Involvement of hexokinase1 in plant growth promotion as mediated by burkholderia phytofirmans

Canadian Journal of Microbiology

Volumn 60, Issue 6, 2014, Pages 343-354

  Park, Jae Min ^a,b   Lazarovits, George ^b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b Agroecology Research Services Centre   (Canada)

Author keywords

Burkholderia phytofirmans; Hexokinase1; Plant growth promoting bacteria; Potato plant; Sugars

Indexed keywords

FRUCTOSE; GLUCOSE; HEXOKINASE 1; MESSENGER RNA; SUCROSE; CARBOHYDRATE; CHLOROPHYLL; HEXOKINASE; MALTOSE; PLANT RNA;

AGAR; BACTERIUM; BIOASSAY; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; GROWTH RATE; GROWTH REGULATOR; INOCULATION; LABORATORY METHOD; POTATO; RNA; SUGAR;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOMASS; BURKHOLDERIA; BURKHOLDERIA PHYTOFIRMANS; CHLOROPHYLL CONTENT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; NONHUMAN; PLANT DEVELOPMENT; PLANT-GROWTH PROMOTING BACTERIUM; ROOT GROWTH; SUGAR TRANSPORT; BACTÉRIES FAVORISANT LA CROISSANCE VÉGÉTALE; CARBOHYDRATE METABOLISM; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEXOKINASE1; METABOLISM; MICROBIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PLANT LEAF; PLANT ROOT; PLANT STEM; PLANT-GROWTH-PROMOTING BACTERIA; PLANTE DE LA POMME DE TERRE; POTATO; POTATO PLANT; SUCRES;

BACTERIA (MICROORGANISMS); BURKHOLDERIA PHYTOFIRMANS; SOLANUM TUBEROSUM;

BACTÉRIES FAVORISANT LA CROISSANCE VÉGÉTALE; BURKHOLDERIA PHYTOFIRMANS; HEXOKINASE1; PLANT-GROWTH-PROMOTING BACTERIA; PLANTE DE LA POMME DE TERRE; POTATO PLANT; SUCRES; SUGARS;

BURKHOLDERIA; CARBOHYDRATE METABOLISM; CHLOROPHYLL; FRUCTOSE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; GLUCOSE; HEXOKINASE; MALTOSE; PHOSPHORYLATION; PLANT LEAVES; PLANT ROOTS; PLANT STEMS; RNA, PLANT; SOLANUM TUBEROSUM; SUCROSE;

EID: 84907963385     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2014-0053     Document Type: Article

References (49)

