ENO2 activity is required for the development and reproductive success of plants, and is feedback-repressed by AtMBP-1

Plant Journal

Volumn 81, Issue 6, 2015, Pages 895-906

  Eremina, Marina ^a   Rozhon, Wilfried ^a   Yang, Saiqi ^a   Poppenberger, Brigitte ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Arabidopsis; bifunctional; glycolysis; lignification; LOS2; secondary growth

Indexed keywords

DEFECTS; FATTY ACIDS; METABOLITES; PLANTS (BOTANY); TRANSCRIPTION;

ARABIDOPSIS; BI-FUNCTIONAL; GLYCOLYSIS; LIGNIFICATION; LOS2; SECONDARY GROWTH;

SALICYLIC ACID;

ARABIDOPSIS; EUKARYOTA; PROKARYOTA;

2-O-SINAPOYLMALATE; ARABIDOPSIS PROTEIN; CHORISMIC ACID; ENOLASE; LIGNIN; LOS2 PROTEIN, ARABIDOPSIS; MALIC ACID DERIVATIVE; PHENYLPROPIONIC ACID DERIVATIVE; SALICYLIC ACID;

ARABIDOPSIS; ENZYMOLOGY; FEEDBACK SYSTEM; FLOWER; GENE INACTIVATION; GENETICS; GLYCOLYSIS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGY; PLANT SEED; PLANT STEM; REPRODUCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHORISMIC ACID; FEEDBACK, PHYSIOLOGICAL; FLOWERS; GENE KNOCKOUT TECHNIQUES; GLYCOLYSIS; LIGNIN; MALATES; METABOLIC NETWORKS AND PATHWAYS; MUTATION; PHENOTYPE; PHENYLPROPIONATES; PHOSPHOPYRUVATE HYDRATASE; PLANT STEMS; REPRODUCTION; SALICYLIC ACID; SEEDS;

EID: 84924445555     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12775     Document Type: Article

References (40)

