DISSECTING THE HORMONAL CONTROL OF THE SALT STRESS RESPONSE IN ARABIDOPSIS ROOTS 2

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DISSECTING THE HORMONAL CONTROL OF THE SALT STRESS RESPONSE IN ARABIDOPSIS ROOTS 2

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  Chapter RESULTS AND DISCUSSION 87       4.1 Abstract   High salinity is an important agricultural contaminant that causes damage to the plant However, the distinctive roles of different cell types in the transition process from normal growth to stress acclimation are largely unknown Here, we show that ethylene promotes radial expansion of cortex cells through the canonical ethylene signaling pathway, while its precursor ACC may have an ethylene-independent function of inhibiting cell elongation during salt stress By using mutants that have radial patterning defects, we show that salt-mediated induction of ethylene biosynthetic pathway members at the transcriptional level depends on the endodermis In order to find the components that work downstream of ethylene in regulating salt-mediated cell swelling, we performed microarray experiments with ethylene signaling mutants at early stages of salt stress Bioinformatic analysis revealed cell-type specificity in the expression pattern of the downstream targets of ethylene during salt stress, indicating the cell-type specific function of ethylene in regulating the salt response Further, we demonstrated that local synthesis of auxin in the early elongation zone serves as a downstream component of ethylene signaling during salt stress Based on these observations, we that ethylene promotes salt-mediated cortical cell swelling through auxin signaling in an endodermisdependent manner           88       4.2 Introduction   Plants, through intricate compositions of cell and tissue types, are good planners In favorable habitats, they plan their lives in a simple and effective way However, when they are facing stressful environments, they need to quickly coordinate their different tissue layers, conduct complex regulation to change their developmental and physiological plane to adapt to such environments Salt stress is one of the most common environmental stresses It creates both osmotic and ionic stress to affect plant growth Decades of research into the effects of salinity on plant physiology and development have generated a wealth of information However, the distinctive roles of different cell types in the transition process from normal growth to stress adaptation are largely unknown In this study, we used a particular salt-sensitive plant, Arabidopsis thaliana, focusing on one environmental stress, high salinity, in order to understand how plants make this transition and how different cell types contribute to this process     High salinity has complex effects on root physiology These effects are mainly caused by both osmotic stress and ionic stress When the rhizosphere soil is contaminated with toxic soluble molecules, like NaCl, the water potential of the soil become lower, making it more difficult for plants to take up water from the environment When the cells are suffering from dehydration, the turgor pressure of the cells against their cell walls is reduced, which can reduce the rigidity of plants and make them more vulnerable to wounding Along with water deprivation becoming more and more severe, many biological processes, such as photosynthesis, are disrupted (Allen et al., 2001) 89       Furthermore, due to their similar chemical properties, the high amount of Na+ will break the K+/Na+ balance, leading to K+ deprivation by engrossing ion channels, which are normally used to transport K+ into the cell (Rubio et al., 1995) It has been shown that K+ is crucial for the activity of many enzymes; lack of K+ will largely affect plant development and growth (Shabala et al., 2008)     When exposed to salt stress, the Arabidopsis root undergoes dramatic morphological changes, which include the inhibition of primary root elongation, reduction of meristem size, and inhibition of lateral root formation in a dosage-dependent manner (Burssens et al., 2000; West et al., 2004; Wang et al., 2009) Besides generally affecting root growth, high salinity also leas to cell type–specific morphological changes For example, the epidermis shows an