1. Ait Barka, E., Nowak, J., and Clément, C. 2006. Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhi-zobacterium, Burkholderia phytofirmans strain PsJN. Appl. Environ. Microbiol. 72: 7246–7252. doi:10.1128/AEM.01047-06. PMID:16980419.
2. Arkhipova, T.N., Veselov, S.U., Melentiev, A.L., Martynenko, E.V., and Kudoyarova, G.R. 2005. Ability of bacterium Bacillus subtilis to produce cyto-kinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil, 272: 201–209. doi:10.1007/s11104-004-5047-x.
3. Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., and Vivanco, J.M. 2006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57: 233–266. doi:10.1146/annurev.arplant.57.032905. 105159. PMID:16669762.
4. Cho, Y.H., and Yoo, S.D. 2011. Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PloS Genet. 6: e1001263. doi:10.1371/journal.pgen. 1001263. PMID:21253566.
5. Cho, Y.H., Yoo, S.D., and Sheen, J. 2006. Regulatory functions of nuclear hexo-kinase1 complex in glucose signaling. Cell, 127: 579–589. doi:10.1016/j.cell. 2006.09.028. PMID:17081979.
6. Claeyssen, É., and Rivoal, J. 2007. Isozymes of plant hexokinase: occurrence, properties and function. Phytochemistry, 68: 709–731. doi:10.1016/j.phyto chem.2006.12.001. PMID:17234224.
7. Damari-Weissler, H., Rachamilevitch, S., Aloni, R., German, M.A., Cohen, S., Zwieniecki, M.A., et al. 2009. LeFRK2 is required for phloem and xylem differentiation and the transport of both sugar and water. Planta, 230: 795–805. doi:10.1007/s00425-009-0985-4. PMID:19633866.
8. Eveland, A.L., and Jackson, D.P. 2012. Sugars, signaling, and plant development. J. Exp. Bot. 63: 3367–3377. doi:10.1093/jxb/err379. PMID:22140246.
9. Frommel, M.I., Nowak, J., and Lazarovits, G. 1991. Growth enhancement and development modifications of in vitro grown potato (Solanum tuberosum ssp. tuberosum) as affected by a non fluorescent Pseudomonas sp. Plant Physiol. 96: 928–936. doi:10.1104/pp.96.3.928. PMID:16668277.
10. Fukuhara, H., Minakawa, Y., Akao, S., and Minamisawa, K. 1994. The involvement of indole-3-acetic acid produced by Bradyrhizobium elkanii in nodule formation. Plant Cell Physiol. 35: 1261–1265.
11. Gamalero, E., and Glick, B.R. 2011. Mechanism used by plant growth promoting bacteria. In Bacteria in agrobiology: plant nutrient management. Edited by D.K. Maheshwari. Springer, Berlin, Heidelberg, Germany. pp. 17–46.
12. German, M.A., Dai, N., Chmelnitsky, I., Sobolev, I., Salts, Y., Barg, R., et al. 2002. LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically expressed in stamens. Plant Sci. 163: 607–613. doi:10.1016/S0168-9452(02) 00170-X.
13. Gibson, S.I. 2005. Control of plant development and gene expression by sugar signaling. Curr. Opin. Plant Biol. 8: 93–102. doi:10.1016/j.pbi.2004.11.003. PMID:15653406.
14. Glick, B.R., Jacobson, C.B., Schwarze, M.M.K., and Pasternak, J.J. 1994. 1-Amino-cycloprapane-1-carboxylic acid deaminase mutants of the plant growth promoting rhizobacterium Pseudomonas putida GR12-2 do not stimulate canola root elongation. Can. J. Microbiol. 40: 911–915. doi:10.1139/m94-146.
15. Granot, D., David-Schwartz, R., and Kelly, G. 2013. Hexose kinases and their role in sugar-sensing and plant development. Front. Plant Sci. 4: 44. doi:10.3389/ fpls.2013.00044. PMID:23487525.
16. Granot, D., Kelly, G., Stein, O., and David-Schwartz, R. 2014. Substantial roles of hexokinase and fructokinase in the effects of sugars on plant physiology and development. J. Exp. Bot. 66: 809–819. doi:10.1093/jxb/ert400. PMID: 24293612.
17. Hida, A., Shimizu, K., Nagata, R., Yabuya, T., and Adachi, T. 1999. Plant regeneration from protoplast of Iris hollandica Hort. Euphytica, 105: 99–102. doi:10. 1023/A:1003407501918.
18. Jang, J.C., and Sheen, J. 1994. Sugar sensing in higher plants. Plant Cell, 6: 1665–1679. doi:10.1105/tpc.6.11.1665. PMID:7827498.
19. Jang, J.C., León, P., Zhou, L., and Sheen, J. 1997. Hexokinase as a sugar sensor in higher plants. Plant Cell, 9: 5–19. doi:10.1105/tpc.9.1.5. PMID:9014361.
20. Lejay, L., Gansel, X., Cerezo, M., Tillard, P., Muller, C., Krapp, A., et al. 2003. Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell, 15: 2218–2232. doi:10.1105/tpc. 013516. PMID:12953122.
21. Lejay, L., Wirth, J., Pervent, M., Cross, J.M., Tillard, P., and Gojon, A. 2008. Oxi-dative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol. 146: 2036–2053. doi:10.1104/pp.107.114710. PMID:18305209.
22. León, P., and Sheen, J. 2003. Sugar and hormone connections. Trends Plant Sci. 8: 110–116. doi:10.1016/S1360-1385(03)00011-6. PMID:12663220.
23. Li, P., Wind, J.J., Shi, X., Zhang, H., Hanson, J., Smeekens, S.C., and Teng, S. 2011. Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANACo89 lacking the membrane-bound domain. Proc. Natl. Acad. Sci. U.S.A. 22: 3436–3441. doi:10.1073/pnas.1018665108. PMID:21300879.
24. MacMillan, J. 2001. Occurrence of gibberellins in vascular plants, fungi, and bacteria. J. Plant Growth Regul. 20: 387–442. doi:10.1007/s003440010038. PMID:11986764.
