999: Selective herbivory on low-zinc phenotypes of Thlaspi caerulescens (Brassicaceae). Chemoecology 9: 93-95.
31. JHEE, E.M.; BOYD, R.S.; EUBANKS, M.D.; DAVIS, A.M., 2005: Nickel hyperaccumulation by Streptanthus polygaloides protects against the folivore Pluttella xylostella (Lepidoptera: Plutellidae). Plant Ecol. 183: 91-104.
32. JIANG, R.F.; MA, D.Y.; ZHAO, F.J.; MCGRATH, S.P., 2005: Cadmium hyperaccumulation protects Thlaspi caerulescens from leaf feeding damage by thrips (Frankliniella occidentalis). New Phytol. 167: 805-813.
33. JONAK, C.; OKRESZ, L., BOGRE, L., HIRT, H., 2002: Complexity, cross talk and integration of plant MAP kinase signalling. Curr. Opin. Plant Biol. 5: 415-424.
34. JONAK, C.; NAKAGAMI, H.; HIRT, H., 2004: Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol. 136: 3276-3283.
35. KESSLER, A.; BALDWIN, I.T., 2002: Plant responses to insect herbivory: The emerging molecular analysis. Annu. Rev. Plant Biol. 53: 299-328.
36. KIDD, P.S.; LLUGANY, M.; POSCHENRIEDER, C.; GUNSÉ, B., BARCELÓ, J., 2001: The role of root exudates in aluminium resistance and silicon-induced amelioration of aluminium toxicity in three varieties of maize (Zea mays L.). J. Exp. Bot. 52: 1339-1352.
37. KOBAE, Y.; UEMURA, T.; SATO, M.H., OHNISHI, M.; MIMURA, T., NAKAGAWA, T.; MAESHIA, M., 2004: Zinc transporter in Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol. 45: 1749-1758.
38. KOCHIAN, L.V.; PENCE, N.S.; LETHAM, D.L.D.; PIÑEROS, M.A.; MAGAKHAES, J.V., HOEKENGA, D.A.; GARVIN, D.F., 2002: Mechanisms of metal resistance in plants: aluminum and heavy metals. Plant Soil 247: 109-119.
39. LAHAYE, T. 2004: Illuminating the molecular basis of gene-for-gene resistance; Arabidopsis thaliana PRS1-R and its interaction with Ralstonia solancearum popP2. Trends Plant Sci. 9: 1-4.
40. LALOI, C.; MESTRES-ORTEGA, D.; MARCO, Y., MEYER, Y.; REICHHELD, J.P., 2004a: The Arabidopsis thioredoxin h 5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitors. Plant Physiol. 134: 1006-1016.
41. LALOI, C.; APEL, K.; DANON, A., 2004b: Relative oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7: 323-328.
42. LAMBDON, P.W.; HASSALL, M.; BOAR, R.R.; MITHEN, R., 2003: Asynchrony in the nitrogen glucosinolate leaf-age profiles of Brassica: is this a defensive strategy against generalist herbivores? Agric. Ecosyst. Environ. 97: 205-214.
43. MAGIDIN, M.; PITTMAN, J.K.; HIRSCHI, K., BARTEL, B., 2003: ILR2, a novel gene regulating IAA conjugate sensitivity and metal transport in Arabidopsis thaliana. Plant J. 35: 523-534.
44. MARTENS, S.N.; BOYD, R.S., 2002: The defensive role of nickel hyperaccumulation in plants: a field experiment. Am. J. Bot. 89: 998-1003.
45. MATHYS, W., 1977: Role of malate, oxalate, and mustard oil glucosides in evolution of zinc resistance in herbage plants. Physiol. Plant. 40: 130-136.
46. MITTLER, R.; VANDERAUWERA, S.; GOLLERY, M., VAN BREUSEGEM, F., 2004: Reactive oxygen gene network of plants. Trends Plant Sci. 9: 490-498.
47. NAKAGAMI, H.; PITZSCHKE, A.; HIRT, H., 2005: Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10: 339-346.
48. NIYOGI, K.K.; FINK, G.R., 1992: Two anthranilate synthase genes in Arabidopsis defense-related regulation of the tryptofan pathway. Plant Cell 4: 721-733.
49. NORET, N.; MEERTS, P.; TOLRÀ, R.; POSCHENRIEDER, C.; BARCELÓ, J., ESCARRÉ, J., 2005: Palatability of Thlaspi caerulescens for snails: influence of zinc and glucosinolates. New Phytol. 165: 763-772.
50. PAPOYAN, A.; KOCHIAN, L.V., 2004: Characterization of a heavy metal transporting P-type Atpase from Thlaspi caerulescens: does it play a role in heavy metal hyperaccumulation? Plant Physiol. 136: 3814-3823.
51. PEDLEY, K.F.; MARTIN, G.B., 2005: Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol. 8: 541-547.
52. PENCE, N.S.; LARSEN, P.B.; EBBS, S.D.; LASAT, M.M.; LETHAM, D.L.D., GARVIN, D.F., EIBE, D.E., KOCHIAN, L.V., 2000: The molecular basis for heavy metal hyperaccumulation in Thlaspi caerulescens. Proc. Natl. Acad. Sci. U.S.A. 97: 4956-4960.
53. 3+-induced anion channels. Plant Physiol. 125: 292-305.
54. POLLARD, A.J.; BAKER, A.J.M., 1997: Deterrence of herbivory by Zinc hyperaccumulation in Thlaspi caerulescens (Brassicaceae). New Phytol. 135: 655-658.
