Transport of defense compounds from source to sink: Lessons learned from glucosinolates

Trends in Plant Science

Volumn 20, Issue 8, 2015, Pages 508-514

  Jørgensen, Morten Egevang ^a   Nour Eldin, Hussam Hassan ^a   Halkier, Barbara Ann ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Defense compound; Glucosinolates; NPF transporters; Source sink distribution

Indexed keywords

ARABIDOPSIS;

GLUCOSINOLATE; VEGETABLE PROTEIN;

ARABIDOPSIS; METABOLISM; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; BIOLOGICAL TRANSPORT; GLUCOSINOLATES; PLANT PROTEINS;

EID: 84938998535     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2015.04.006     Document Type: Review

References (77)

1. Dixon R.A. Natural products and plant disease resistance. Nature 2001, 411:843-847.
2. McKey D. Adaptive patterns in alkaloid physiology. Am. Nat. 1974, 108:305-320.
3. Brown P.D., et al. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 2003, 62:471-481.
4. Meldau S., et al. Defence on demand: mechanisms behind optimal defence patterns. Ann. Bot. 2012, 110:1503-1514.
5. Ohnmeiss T.E., Baldwin I.T. Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 2000, 81:1765-1783.
6. Hildreth S.B., et al. Tobacco nicotine uptake permease (NUP1) affects alkaloid metabolism. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:18179-18184.
7. Shoji T., et al. Multidrug and toxic compound extrusion-type transporters implicated in vacuolar sequestration of nicotine in tobacco roots. Plant Physiol. 2009, 149:708-718.
8. Morita M., et al. Vacuolar transport of nicotine is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2447-2452.
9. Shitan N., et al. Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:751-756.
10. Shitan N., et al. Characterization of Coptis japonica CjABCB2, an ATP-binding cassette protein involved in alkaloid transport. Phytochemistry 2013, 91:109-116.
11. Otani M., et al. Characterization of vacuolar transport of the endogenous alkaloid berberine in Coptis japonica. Plant Physiol. 2005, 138:1939-1946.
12. Rentsch D., et al. NTR1 encodes a high-affinity oligopeptide transporter in Arabidopsis. FEBS Lett. 1995, 370:264-268.
13. Frommer W.B., et al. Cloning of an arabidopsis histidine transporting protein related to nitrate and peptide transporters. FEBS Lett. 1994, 347:185-189.
14. Hsu L.C., et al. Cloning a plant amino acid transporter by functional complementation of a yeast amino acid transport mutant. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:7441-7445.
15. Riesmeier J.W., et al. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 1992, 11:4705-4713.
16. Anderson J.A., et al. Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:3736-3740.
17. Steiner H.Y., et al. An Arabidopsis peptide transporter is a member of a new class of membrane transport proteins. Plant Cell 1994, 6:1289-1299.
18. Kwart M., et al. Differential expression of two related amino acid transporters with differing substrate specificity in Arabidopsis thaliana. Plant J. 1993, 4:993-1002.
19. Nour-Eldin H.H., et al. NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 2012, 488:531-534.
20. Nour-Eldin H.H., et al. Screening for plant transporter function by expressing a normalized Arabidopsis full-length cDNA library in Xenopus oocytes. Plant Methods 2006, 2:17.
21. Andersen T.G., et al. Integration of biosynthesis and long-distance transport establish organ-specific glucosinolate profiles in vegetative Arabidopsis. Plant Cell 2013, 25:3133-3145.
22. Magrath R., Mithen R. Maternal effects on the expression of individual aliphatic glucosinolates in seeds and seedlings of Brassica napus. Plant Breed. 1993, 111:249-252.
23. Kondra Z.P., Stefansson B.R. inheritance of the major glucosinolates of rapeseed (Brassica napus) meal. Can. J. Plant Sci. 1970, 50:643-647.
24. Baldwin I.T. Mechanism of damage-induced alkaloid production in wild tobacco. J. Chem. Ecol. 1989, 15:1661-1680.
25. Jørgensen K., et al. Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology. Plant Physiol. 2005, 139:363-374.
26. Jørgensen K., et al. Biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in cassava: isolation, biochemical characterization, and expression pattern of CYP71E7, the oxime-metabolizing cytochrome P450 enzyme. Plant Physiol. 2011, 155:282-292.
27. Brudenell A.J.P., et al. The phloem mobility of glucosinolates. J. Exp. Bot. 1999, 50:745-756.
28. Chen S.X., et al. Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol. 2001, 127:194-201.
29. Hagel J.M., et al. Got milk? The secret life of laticifers. Trends Plant Sci. 2008, 13:631-639.
30. Liangcheng D., Halkier A.B. Biosynthesis of glucosinolates in the developing silique walls and seeds of Sinapis alba. Phytochemistry 1998, 48:1145-1150.
31. Ellerbrock B.L., et al. Contribution of glucosinolate transport to Arabidopsis defense responses. Plant Signal. Behav. 2007, 2:282-283.
32. Müller R., et al. Differential effects of indole and aliphatic glucosinolates on lepidopteran herbivores. J. Chem. Ecol. 2010, 36:905-913.
33. Moussaieff A., et al. High-resolution metabolic mapping of cell types in plant roots. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:E1232-E1241.
34. Andersen T.G., et al. Grafting Arabidopsis. Bioprotocol 2014, 4:e1164.
35. Andersen T.G., Halkier B.A. Upon bolting the GTR1 and GTR2 transporters mediate transport of glucosinolates to the inflorescence rather than roots. Plant Signal. Behav. 2014, 9:e27740.
36. Agrawal A.A. Macroevolution of plant defense strategies. Trends Ecol. Evol. 2007, 22:103-109.
37. Kojima M., et al. Tissue distributions of dhurrin and of enzymes involved in its metabolism in leaves of Sorghum bicolor. Plant Physiol. 1979, 63:1022-1028.
