Identification of the Arabidopsis dry2/sqe1-5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species

Plant Journal

Volumn 59, Issue 1, 2009, Pages 63-76

  Posé, David ^a   Castanedo, Itziar ^a   Borsani, Omar ^b   Nieto, Benjamín ^c   Rosado, Abel ^a,f   Taconnat, Ludivine ^d   Ferrer, Albert ^c   Dolan, Liam ^e   Valpuesta, Victoriano ^a   Botella, Miguel A ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^c UNIVERSITY OF BARCELONA   (Spain)

^d INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^e JOHN INNES CENTRE   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Drought tolerance; NADPH oxidase; Reactive oxygen species; Squalene epoxidase; Sterol biosynthesis

Indexed keywords

ARABIDOPSIS PROTEIN; PLANT DNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SQUALENE MONOOXYGENASE; STEROL;

ARABIDOPSIS; ARTICLE; DEHYDRATION; DNA MICROARRAY; DROUGHT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MUTATION; PHYSIOLOGICAL STRESS; PLANT ROOT; PLANT STOMA;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DEHYDRATION; DNA, PLANT; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; MUTATION; NADPH OXIDASE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT ROOTS; PLANT STOMATA; REACTIVE OXYGEN SPECIES; SQUALENE MONOOXYGENASE; STEROLS; STRESS, PHYSIOLOGICAL;

ARABIDOPSIS;

EID: 67649482618     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2009.03849.x     Document Type: Article

References (61)