1. Andriotis, V.M.E., Kruger, N.J., Pike, M.J., and, Smith, A.M., (2010) Plastidial glycolysis in developing Arabidopsis embryos. New Phytol. 185, 649-662.
2. Barkla, B.J., Vera-Estrella, R., Hernández-Coronado, M., and, Pantoja, O., (2009) Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. Plant Cell, 21, 4044-4058.
3. Beeckman, T., and, Viane, R., (2000) Embedding thin plant specimens for oriented sectioning. Biotech. Histochem. 75, 23-26.
4. Brown, D.M., Zeef, L.A., Ellis, J., Goodacre, R., and, Turner, S.R., (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell, 17, 2281-2295.
5. Canback, B., Andersson, S.G.E., and, Kurland, C.G., (2002) The global phylogeny of glycolytic enzymes. Proc. Natl Acad. Sci. USA, 99, 6097-6102.
6. 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.
7. Díaz-Ramos, A., Roig-Borrellas, A., García-Melero, A., and, López-Alemany, R., (2012) α-Enolase, a multifunctional protein: its role on pathophysiological situations. J. Biomed. Biotechnol. 2012, 156795.
8. Fan, L.M., Wang, Y.F., Wang, H., and, Wu, W.H., (2001) In vitro Arabidopsis pollen germination and characterization of the inward potassium currents in Arabidopsis pollen grain protoplasts. J. Exp. Bot. 52, 1603-1614.
9. Feo, S., Arcuri, D., Piddini, E., Passantino, R., and, Giallongo, A., (2000) ENO1 gene product binds to the c-myc promoter and acts as a transcriptional repressor: relationship with Myc promoter-binding protein 1 (MBP-1). FEBS Lett. 473, 47-52.
10. Franke, R., Hemm, M.R., Denault, J.W., Ruegger, M.O., Humphreys, J.M., and, Chapple, C., (2002) Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J. 30, 47-59.
11. Gallego-Giraldo, L., Escamilla-Trevino, L., Jackson, L.A., and, Dixon, R.A., (2011a) Salicylic acid mediates the reduced growth of lignin down-regulated plants. Proc. Natl Acad. Sci. USA, 108, 20814-20819.
12. Gallego-Giraldo, L., Jikumaru, Y., Kamiya, Y., Tang, Y., and, Dixon, R.A., (2011b) Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.). New Phytol. 190, 627-639.
13. Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D., and, Thomashow, M.F., (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol. 124, 1854-1865.
14. Hsu, K.W., Hsieh, R.H., Wu, C.W., Chi, C.W., Lee, Y.H., Kuo, M.L., Wu, K.J., and, Yeh, T.S., (2009) MBP-1 suppresses growth and metastasis of gastric cancer cells through COX-2. Mol. Biol. Cell, 20, 5127-5137.
15. Jones, L., Ennos, A.R., and, Turner, S.R., (2001) Cloning and characterization of irregular xylem4 (irx4): a severely lignin-deficient mutant of Arabidopsis. Plant J. 26, 205-216.
16. Kachroo, A., Lapchyk, L., Fukushige, H., Hildebrand, D., Klessig, D., and, Kachroo, P., (2003) Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell, 15, 2952-2965.
17. Kang, M., Abdelmageed, H., Lee, S., Reichert, A., Mysore, K.S., and, Allen, R.D., (2013) AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. Plant J. 76, 481-493.
18. Landry, L.G., Chapple, C.C.S., and, Last, R.L., (1995) Arabidopsis mutants lacking phenolic sunscreens exhibit enhanced ultraviolet-B injury and oxidative damage. Plant Physiol. 109, 1159-1166.
19. Lee, H., Guo, Y., Ohta, M., Xiong, L., Stevenson, B., and, Zhu, J.K., (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J. 21, 2692-2702.
20. Li, X., Bonawitz, N.D., Weng, J.K., and, Chapple, C., (2010) The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. Plant Cell, 22, 1620-1632.
21. Lim, H., Cho, M.H., Jeon, J.S., Bhoo, S.H., Kwon, Y.K., and, Hahn, T.R., (2009) Altered expression of pyrophosphate: fructose-6-phosphate 1-phosphotransferase affects the growth of transgenic Arabidopsis plants. Mol. Cells, 27, 641-649.
22. Osthus, R.C., Shim, H., Kim, S., Li, Q., Reddy, R., Mukherjee, M., Xu, Y., Wonsey, D., Lee, L.A., and, Dang, C.V., (2000) Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 275, 21797-21800.
23. Plaxton, W.C., (1996) The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 185-214.
24. Prabhakar, V., Löttgert, T., Gigolashvili, T., Bell, K., Flügge, U.I., and, Häusler, R.E., (2009) Molecular and functional characterization of the plastid-localized phosphoenolpyruvate enolase ENO1 from Arabidopsis thaliana. FEBS Lett. 583, 983-991.
25. Prabhakar, V., Löttgert, T., Geimer, S., et al. (2010) Phosphoenolpyruvate provision to plastids is essential for gametophyte and sporophyte development in Arabidopsis thaliana. Plant Cell, 22, 2594-2617.
26. Rawsthorne, S., (2002) Carbon flux and fatty acid synthesis in plants. Prog. Lipid Res. 41, 182-196.
27. Rius, S.P., Casati, P., Iglesias, A.A., and, Gomez-Casati, D.F., (2008) Characterization of Arabidopsis lines deficient in GAPC-1, a cytosolic NAD-dependent glyceraldehyde-3-phosphate dehydrogenase. Plant Physiol. 148, 1655-1667.
28. Rivas-San Vicente, M., and, Plasencia, J., (2011) Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62, 3321-3338.
29. Rozhon, W., Mayerhofer, J., Petutschnig, E., Fujioka, S., and, Jonak, C., (2010) ASKtheta, a group-III Arabidopsis GSK3, functions in the brassinosteroid signalling pathway. Plant J. 62, 215-223.
30. Sanchez, P., Nehlin, L., and, Greb, T., (2012) From thin to thick: major transitions during stem development. Trends Plant Sci. 17, 113-121.
31. Uemura, M., Joseph, R.A., and, Steponkus, P.L., (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol. 109, 15-30.
32. Van Der Straeten, D., Rodrigues-Pousada, R.A., Goodman, H.M., and, Van Montagu, M., (1991) Plant enolase: gene structure, expression, and evolution. Plant Cell, 3, 719-735.
33. Vanholme, R., Demedts, B., Morreel, K., Ralph, J., and, Boerjan, W., (2010) Lignin biosynthesis and structure. Plant Physiol. 153, 895-905.
34. Vermerris, W., and, Nicholson, R., (2006) Phenolic Compound Biochemistry. Dordrecht, Netherlands: Springer.
35. Voll, L.M., Hajirezaei, M.R., Czogalla-Peter, C., Lein, W., Stitt, M., Sonnewald, U., and, Börnke, F., (2009) Antisense inhibition of enolase strongly limits the metabolism of aromatic amino acids, but has only minor effects on respiration in leaves of transgenic tobacco plants. New Phytol. 184, 607-618.
36. Wang, D., Pajerowska-Mukhtar, K., Culler, A.H., and, Dong, X., (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17, 1784-1790.
37. Wen, W., Meinkoth, J.L., Tsien, R.Y., and, Taylor, S.S., (1995) Identification of a signal for rapid export of proteins from the nucleus. Cell, 82, 463-473.
38. Yoo, S.D., Cho, Y.H., and, Sheen, J., (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565-1572.
39. Zhao, Z., and, Assmann, S.M., (2011) The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. J. Exp. Bot. 62, 5179-5189.
40. Zhao, Q., Nakashima, J., Chen, F., Yin, Y., Fu, C., Yun, J., Shao, H., Wang, X., Wang, Z.Y., and, Dixon, R.A., (2013) Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell, 25, 3976-3987.