immediate suppression of hair outgrowth, whereas the cortex undergoes radial expansion, which may act to prevent additional uptake of salt into the vasculature (Burssens et al., 2000; Dinneny et al., 2008; Dinneny, 2009)     It has been shown that high salinity increases ethylene production (Achard et al., 2006) Interestingly, like high salinity, ethylene and its precursor ACC can also inhibit root cell elongation and promote cell radial expansion Previous studies have shown that ethylene regulates root growth, especially through the inhibition of cell elongation This occurs largely through the production and transportation of another important phytohormone, auxin (Ruzicka et al., 2007; Swarup et al., 2007) However, there is a report showing that the canonical ethylene signaling pathway may not be necessary for promoting radial cell 90       expansion This report suggested that ACS5, a member of ACS family, can regulate radial cell expansion by directly binding to two leucine-rich repeat receptor kinases, FEI1 and FEI2 (Xu et al., 2008)   In this study, by focusing on one particular morphological change, cortical cell swelling during salt stress, we provided a detailed analysis on the distinctive functions of different cell types in this process We show that the endodermis is important for the promotion of ethylene production by salt The epidermis is crucial for the activation of auxin biosynthesis by the canonical ethylene signaling pathway in order to promote cell expansion during salt stress We also show that ethylene signaling target genes that are enriched in cortex that may be directly involved in regulating salt-mediated cell expansion                   91       4.3 Results   4.3.1 During salt stress, Arabidopsis roots undergo dramatic morphological changes   As shown previously, Arabidopsis roots gradually stop growing and stay in a quiescent state for approximately four hours after salt treatment With confocal microscopy, we were not able to observe any significant morphological changes in the time point before four hours (Figure 16A, B, and C) In the quiescent stage, cells in the outer tissue layers (including the epidermis, cortex and endodermis), exhibited radial expansion in the early elongation zone The early elongation zone refers to the boundary of the meristematic and elongation zones in roots Among those layers, the cortex showed the most dramatic cell shape change (Figure 16A) Along with radial cell expansion, the roots bend at the elongation zone and grew into other directions (Figure 16A, C) Correlated with the event of roots recovering growth rates in the homeostasis phase, the inhibition of cell elongation was partially released (Figure 16A) Due to the rigidity of plant cell walls, all of these morphological changes are irreversible after the cells enter into the maturation zone, allowing us to observe them after they occur (Figure 17A) Among these morphological changes, the inhibition of cortical cell elongation and radial expansion were very consistent, easy to observe with microscopy, and quantifiable Figure 17 shows quantification of cortical cell length (Figure 17B) and cell width (Figure 17C) along the longitudinal axis from the transfer point to the root tip From the transfer point, the first four cells gradually become shorter, while the cell width of the first four cells largely remained unchanged (Figure 17B and C) This indicates that the inhibition of cell elongation may happen earlier than radial expansion during salt stress When comparing 92       Figure 17B to Figure 3B, we found the primary root growth pattern and the profile of cell length shared a certain level of similarity This suggests that inhibition of cell elongation contributes to inhibition of growth during salt stress   We next focused on cortical cell shape changes to understand the roles of different cell types in acclimation during salt stress To simplify the analysis, we used the ratio between cell width and cell length (Figure 17D) of the 10 cells that showed the most dramatic cell shape changes (Figure 17B and C, marked in grey) to represent the cortical cell shape changes   93       Figure 16 Arabidopsis roots undergo drastic cell shape changes during salt stress A) Plasma membrane marker WAVE131: YFP showed morphological changes in