1. Alonso, J.M., Hirayama, T., Roman, G., Nourizadeh, S. Ecker, J.R. (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science, 284, 2148 2152. (Pubitemid 29297469)
2. Al-Shahrour, F., Minguez, P., Tárraga, J., Medina, I., Alloza, E., Montaner, D. Dopazo, J. (2007) FatiGO+: a functional profiling tool for genomic data. Integration of functional annotation, regulatory motifs and interaction data with microarray experiments. Nucleic Acids Res. 35, W91 W96.
3. Babiychuk, E., Bouvier-Navé, P., Compagnon, V., Suzuki, M., Muranaka, T., Van Montagu, M., Kushnir, S. Schaller, H. (2008) Allelic mutant series reveal distinct functions for Arabidopsis cycloartenol synthase 1 in cell viability and plastid biogenesis. Proc. Natl Acad. Sci. USA, 105, 3163 3168. (Pubitemid 351723685)
4. Benveniste, P. (2004) Biosynthesis and accumulation of sterols. Annu. Rev. Plant Biol. 55, 429 457. (Pubitemid 38940939)
5. Borsani, O., Cuartero, J., Fernandez, J.A., Valpuesta, V. Botella, M.A. (2001) Identification of two loci in tomato reveals distinct mechanisms for salt tolerance. Plant Cell, 13, 873 887. (Pubitemid 32375907)
6. Borsani, O., Cuartero, J., Valpuesta, V. Botella, M.A. (2002) Tomato tos1 mutation identifies a gene essential for osmotic tolerance and abscisic acid sensitivity. Plant J. 32, 905 914. (Pubitemid 36108058)
7. Brady, S.M., Orlando, D.A., Lee, J.Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U. Benfey, P.N. (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 318, 801 806.
8. 2. Ann. Bot. 75, 143 150.
9. Carland, F., Fujioka, S., Takatsuto, S., Yoshida, S. Nelson, T. (2002) The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell, 14, 2045 2058.
10. Carol, R., Takeda, S., Linstead, P., Durrant, M., Kakesova, H., Derbyshire, P., Drea, S., Zarsky, V. Dolan, L. (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature, 438, 1013 1016. (Pubitemid 43093973)
11. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W. Ecker, J. (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell, 89, 1133 1144. (Pubitemid 127678746)
12. Clough, S.J. Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735 743.
13. Clouse, S. (2002) Arabidopsis mutants reveal multiple roles for sterols in plant development. Plant Cell, 14, 1995 2000.
14. Curtis, M.D. Grossniklaus, U. (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462 469. (Pubitemid 37325657)
15. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D., Coutu, J., Shulaev, V., Schlauch, K. Mittler, R. (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell, 17, 268 281. (Pubitemid 41673002)
16. Diener, A., Li, H., Zhou, W., Whoriskey, W., Nes, W. Fink, G. (2000) Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell, 12, 853 870. (Pubitemid 30458033)
17. van Englen, F.A., Molthoff, J.W., Connor, A.J., Nap, J.P., Pereira, A. Stiekema, W.J. (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res. 4, 288 290.
18. Foreman, J., Demidchik, V., Bothwell, J. et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422, 442 446. (Pubitemid 36411398)
19. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R. Jürgens, G. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature, 426, 147 153. (Pubitemid 37442576)
20. Fryer, M.J., Oxborough, K., Mullineaux, P.M. Baker, N.R. (2002) Imaging of photo-oxidative stress responses in leaves. J. Exp. Bot. 53, 1249 1254. (Pubitemid 34544047)
21. Gapper, C. Dolan, L. (2006) Control of plant development by reactive oxygen species. Plant Physiol. 141, 341 345. (Pubitemid 43974525)
22. Guzmán, P. Ecker, J. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell, 2, 513 523. (Pubitemid 120029609)
23. Hartmann, A.M. (1998) Plant sterols and the membrane environment. Trends Plant Sci. 3, 170 175.
24. Hetherington, A.M. Woodward, F.I. (2003) The role of stomata in sensing and driving environmental change. Nature, 424, 901 908. (Pubitemid 37051674)
25. Jang, J., Fujioka, S., Tasaka, M., Seto, H., Takatsuto, S., Ishii, A., Aida, M., Yoshida, S. Sheen, J. (2000) A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev. 14, 1485 1497. (Pubitemid 30421841)
26. 2+ binding motifs. Plant Cell, 10, 255 266.
27. Kim, H., Schaller, H., Goh, C., Kwon, M., Choe, S., An, C., Durst, F., Feldmann, K. Feyereisen, R. (2005) Arabidopsis cyp51 mutant shows postembryonic seedling lethality associated with lack of membrane integrity. Plant Physiol. 138, 2033 2047. (Pubitemid 43733548)
28. Kwak, J.M., Mori, I.C., Pei, Z.M., Leonhardt, N., Torres, M.A., Dangl, J.L., Bloom, R.E., Bodde, S., Jones, J.D. Schroeder, J.I. (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J. 22, 2623 2633. (Pubitemid 36712360)
29. Kwak, J.M., Nguyen, V. Schroeder, J.I. (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol. 141, 323 329. (Pubitemid 43974522)
30. Li, S., Assmann, S. Albert, R. (2006) Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biol. 4, e312.
31. Maere, S., Heymans, K. Kuiper, M. (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics, 21, 3448 3449. (Pubitemid 41222459)
32. Masferrer, A., Arro, M., Manzano, D., Schaller, H., Fernandez-Busquets, X., Moncalean, P., Fernandez, B., Cunillera, N., Boronat, A. Ferrer, A. (2002) Overexpression of Arabidopsis thaliana farnesyl diphosphate synthase (FPS1S) in transgenic Arabidopsis induces a cell death/senescence-like response and reduced cytokinin levels. Plant J. 30, 123 132. (Pubitemid 34536233)