38. Weid M., et al. The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13957-13962.
39. Koroleva O.A., et al. Glucosinolate-accumulating S-cells in Arabidopsis leaves and flower stalks undergo programmed cell death at early stages of differentiation. Plant J. 2010, 64:456-469.
40. Koroleva O.A., et al. Identification of a new glucosinolate-rich cell type in Arabidopsis flower stalk. Plant Physiol. 2000, 124:599-608.
41. Shroff R., et al. Nonuniform distribution of glucosinolates in Arabidopsis thaliana leaves has important consequences for plant defense. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6196-6201.
42. Shroff R., et al. Quantification of plant surface metabolites by matrix-assisted laser desorption mass spectrometry imaging: glucosinolates on Arabidopsis thaliana leaves. Plant J. 2015, 81:961-972.
43. Chen S., et al. CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J. 2003, 33:923-937.
44. Grubb D.C., et al. Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J. 2004, 40:893-908.
45. Gigolashvili T., et al. The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 2007, 51:247-261.
46. Malitsky S., et al. The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol. 2008, 148:2021-2049.
47. Reintanz B., et al. Bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 2001, 13:351-367.
48. Schuster J., Binder S. The mitochondrial branched-chain aminotransferase (AtBCAT-1) is capable to initiate degradation of leucine, isoleucine and valine in almost all tissues in Arabidopsis thaliana. Plant Mol. Biol. 2005, 57:241-254.
49. Madsen S.R., et al. Elucidating the role of transport processes in leaf glucosinolate distribution. Plant Physiol. 2014, 166:1450-1462.
50. Baetz U., Martinoia E. Root exudates: the hidden part of plant defense. Trends Plant Sci. 2014, 19:90-98.
51. Brown P.D., Morra M.J. Control of soil-borne plant pests using glucosinolate-containing plants. Adv. Agron. 1997, 61:167-231.
52. Bais H.P., et al. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 2006, 57:233-266.
53. Vaughan M.M., et al. Formation of the unusual semivolatile diterpene rhizathalene by the Arabidopsis class i terpene synthase TPS08 in the root stele is involved in defense against belowground herbivory. Plant Cell 2013, 25:1108-1125.
54. Toyomasu T., et al. Diterpene phytoalexins are biosynthesized in and exuded from the roots of rice seedlings. Biosci. Biotechnol. Biochem. 2008, 72:562-567.
55. Strehmel N., et al. Profiling of secondary metabolites in root exudates of Arabidopsis thaliana. Phytochemistry 2014, 108:35-46.
56. Vivanco J.M., et al. Altered profile of secondary metabolites in the root exudates of Arabidopsis ATP-binding cassette transporter mutants. Plant Physiol. 2008, 146:762-771.
57. Fourcroy P., et al. Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol. 2014, 201:155-167.
58. Rumberger A., Marschner P. 2-Phenylethylisothiocyanate concentration and microbial community composition in the rhizosphere of canola. Soil Biol. Biochem. 2003, 35:445-452.
59. Bressan M., et al. Exogenous glucosinolate produced by Arabidopsis thaliana has an impact on microbes in the rhizosphere and plant roots. ISME J. 2009, 3:1243-1257.
60. Schreiner M., et al. Enhanced glucosinolates in root exudates of Brassica rapa ssp rapa mediated by salicylic acid and methyl jasmonate. J. Agric. Food Chem. 2011, 59:1400-1405.
61. Grotewold E. The challenges of moving chemicals within and out of cells: insights into the transport of plant natural products. Planta 2004, 219:906-909.
62. Halkier B.A., Gershenzon J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 2006, 57:303-333.
63. Kliebenstein D.J., et al. Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 2001, 159:359-370.
64. Sonderby I.E., et al. Biosynthesis of glucosinolates - gene discovery and beyond. Trends Plant Sci. 2010, 15:283-290.
65. Li J., et al. Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol. 2008, 148:1721-1733.
66. Hansen B.G., et al. Identification of a flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J. 2007, 50:902-910.
67. Pfalz M., et al. Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification. Plant Cell 2011, 23:716-729.
68. Clay N.K., et al. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 2009, 323:95-101.
69. Bednarek P., et al. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 2009, 323:101-106.
70. Halkier B.A., Nour-Eldin H.H. Piecing together the transport pathway of aliphatic glucosinolates. Phytochem. Rev. 2009, 8:53-67.
71. Onoyovwe A., et al. morphine biosynthesis in opium poppy involves two cell types: sieve elements and laticifers. Plant Cell 2013, 25:4110-4122.
72. Koroleva O.A., Cramer R. Single-cell proteomic analysis of glucosinolate-rich S-cells in Arabidopsis thaliana. Methods 2011, 54:413-423.
73. Mikkelsen M.D., et al. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol. 2003, 131:298-308.
74. Burow M., et al. The glucosinolate biosynthetic gene AOP2 mediates feed-back regulation of jasmonic acid signaling in Arabidopsis. Mol. Plant. 2015, Published online March 7, 2015. 10.1016/j.molp.2015.03.001.
75. Frerigmann H., et al. bHLH05 is an interaction partner of MYB51 and a novel regulator of glucosinolate biosynthesis in Arabidopsis. Plant Physiol. 2014, 166:349-369.
76. Brader G., et al. Altering glucosinolate profiles modulates disease resistance in plants. Plant J. 2006, 46:758-767.
77. Saito H., et al. The jasmonate-responsive GTR1 transporter is required for gibberellin-mediated stamen development in Arabidopsis. Nat. Commun. 2015, Published online February 4, 2015. 10.1038/ncomms7095.