Metabolic engineering of raffinose-family oligosaccharides in the phloem reveals alterations in carbon partitioning and enhances resistance to green peach aphid

Frontiers in Plant Science

Volumn 4, Issue JUL, 2013, Pages

  Cao, Te ^a   Lahiri, Ipsita ^a   Singh, Vijay ^a   Louis, Joe ^a,b   Shah, Jyoti ^a   Ayre, Brian G ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Green peach aphid; Metabolic engineering; Phloem transport; Raffinose family oligosaccharides; Sugar transport

Indexed keywords

EID: 84900812474     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00263     Document Type: Article

References (61)

1. Ayre, B. G. (2011). Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol. Plant 4, 377-394. doi: 10.1093/mp/ssr014
2. Ayre, B. G., Blair, J. E., and Turgeon, R. (2003a). Functional and phylogenetic analyses of a conserved regulatory program in the phloem of minor veins. Plant Physiol. 133, 1229-1239. doi: 10.1104/pp.103.027714
3. Ayre, B. G., Keller, F., and Turgeon, R. (2003b). Symplastic continuity between companion cells and the translocation stream: long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol. 131, 1518-1528. doi: 10.1104/pp.012054
4. Ayre, B. G., and Turgeon, R. (2004). Graft transmission of a floral stimulant derived from CONSTANS. Plant Physiol. 135, 2271-2278. doi: 10.1104/pp.104.040592
5. Bailly, C., Audigier, C., Ladonne, F., Wagner, M. H., Coste, F., Corbineau, F., et al. (2001). Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. J. Exp. Bot. 52, 701-708.
6. Becker, D., Kemper, E., Schell, J., and Masterson, R. (1992). New plant binary vectors with selectable markers located proximal to the left T-DNA border. Plant Mol. Biol. 20, 1195-1197. doi: 10.1007/BF00028908
7. Beebe, D. U., and Turgeon, R. (1992). Localization of galactinol, raffinose, and stachyose synthesis in Cucurbita pepo leaves. Planta 188, 354-361. doi: 10.1007/BF00192802
8. Bernier, G. (1988). The control of floral evocation and morphogenesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 175-219. doi: 10.1146/annurev.pp.39.060188.001135
9. Blasing, O. E., Gibon, Y., Gunther, M., Hohne, M., Morcuende, R., Osuna, D., et al. (2005). Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17, 3257-3281. doi: 10.1105/tpc.105.035261
10. Burch-Smith, T. M., and Zambryski, P. C. (2012). Plasmodesmata paradigm shift: regulation from without versus within Annu. Rev. Plant Biol. 63, 239-260. doi: 10.1146/annurev-arplant-042811-105453
11. Chen, L.-Q., Qu, X.-Q., Hou, B.-H., Sosso, D., Osorio, S., Fernie, A. R., et al. (2012). Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335, 207-211. doi: 10.1126/science.1213351
12. Chincinska, I. A., Liesche, J., Krugel, U., Michalska, J., Geigenberger, P., Grimm, B., et al. (2008). Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol. 146, 515-528. doi: 10.1104/pp.107.112334
13. Cho, S. M., Kang, E. Y., Kim, M. S., Yoo, S. J., Im, Y. J., Kim, Y. C., et al. (2010). Jasmonate-dependent expression of a galactinol synthase gene is involved in priming of systemic fungal resistance in Arabidopsis thaliana. Botany-Botanique 88, 452-461. doi: 10.1139/B10-009
14. Clough, S. J., and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743. doi: 10.1046/j.1365-313x.1998.00343.x
15. Corbesier, L., Lejeune, P., and Bernier, G. (1998). The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206, 131-137. doi: 10.1007/s004250050383
16. Erickson, R. O., and Michelini, F. J. (1957). The plastochron index. Am. J. Bot. 44, 297-305. doi: 10.2307/2438380
17. Gamalei, Y. V. (1989). Structure and function of leaf minor veins trees and herbs. A taxonomic review. Trees 3, 96-110. doi: 10.1007/BF01021073
18. Gamalei, Y. V. (1991). Phloem loading and its development related to plant evolution from trees to herbs. Trees 5, 50-64. doi: 10.1007/BF00225335
19. Gottwald, J. R., Krysan, P. J., Young, J. C., Evert, R. F., and Sussman, M. R. (2000). Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc. Natl. Acad. Sci. U.S.A. 97, 13979-13984. doi: 10.1073/pnas.250473797