33. Men, S., Boutté, Y., Ikeda, Y., Li, X., Palme, K., Stierhof, Y.D., Hartmann, M.A., Moritz, T. Grebe, M. (2008) Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nature Cell Biol. 10, 237 244. (Pubitemid 351194054)
34. Nieto, B., Forés, O., Arró, M. Ferrer, A. (2009) Arabidopsis 3-hydroxy-3-methylglutaryl-CoA reductase is regulated at the post-translational level in response to alterations of the sphingolipid and the sterol biosynthetic pathways. Phytochemistry, 70, 58 64.
35. O'Brien, M., Chantha, S.C., Rahier, A. Matton, D.P. (2005) Lipid signaling in plants. Cloning and expression analysis of the obtusifoliol 14α-demethylase from Solanum chacoense Bitt., a pollination- and fertilization-induced gene with both obtusifoliol and lanosterol demethylase activity. Plant Physiol. 139, 734 749. (Pubitemid 43907103)
36. Orozco-Cardenas, M. Ryan, C.A. (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl Acad. Sci. USA, 96, 6553 6557. (Pubitemid 29256704)
37. Ortega-Martínez, O., Pernas, M., Carol, R. Dolan, L. (2007) Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science, 317, 507 510. (Pubitemid 47196113)
38. Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klusener, B., Allen, G.J., Grill, E. Schroeder, J.I. (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406, 731 734. (Pubitemid 30671226)
39. Phillips, D., Rasbery, J., Bartel, B. Matsuda, S. (2006) Biosynthetic diversity in plant triterpene cyclization. Curr. Opin. Plant Biol. 9, 305 314.
40. Rasbery, J., Shan, H., Leclair, R., Norman, M., Matsuda, S. Bartel, B. (2007) Arabidopsis thaliana SQUALENE EPOXIDASE 1 is essential for root and seed development. J. Biol. Chem. 282, 17002 17013. (Pubitemid 47093232)
41. Rosado, A., Amaya, I., Valpuesta, V., Cuartero, J., Botella, M. Borsani, O. (2006a) ABA- and ethylene-mediated responses in osmotically stressed tomato are regulated by the TSS2 and TOS1 loci. J. Exp. Bot. 57, 3327 3335. (Pubitemid 44453542)
42. Rosado, A., Schapire, A., Bressan, R., Harfouche, A., Hasegawa, P., Valpuesta, V. Botella, M. (2006b) The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol. 142, 1113 1126. (Pubitemid 44764636)
43. Schaller, H., Grausem, B., Benveniste, P., Chye, M.L., Tan, C.T., Song, Y.H. Chua, N.H. (1995) Expression of the Hevea brasiliensis (H.B.K.) Mull 3-hydroxy-3-methylglutaryl-coenzyme A reductase 1 in tobacco results in sterol overproduction. Plant Physiol. 109, 761 770. (Pubitemid 3009544)
44. Schaller, H. (2003) The role of sterols in plant growth and development. Prog. Lipid Res. 42, 163 175. (Pubitemid 36411691)
45. Schaller, H. (2004) New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiol. Biochem. 42, 465 476. (Pubitemid 38893953)
46. Schrick, K., Mayer, U., Horrichs, A., Kuhnt, C., Bellini, C., Dangl, J., Schmidt, J. Jürgens, G. (2000) FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev. 14, 1471 1484. (Pubitemid 30421840)
47. Schrick, K., Mayer, U., Martin, G., Bellini, C., Kuhnt, C., Schmidt, J. Jürgens, G. (2002) Interactions between sterol biosynthesis genes in embryonic development of Arabidopsis. Plant J. 31, 61 73. (Pubitemid 34801015)
48. Schrick, K., Fujioka, S., Takatsuto, S., Stierhof, Y.D., Stransky, H., Yoshida, S. Jürgens, G. (2004a) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J. 38, 227 243. (Pubitemid 38503725)
49. Schrick, K., Nguyen, D., Karlowski, W. Mayer, K. (2004b) START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 5, R41.
50. Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B. Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498 2504. (Pubitemid 37428274)
51. Souter, M., Topping, J., Pullen, M., Friml, J., Palme, K., Hackett, R., Grierson, D. Lindsey, K. (2002) hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell, 14, 1017 1031. (Pubitemid 34609214)
52. Souter, M.A., Pullen, M.L., Topping, J.F., Zhang, X. Lindsey, K. (2004) Rescue of defective auxin-mediated gene expression and root meristem function by inhibition of ethylene signalling in sterol biosynthesis mutants of Arabidopsis. Planta, 219, 773 783. (Pubitemid 39282941)
53. Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K. Dolan, L. (2008) Local positive feedback regulation determines cell shape in root hair cells. Science, 319, 1241 1244. (Pubitemid 351323019)
54. Torres, M. Dangl, J. (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr. Opin. Plant Biol. 8, 397 403. (Pubitemid 40817382)
55. Torres, M., Jones, J. Dangl, J. (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet. 37, 1130 1134. (Pubitemid 41486668)
56. Torres, M.A., Onouchi, H., Hamada, S., Machida, C., Hammond-Kosack, K.E. Jones, J.D. (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J. 14, 365 370. (Pubitemid 28236000)
57. Ulmasov, T., Murfett, J., Hagen, G. Guilfoyle, T. (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell, 9, 1963 1971. (Pubitemid 28174069)
58. Wentzinger, L., Bach, T. Hartmann, M. (2002) Inhibition of squalene synthase and squalene epoxidase in tobacco cells triggers an up-regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Plant Physiol. 130, 334 346.
59. Willemsen, V., Friml, J., Grebe, M., van den Toorn, A., Palme, K. Scheres, B. (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell, 15, 612 625. (Pubitemid 36339577)
60. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V. Provart, N.J. (2007) An 'electronic fluorescent pictograph' browser for exploring and analyzing large-scale biological data sets. PLoS ONE, 2, e718.
61. Xu, J. Scheres, B. (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell, 17, 525 536. (Pubitemid 41672972)