Arabidopsis roots at different time points during salt stress Yellow arrows point at the first cell undergoing ectopic radial expansion Noted after hours of salt treatment, the cells in the early elongation zone started to expand radially Scale bar= 200 µm B) Cortical cell length from quiescent center to elongation zone 94       C) Cortical cell width from quiescent center to elongation zone Cell width increased in the early elongation zone after to hours of salt treatment Figure 17 Cell shape change is irreversible due to the rigid plant cell walls A) Salt-mediated cortical cell swelling is easy to observe under confocal microscopy FM 4-64 was used as counterstain to highlight the cell shape B) Quantification of cortical cell length from the transfer point Grey area highlights the cells that are most strongly affected by salt 95       C) Quantification of cortical cell width from the transfer point Grey area highlights the cells that are most strongly affected by salt D) Phenotype was presented as the ratio between cell width and cell length of those cells that show most dramatic changes Error=SEM 4.3.2 Ethylene is involved in the morphological changes of the roots during salt stress   Ethylene and its precursor ACC have been described to cause an increase in the width of the root (Smalle and Van Der Straeten, 1997) and a rapid decrease in cell elongation (Lee et al., 2001) To test if the ethylene precursor ACC can cause morphological changes in cortex cells similar to those caused by salt treatment, we treated Arabidopsis wild type Columbia-0 (Col-0) seedlings with 140mM NaCl and different concentrations of ACC As shown in Figure 18A, ACC can cause a concentration-dependent effect on cortical cell swelling: from 0.5 µM to 1.3 µM, ACC can cause very similar cell shape changes with 140mM NaCl As mentioned before, high salinity elevates ethylene production (Achard et al., 2006) It is possible that the cortical cell swelling under high salinity is due to elevated ethylene production   To test this hypothesis, we treated Col-0 with amino oxyacetic acid (AOA) in the presence or absence of 140 mM NaCl using methods similar to the previous experiment AOA inhibits enzymes that require pyroxidal phosphate, including ACS, the key enzyme for ethylene biosynthesis The results are shown in Figure 18B Compared to seedlings under salt treatment alone, there was a significant reduction in cell swelling in the seedlings that were treated with both salt and AOA Together with the results from the 96       He, J.X., Gendron, J.M., Sun, Y., Gampala, S.S., Gendron, N., Sun, C.Q., and Wang, Z.Y (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses Science 307, 1634-1638 Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T., and Benfey, P.N (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling Cell 101, 555-567 Iraki NM, Bressan RA, Hasegawa PM, Carpita NC (1989) Alteration of the physical and chemical structure of the primary cell wall of growth-limited plant cellsadapted to osmotic stress Plant Physiol 91(1):39-47 Irizarry, R.A., Wu, Z., and Jaffee, H.A (2006) Comparison of Affymetrix GeneChip expression measures Bioinformatics 22, 789-794 Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding Plant Cell 12(9):1667-78 Ivashuta S, Liu J, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calciumdependent protein kinase involved in Medicago truncatula root development Plant Cell 17(11):2911-21 Joo S, Liu Y, Lueth A, Zhang S (2008) MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway Plant J 54: 129-40 Karahara, I., Ikeda, A., Kondo, T., and Uetake, Y (2004) Development of the Casparian strip in primary roots of maize under salt stress Planta 219, 41-47 146       Kasuga M, Liu Q, Miura S, Yamaguchi- Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stressinducible transcription factor Nat Biotechnol 17:287–91 Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J., and Harter, K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses Plant J 50, 347-363 Kim, C.Y., Liu, Y., Thorne, E.T., Yang, H., Fukushige, H., Gassmann, W., Hildebrand, D., Sharp, R.E., and Zhang, S (2003) Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants Plant Cell 15, 2707-2718 Kim SK, Sohn EY, Joo GJ, Lee IJ (2009) Influence of jasmonic acid on endogenous gibberellin