20. Hannah, M. A., Zuther, E., Buchel, K., and Heyer, A. G. (2006). Transport and metabolism of raffinose family oligosaccharides in transgenic potato. J. Exp. Bot. 57, 3801-3811. doi: 10.1093/jxb/erl152
21. Haritatos, E., Ayre, B. G., and Turgeon, R. (2000a). Identification of phloem involved in assimilate loading in leaves by the activity of the GALACTINOL SYNTHASE promoter. Plant Physiol. 123, 929-937. doi: 10.1104/pp.123.3.929
22. Haritatos, E., Medville, R., and Turgeon, R. (2000b). Minor vein structure and sugar transport in Arabidopsis thaliana. Planta 211, 105-111. doi: 10.1007/s004250000268
23. Harrison, S. J., Mott, E. K., Parsley, K., Aspinall, S., Gray, J. C., and Cottage, A. (2006). A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2:19. doi: 10.1186/1746-4811-2-19
24. Hewer, A., Becker, A., and van Bel, A. J. E. (2011). An aphid's Odyssey-the cortical quest for the vascular bundle. J. Exp. Biol. 214, 3868-3879. doi: 10.1242/jeb.060913
25. Hewer, A., Will, T., and van Bel, A. J. E. (2010). Plant cues for aphid navigation in vascular tissues. J. Exp. Biol. 213, 4030-4042. doi: 10.1242/jeb.046326
26. Keller, F., and Pharr, D. M. (1996). "Metabolism of carbohydrates in sinks and sources: galactosyl-sucrose oligosaccharides, " in Photoassimilate Distribution in Plants and Crops: Source-Sink Relationships, eds E. Zamski and A. A. Schaffer (New York, NY: Marcel Dekker), 157-183.
27. Kempers, R., and van Bel, A. J. E. (1997). Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L have a molecular exclusion limit of at least 10 kDa. Planta 201, 195-201. doi: 10.1007/BF01007704
28. Kim, M. S., Cho, S. M., Kang, E. Y., Im, Y. J., Hwangbo, H., Kim, Y. C., et al. (2008). Galactinol is a signaling component of the induced systemic resistance caused by Pseudomonas chlororaphis O6 root rolonization. Mol. Plant Microbe Interact. 21, 1643-1653. doi: 10.1094/MPMI-21-12-1643
29. King, R. W., and Zeevaart, J. A. (1974). Enhancement of phloem exudation from cut petioles by chelating-agents. Plant Physiol. 53, 96-103. doi: 10.1104/pp.53.1.96
30. Knoblauch, M., and van Bel, A. J. E. (1998). Sieve tubes in action. Plant Cell 10, 35-50.
31. Koncz, C., and Schell, J. (1986). The promoter of Ti-DNA gene 5 controls the tissue-specific expression of chimeric genes carried by a novel type of Agrobacterium binary vector. Mol. Gen. Genet. 204, 383-396. doi: 10.1007/BF00331014
32. Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W. B., and Patrick, J. W. (2003). Phloem loading and unloading of sugars and amino acids. Plant Cell Environ. 26, 37-56. doi: 10.1046/j.1365-3040.2003.00847.x
33. Liu, D. D., Chao, W. M., and Turgeon, R. (2012). Transport of sucrose, not hexose, in the phloem. J. Exp. Bot. 63, 4315-4320. doi: 10.1093/jxb/ers127
34. Liu, J.-J. J., Krenz, D. C., Galvez, A. F., and De Lumen, B. O. (1998). Galactinol synthase (GS): increased enzyme activity and levels of mRNA due to cold and desiccation. Plant Sci. 134, 11-20. doi: 10.1016/S0168-9452(98)00042-9
35. Louis, J., Leung, Q., Pegadaraju, V., Reese, J., and Shah, J. (2010). PAD4-dependent antibiosis contributes to the ssi2-conferred hyper-resistance to the green peach aphid. Mol. Plant Microbe Interact. 23, 618-627. doi: 10.1094/MPMI-23-5-0618
36. Lunn, J. E., Feil, R., Hendriks, J. H. M., Gibon, Y., Morcuende, R., Osuna, D., et al. (2006). Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem. J. 397, 139-148. doi: 10.1042/BJ20060083
37. Martinez-Villaluenga, C., Frias, J., and Vidal-Valverde, C. (2008). Alpha-galactosides: antinutritional factors or functional ingredients. Crit. Rev. Food Sci. Nutr. 48, 301-316. doi: 10.1080/10408390701326243
38. Maule, A. J., Benitez-Alfonso, Y., and Faulkner, C. (2011). Plasmodesmata-membrane tunnels with attitude. Curr. Opin. Plant Biol. 14, 683-690. doi: 10.1016/j.pbi.2011.07.007
39. McGarry, R. C., and Ayre, B. G. (2008). A DNA element between At4g28630 and At4g28640 confers companion-cell specific expression following the sink-to-source transition in mature minor vein phloem. Planta 228, 839-849. doi: 10.1007/s00425-008-0786-1