55. POSCHENRIEDER, C.; TOLRÀ, R.; BARCELÓ, J., 2005: A role for cyclic hydroxamates in aluminum resistance in maize. J. Inorg. Biochem. 99: 1830-1836.
56. POSCHENRIEDER, C.; TOLRÀ, R.; BARCELÓ, J., 2006: Can metals defend plants against biotic stress? Trends Plant Sci. 11, 6: 288-295.
57. ROMERO-PUERTAS, M.; PERAZZOLLI, M., ZAGO, E.D., DELLEDONNI, M., 2004: Nitric oxide signalling function in plant pathogen interactions. Cell. Microbiol. 6: 795-803.
58. RÖMHELD, V.; GULDNER, M.; YAMADA, G.T.; OZTURK, L.; NEUMANN, G., 2005: Relevance of glyphosate in the rhizosphere of non-target plants in orchards for plant health. In: LI, C.J.; ZHANG, F.S.; DOBERMANN, A.; HINSINGER, P.; LAMBERS, H.; LI, X.L.; MARSCHNER, P.; MAENE, L.; MCGRATH, S.; OENEMA, O.; PENG, S.B.; RENGEL, Z.; SHEN, Q.R.; WELCH, R.; VON WIRÉN, N.; YAN, X.L.; ZHU, Y.G. (eds) Plant Nutrition for Food Security, Human Health and Environmental Protection. Beijing, China, Tsinghua University Press. 476-477.
59. RYAN, P.R.; DELHAIZE, E.; JONES, D.L., 2001: Function and mechanism of organic anion exudation from plant roots. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52: 527-560.
60. SCHAT, H.; LLUGANY, M.; BERNHARD, R., 2000: Metal-specific patterns of tolerance, uptake, and transport of heavy metals in hyperaccumulating and nonhyperaccumulating metallophytes. In: TERRY, N.; BAÑUELOS, G. (eds) Phytoremediation of Contaminated Soil and Water. Boca Raton, CRC Press LLC, Lewis Publishers. 171-188.
61. SCHÜTZENDÜBEL, A.; POLLE, A., 2002: Plant responses to abiotic stress: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 53: 1351-1365.
62. SIVAGURU, M.: EZAKI, B.; HE, Z-H., TANG, H.; OSAVA, H., BALUSKA, F.; VOLKMANN, D.; MATSUMOTO, H., 2003: Aluminum-induced gene-expression and protein localization of a cell wall associated receptor protein kinase in Arabidopsis thaliana. Plant Physiol. 132: 2256-2266.
63. STOUGAARD, J., 2000: Regulators and regulation of legume root nodule development. Plant Physiol. 124: 531-540.
64. TAKKEN, F.L.W.; JOOSTEN, M.H.A.J., 2000: Plant resistance genes: their structure, function and evolution. Eur. J. Plant Pathol. 106: 699-703.
65. TOLRÀ, R.P.; POSCHENRIEDER, C., BARCELÓ, J., 1996a: Zinc hyperaccumulation in Thlaspi caerulescens. I. Influence on growth and mineral nutrition. J. Plant Nutr. 19: 1531-1540.
66. TOLRÀ, R.P.; POSCHENRIEDER, C.; BARCELÓ, J., 1996b: Zinc hyperaccumulation in Thlaspi caerulescens. II. Influence on organic acids. J. Plant Nutr. 19: 1541-1550.
67. TOLRÀ, R.; POSCHENRIEDER, C.; ALONSO, R.; BARCELÓ, D.; BARCELÓ, J., 2001: Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens. New Phytol. 151: 621-626.
68. VAN HOOF, N.A.L.M.; HASSINEN, V.H.; HAKVOORT, H.W.J.; BALLINTJIN, K.F.; SCHAT, H.; VERKLEIJ, J.A.C., ERNST, W.H.O.; KARENLAMPI, S.O.; TERVAHAUTA, A.L., 2001a: Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b type metallothioneine gene. Plant Physiol. 126: 1519-1526.
69. VAN HOOF, N.A.L.M.; KOEVOETS, P.L.M.; TEN BOOKUM, W.M.; SCHAT, H.; VERKLEIJ, J.A.C.; ERNST, W.H.O., 2001b: Enhanced ATP-dependent copper efflux across the root cell plasma membrane in copper tolerant Silene vulgaris. Physiol. Plant. 113: 225-236.
70. VERKLEIJ, J.A.C.; KOEVOETS, P.L.M.; BLAKE-KALFF, M.M.A.; CHARDONNENS, A.N., 1998: Evidence for an important role of the tonoplast in the mechanism of naturally selected zinc tolerance in Silene vulgaris. J. Plant Physiol. 153: 188-191.
71. VOLLENWEIDER, P.; GÜNTHARDT-GOERG, M.S., 2005: Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. Environ. Pollut. 137: 455-465.
72. XIANG, C.; OLIVER, D.J., 1998: Glutathione metabolic genes coordinate response to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10: 1539-1550.
73. ZHAO, F.J.; WONG, J.R.; BARKER, J.H.A.; SCHAT, H.; BLEEKER, P.M., MCGRATH, S.P., 2003: The role of phytochelatins in arsenic tolerance in the hyperaccumulator Pteris vittata. New Phytol. 159: 403-410.
74. ZIPFEL, C.; FELIX, G., 2005: Plants and animals: a different taste for microbes. Curr. Opin. Plant Biol. 8: 353-360.