and abscisic acid in salt-stressed chard plant J Environ Biol 30(3):333-8 Kim, T.H., Hauser, F., Ha, T., Xue, S., Bohmer, M., Nishimura, N., Munemasa, S., Hubbard, K., Peine, N., Lee, B.H., Lee, S., Robert, N., Parker, J.E., and Schroeder, J.I (2011) Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway Curr Biol 21, 990-997 Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H (2010) Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation Plant J 64,140-50 Kim BG, Waadt R, Cheong YH, Pandey GK, Dominguez-Solis JR, Schultke S, Lee SC, Kudla J, Luan S (2007) The calcium sensor CBL10 mediates salt tolerance by regulating ion homeostasis in Arabidopsis Plant J, 52, 473-484 147       Koizumi, Koji, Tomomi Hayashi, Shuang Wu, Kimberly L Gallagher (2012) "The SHORT-ROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue." PANS 109, 13010-13015 Kroeger JH, Zerzour R, Geitmann A (2011) Regulator or Driving Force? The Role of Turgor Pressure in Oscillatory Plant Cell Growth PLoS ONE 6(4):e18549 doi:10.1371/journal.pone.0018549 Kuhn, J M., Boisson-Dernier, A., Dizon, M B., Maktabi, M H and Schroeder, J I (2006) 'The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA', Plant Physiol 140(1): 127-139 Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y., and Nambara, E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8'-hydroxylases: key enzymes in ABA catabolism EMBO J 23, 1647-1656 Kurth E, Cramer GR, Läuchli A, Epstein E (1986) Effects of NaCl and CaCl2 on Cell Enlargement and Cell Production in Cotton Roots Plant Physiol 82(4):1102-6 Kroeger JH, Zerzour R, Geitmann A (2011) Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth PLoS One 6(4):e18549 doi: 10.1371/journal.pone.0018549 Lei, G., Shen, M., Li, Z.G., Zhang, B., Duan, K.X., Wang, N., Cao, Y.R., Zhang, W.K., Ma, B., Ling, H.Q., Chen, S.Y., and Zhang, J.S.( 2011) EIN2 regulates salt 148       stress response and interacts with a MA3 domain-containing protein ECIP1 in Arabidopsis Plant Cell Environ 34(10):1678-92 Lee, J.Y., Colinas, J., Wang, J.Y., Mace, D., Ohler, U., and Benfey, P.N (2006) Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots Proc Natl Acad Sci USA 103, 6055-6060 Lee, M.M., and Schiefelbein, J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning Cell 99, 473483 Leek, J.T., Monsen, E., Dabney, A.R., and Storey, J.D (2006) EDGE: extraction and analysis of differential gene expression Bioinformatics 22, 507-508 Levesque M.P., Vernoux T., Busch W., Cui H., Wang J.Y., Blilou I., Hassan H., Nakajima K., Matsumoto N., Lohmann J.U., Scheres B., Benfey P.N (2006) Wholegenome analysis of the SHORT-ROOT developmental pathway in Arabidopsis PLoS Biol 4: e143 Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K(+) channel for low-K response in Arabidopsis.Proc Natl Acad Sci U S A 103(33):12625-30 Lovegrove, A., Barratt, D H., Beale, M H and Hooley, R (1998) Gibberellin photoaffinity labelling of two polypeptides in plant plasma membranes Plant J 15, 311320 Lux, A., Morita, S., Abe, J., and Ito, K (2005) An improved method for clearing and staining free-hand sections and whole-mount samples Annals of botany 96, 989-996 149       Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis Plant J 27, 325-333 Luan, S., Lan, W and Chul Lee, S (2009) 'Potassium nutrition, sodium toxicity, and calcium signaling: connections through the CBL-CIPK network', Curr Opin Plant Biol 12(3): 339-346 Iyer-Pascuzzi, A.S., Jackson, T., Cui, H., Petricka, J.J., Busch, W., Tsukagoshi, H., and Benfey, P.N (2011) Cell identity regulators link development and stress responses in the Arabidopsis root Dev Cell 21, 770-782 Ma, S., Gong, Q., and Bohnert, H.J (2006) Dissecting salt stress pathways J Exp Bot 57, 1097-1107 Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., and Grill, E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors Science 324, 1064-1068 Miller, N.D., Parks, B.M., and Spalding, E.P (2007) Computer-vision analysis of seedling responses to light and gravity Plant J 52, 374-381 Mizoguchi, M., Umezawa, T., Nakashima, K., Kidokoro, S., Takasaki, H., Fujita, Y., Yamaguchi-Shinozaki, K and Shinozaki, K (2010) 'Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression', Plant Cell Physio 51(5): 842-847 Munns, R (2002) Comparative physiology of salt and water stress