40. Mittler, T. E., and Dadd, R. H. (1965). Differences in the probing responses of Myzus persicae (Sulzer) elicited by different feeding solutions behind a parafilm membrane. Entomol. Exp. Appl. 8, 107-122.
41. Nishizawa, A., Yabuta, Y., and Shigeoka, S. (2008). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263. doi: 10.1104/pp.108.122465
42. Otto, K. (1968). "Carbon metabolism: Nature and formation of end products, " in Harvesting The Sun-Photosynthesis In Plant Life, ed A. San Pietro (New York, NY: Academic Press, Incorporated), 131-152.
43. Patrick, J. W., Botha, F. C., and Birch, R. G. (2013). Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnol. J. 11, 142-156. doi: 10.1111/pbi.12002
44. Pegadaraju, V., Knepper, C., Reese, J., and Shah, J. (2005). Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol. 139, 1927-1934. doi: 10.1104/pp.105.070433
45. Pegadaraju, V., Louis, J., Singh, V., Reese, J. C., Bautor, J., Feys, B., et al. (2007). Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1. Plant J. 52, 332-341. doi: 10.1111/j.1365-313X.2007.03241.x
46. Peters, S., and Keller, F. (2009). Frost tolerance in excised leaves of the common bugle (Ajuga reptans L.) correlates positively with the concentrations of raffinose family oligosaccharides (RFOs). Plant Cell Environ. 32, 1099-1107. doi: 10.1111/j.1365-3040.2009.01991.x
47. Rasband, W. S. (2007). ImageJ. Available online at: http://rsb.info.nih.gov/ij/
48. Rennie, E. A., and Turgeon, R. (2009). A comprehensive picture of phloem loading strategies. Proc. Natl. Acad. Sci. U.S.A. 106, 14162-14167. doi: 10.1073/pnas.0902279106
49. Sivitz, A. B., Reinders, A., Johnson, M. E., Krentz, A. D., Grof, C. P. L., Perroux, J. M., et al. (2007). Arabidopsis sucrose transporter AtSUC9. High-affinity transport activity, intragenic control of expression, and early flowering mutant phenotype. Plant Physiol. 143, 188-198. doi: 10.1104/pp.106.089003
50. Srivastava, A. C., Ganesan, S., Ismail, I. O., and Ayre, B. G. (2008). Functional characterization of the Arabidopsis AtSUC2 Sucrose/H+ symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol. 148, 200-211. doi: 10.1104/pp.108.124776
51. Stadler, R., Wright, K. M., Lauterbach, C., Amon, G., Gahrtz, M., Feuerstein, A., et al. (2005). Expression of GFP-fusions in Arabidopsis companion cells reveals non-specific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J. 41, 319-331. doi: 10.1111/j.1365-313X.2004.02298.x
52. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al. (2002). Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417-426. doi: 10.1046/j.0960-7412.2001.01227.x
53. Truernit, E., and Sauer, N. (1995). The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of β-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196, 564-570. doi: 10.1007/BF00203657
54. Turgeon, R. (1996). Phloem loading and plasmodesmata. Trends Plant Sci. 1, 418-423. doi: 10.1016/S1360-1385(96)10045-5
55. Turgeon, R., and Ayre, B. G. (2005). "Pathways and mechanisms of phloem loading, " in Vascular Transport in Plants. eds N. M. Holbrook and M. A. Zwieniecki (New York, NY: Elsevier Academic Press), 45-67. doi: 10.1016/B978-012088457-5/50005-8
56. Turgeon, R., and Gowan, E. (1990). Phloem loading in Coleus blumei in the absence of carrier-mediated uptake of export sugar from the apoplast. Plant Physiol. 94, 1244-1249. doi: 10.1104/pp.94.3.1244
57. Turgeon, R., and Gowan, E. (1992). Sugar synthesis and phloem loading in Coleus blumei leaves. Planta 187, 388-394. doi: 10.1007/BF00195663
58. Turgeon, R., and Medville, R. (1998). The absence of phloem loading in willow leaves. Proc. Natl. Acad. Sci. U.S.A. 95, 12055-12060. doi: 10.1073/pnas.95.20.12055
59. Turgeon, R., and Medville, R. (2004). Phloem loading. A reevaluation of the relationship between plasmodesmatal frequencies and loading strategies. Plant Physiol. 136, 3795-3803. doi: 10.1104/pp.104.042036
60. Turgeon, R., Medville, R., and Nixon, K. C. (2001). The evolution of minor-vein phloem and phloem loading. Am. J. Bot. 88, 1331-1339. doi: 10.2307/3558441
61. van Bel, A. J. E., and Hess, P. H. (2008). Hexoses as phloem transport sugars: the end of a dogma. J. Exp. Bot. 59, 261-272. doi: 10.1093/jxb/erm294