25. Moisan, M.C., and Rivoal, J. 2011. Purification to homogeneity and characterization of nonproteolyzed potato (Solanum tuberosum) tuber hexokinase 1. Botany, 89(5): 289–299. doi:10.1139/b11-016.
26. Moore, B., Zhou, L., Rolland, F., Hall, Q.I., Cheng, W.H., Liu, Y.X., et al. 2003. Role of Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science, 300: 332–336. doi:10.1126/science.1080585. PMID:12690200.
27. Morgan, J.M. 1984. Osmoregulation and water stress in higher plants. Annu. Rev. Plant Physiol. 35: 299–319. doi:10.1146/annurev.pp.35.060184.001503.
28. Ortíz-Castro, R., Valencia-Cantero, E., and López-Bucio, J. 2008. Plant growth promotion by Bacillus megaterium involves cytokinin signaling. Plant Signaling Behav. 3: 263–265. doi:10.4161/psb.3.4.5204. PMID:19704649.
29. Pego, J.V., and Smeekens, S.C. 2000. Plant fructokinase: a sweet family get-together. Trends Plant Sci. 5: 531–536. doi:10.1016/S1360-1385(00)01783-0. PMID:11120475.
30. Pillay, V.K., and Nowak, J. 1997. Inoculum density, temperature, and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicon esculentum L.) seedling inoculated with a pseu-domonad bacterium. Can. J. Microbiol. 43(4): 354–361. doi:10.1139/m97-049.
31. Plaxton, W.C. 1996. The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 185–214. doi:10.1146/annurev.arplant.47.1.185. PMID:15012287.
32. Poupin, M.J., Timmermann, T., Vega, A., Zúñiga, A., and González, B. 2013. Effects of the plant growth-promoting bacterium Burkholderia phytofirmans PsJN throughout the life cycle of Arabidopsis thaliana. PloS One, 8: e69435. doi:10.1371/journal.pone.0069435. PMID:23869243.
33. Renz, A., and Stitt, M. 1993. Substrate specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. Planta, 190: 166–175. doi:10.1007/BF00196608.
34. Rodrguez, H., and Fraga, F. 1999. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17: 319–339. doi:10.1016/S0734-9750(99)00014-2. PMID:14538133.
35. Rolland, F., Moore, B., and Sheen, J. 2002. Sugar sensing and signaling in plants. Plant Cell, 14: S185–S205. doi:10.1105/tpc.010455. PMID:12045277.
36. Rolland, F., Baena-Gonzales, E., and Sheen, J. 2006. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57: 675–709. doi:10.1146/annurev.arplant.57.032905.105441. PMID:16669778.
37. Rook, F., Gerrits, N., Kortstee, A., van Kampen, M., Borrias, M., Weisbeek, P., and Smeekens, S. 1998. Sucrose-specific signaling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J. 15: 253–263. doi:10. 1046/j.1365-313X.1998.00205.x. PMID:9721683.
38. Saftner, R.A., and Wyse, R.F. 1984. Effect of plant hormones on sucrose uptake by sugar beet root tissue disk. Plant Physiol. 74: 951–955. doi:10.1104/pp.74.4.951. PMID:16663540.
39. Sheen, J. 1990. Metabolic repression of transcription in higher plants. Plant Cell, 2: 1027–1038. doi:10.1105/tpc.2.10.1027. PMID:2136626.
40. Sun, Y., Cheng, Z., and Glick, B.R. 2009. The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophyte plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol. Lett. 296: 131–136. doi:10.1111/j.1574-6968.2009.01625.x. PMID:19459964.
41. Teng, S., Keurentjes, J., Bentsink, L., Koornneef, M., and Smeekens, S. 2005. Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the myb75/pap1 gene. Plant Physiol. 139: 1840–1852. doi:10.1104/pp.105. PMID:16299184.
42. Towle, H.C. 2005. Glucose as a regulator of eukaryotic gene transcription. Trends Endocrinol. Metab. 16: 489–494. doi:10.1016/j.tem.2005.10.003. PMID:16269245.
43. van Rhijn, P., and Vanderleyden, J. 1995. The rhizobium–plant symbiosis. Microbiol. Rev. 59: 124–142. PMID:7708010.
44. Wang, K., Conn, K., and Lazarovits, G. 2006. Involvement of quinolinate phos-phoribosyl transferase in promotion of potato growth by a Burkholderia strain. Appl. Environ. Microbiol. 72: 760–768. doi:10.1128/AEM.72.1.760-768. 2006. PMID:16391116.
45. Wiese, A., Elzinga, N., Wobbes, B., and Smeekens, S. 2004. A conserved upstream open reading frame mediates sucrose-induced repression of translation. Plant Cell, 16: 1717–1729. doi:10.1105/tpc.019349. PMID:15208401.
46. Xu, L. 2008. Bacteria root colonization and its effect on plant growth. M.Sc. thesis, Western University, London, Ont., Canada.
47. Zhang, H., Xie, X., Kim, M.S., Kornyeyev, D.A., Holaday, S., and Paré, P.W. 2008. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J. 56: 264–273. doi:10.1111/j.1365-313X.2008.03593.x. PMID:18573192.
48. Zorb, C., Schmitt, S., and Muhling, K.H. 2010. Proteomic changes in maize roots after short-term adjustment to saline growth condition. Proteomics, 10: 4441–4449. doi:10.1002/pmic.201000231. PMID:21136597.
49. Zúñiga, A., Poupin, M.J., Donoso, R., Ledger, T., Guiliani, N., Gutiérrez, R.A., and González, B. 2013. Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Mol. Plant–Microbe Interact. 26: 546–553. doi:10.1094/MPMI-10-12-0241-R. PMID:23301615.