Plant Cell Environ 25, 239-250 150       Munns R, Tester M (2008) Mechanisms of salinity tolerance Annu Rev Plant Biol.59:651-81 doi: 10.1146/annurev.arplant.59.032607.092911 Munns, R and Passioura, J (1984) 'Effect of prolonged exposure to NaCl on the osmotic pressure of leaf xylem sap from intact, transpiring barley plants', Functional Plant Biology 11(6): 497-507 Munns R., Tonnet M.L., Shennan C & Gardner P.A (1988) Effect of high external NaCl concentrations on ion transport within the shoot of Lupinus albus II Ions in phloem sap Plant, Cell and Environment 11, 291–300 Munns R & Sharp R.E (1993) Involvement of abscisic acid in controlling plant growth in soils of low water potential Australian Journal of Plant Physiology 20, 425–437 Munns R & Passioura J.B (1984) Effect of prolonged exposure to NaCl on the osmotic pressure of leaf xylem sap from intact, transpiring barley plants Australian Journal of Plant Physiology 11, 497–507 Munns R, Passioura JB, Guo J, Chazen O, Cramer GR (2000) Water relations and leaf expansion: importance of time scale J Exp Bot 51(350):1495-504 Mustroph, A., Juntawong, P., and Bailey-Serres, J (2009) Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods Methods Mol Biol 553, 109-126 Mönke G, Seifert M, Keilwagen J, Mohr M, Grosse I, Hähnel U, Junker A, Weisshaar B, Conrad U, Bäumlein H, Altschmied L (2012) Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon Nucleic Acids Res 40(17):8240-54 151       Naseer, S., Lee, Y., Lapierre, C., Franke, R., Nawrath, C., and Geldner, N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin Proc Natl Acad Sci USA 109, 10101-10106 Nawy, T., Lee, J.Y., Colinas, J., Wang, J.Y., Thongrod, S.C., Malamy, J.E., Birnbaum, K., and Benfey, P.N (2005) Transcriptional profile of the Arabidopsis root quiescent center Plant Cell 17, 1908-1925 Nemhauser, J.L., Hong, F., and Chory, J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses Cell 126, 467-475 Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Yoshida, S., Yuan, H., Feldmann, K.A., and Tax, F.E (1999) Brassinosteroid-insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids Plant Physiol 121, 743-752 Oh, E., Zhu, J.Y., and Wang, Z.Y (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses Nat Cell Biol 14, 802-809 Parcy F, Valon C, Kohara A, Miséra S, Giraudat J (1997) The ABSCISIC ACIDlNSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 Loci Act in Concert to Control Multiple Aspects of Arabidopsis Seed Development Plant Cell 9(8):1265-77 Pandey GK, Cheong YH, Kim KN, Grant JJ, Li L, Hung W, D'Angelo C, Weinl S, Kudla J, Luan S (2004) The calcium sensor calcineurin B-like modulates abscisic acid sensitivity and biosynthesis inArabidopsis Plant Cell 16(7):1912-24 Park, S.Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.F., Alfred, S.E., Bonetta, D., Finkelstein, R., Provart, N.J., Desveaux, D., Rodríguez, P.L., McCourt, P., Zhu, J.K., Schroeder, J.I., 152       Volkman, B.F., and Cutler, S.R (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins Science 324, 1068-1071 Passioura, J.B., and Munns, R (2000) Rapid environmental changes that affect leaf water status induce transient surges and pauses in leaf expansion rate Aust J Plant Physiol 27, 941-948 Petersson, S.V., Johansson, A.I., Kowalczyk, M., Makoveychuk, A., Wang, J.Y., Moritz, T., Grebe, M., Benfey, P.N., Sandberg, G., and Ljung, K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cellspecific analysis of IAA distribution and synthesis Plant Cell 21, 1659-1668 Petricka, J.J., Schauer, M.A., Megraw, M., Breakfield, N.W., Thompson, J.W., Georgiev, S., Soderblom, E.J., Ohler, U., Moseley, M.A., Grossniklaus, U., and Benfey, P.N (2012) The protein expression landscape of the Arabidopsis root Proc Natl Acad Sci USA 109: 6811–6818 Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress Plant Cell 19(4):1415-31 Rademacher, W (2000) Growth retardants: Effects on gibberellin biosynthesis and other metabolic pathways Annu Rev Plant Physiol Plant Mol Biol 51, 501-531 Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signaling Trends Plant Sci 15 395–401 Reddy, G.V., Gordon, S.P., and Meyerowitz, E.M (2007) Unravelling developmental dynamics: transient intervention and live imaging in plants Nature 8, 491-501 153       Rhodes, D., and Hanson, A D (1993) Quaternary ammonium and tertiary sulfonium compounds in higher-plants Annu Rev Plant Physiol Plant Mol Biol 44, 357–384 Rodríguez, H.G., Roberts, J., Jordan, W.R., and Drew, M.C (1997) Growth, water relations, and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress Plant Physiol 113, 881-893 Roppolo, D., De Rybel, B., Tendon, V.D., Pfister, A., Alassimone, J., Vermeer, J.E., Yamazaki, M., Stierhof, Y.D., Beeckman, T., and Geldner, N (2011) A novel protein family mediates Casparian strip formation in the endodermis Nature 473, 380-383 Rogers, E.D., Jackson, T., Moussaieff, A., Aharoni, A., and Benfey, P.N (2012) Cell type-specific transcriptional profiling: implications for metabolite profiling Plant J 70, 517 Rubio, F., Gassmann, W and Schroeder, J I (1995) 'Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance', Science 270(5242): 1660-1663 Ruzicka, K., Ljung, K., Vanneste, S., Podhorska, R., Beeckman, T., Friml, J., and Benkova, E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution Plant Cell 19, 2197-2212 Sabatini, S., Heidstra, R., Wildwater, M., and Scheres, B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem Genes Dev 17, 354-358 Saito, S., Hirai, N., Matsumoto, C., Ohigashi, H., Ohta, D., Sakata, K., and Mizutani, M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8'-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid Plant Physiol 134, 1439-1449 154       Schaller, G.E., and Kieber, J.J (2002) Ethylene The Arabidopsis Book 1:e0071 doi:10.1199/tab.0071 Scheres, B., Benfey, P., Dolan, L (2002) Root Development The Arabidopsis Book 1:e0101 doi:10.1199/tab.0101 Shabala, S., and Cuin, T.A (2008) Potassium transport and plant salt tolerance Physiol Plant 133, 651-669 Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks Genome Res 13, 2498-2504 Sharp, R.E., and LeNoble, M.E (2002) ABA, ethylene and the control of shoot and root growth under water stress J Exp Bot 53, 33-37 Sharp, R.E., LeNoble, M.E., Else, M.A., Thorne, E.T., and Gherardi, F (2000) Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: evidence for an interaction with ethylene J Exp Bot 51, 1575-1584 Shi, H., Quintero, F.J., Pardo, J.M., and Zhu, J.K (2002) The putative plasmamembrane Na+/H+ antiporter SOS1 controls long distance Na+ transport in plants Plant Cell 14, 465–477 Skirycz, A., De Bodt, S., Obata, T., De Clercq, I., Claeys, H., De Rycke, R., Andriankaja, M., van Aken, O., van Breusegem, F., Fernie, A.R., and Inze, D (2010) Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress Plant Physiol 152, 226-244 Skirycz, A., Claeys, H., De Bodt, S., Oikawa, A., Shinoda, S., Andriankaja, M., Maleux, K., Eloy, N.B., Coppens, F., Yoo, S.D., Saito, K., and Inze, D (2011) Pause155       and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest Plant Cell 23, 18761888 Smyth, G.K (2005) Limma: linear models for microarray data In Bioinformatics and Computational Biology Solutions Using R and Bioconductor, R Gentleman, V Carey, S Dudoit, R Irizarry, and W Huber, eds (New York: Springer), pp 397-420 Sozzani, R., Cui, H., Moreno-Risueno, M.A., Busch, W., Van Norman, J.M., Vernoux, T., Brady, S.M., Dewitte, W., Murray, J.A., and Benfey, P.N (2010) Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth Nature 466, 128-132 Spollen, W.G., LeNoble, M.E., Samuels, T.D., Bernstein, N., and Sharp, R.E (2000) Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production Plant Physiol 122, 967-976 Stepanova, A.N., and Alonso, J.M (2005) Arabidopsis ethylene signaling pathway Sci STKE 2005, cm4 Storey, J.D., and Tibshirani, R (2003) Statistical significance for genomewide studies Proc Natl Acad Sci USA 100, 9440-9445 Storey, J.D., Xiao, W., Leek, J.T., Tompkins, R.G., and Davis, R.W (2005) Significance analysis of time course microarray experiments Proc Natl Acad Sci USA 102, 12837-12842 Sun, Y., Fan, X.Y., Cao, D.M., Tang, W., He, K., Zhu, J.Y., He, J.X., Bai, M.Y., Zhu, S., Oh, E., Patil, S., Kim, T.W., Ji, H., Wong, W.H., Rhee, S.Y., and Wang, Z.Y 156       (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis Dev Cell 19, 765-777 Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G.T., Sandberg, G., Bhalerao, R., Ljung, K., and Bennett, M.J (2007) Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation Plant Cell 19, 2186-2196 Székely G, Abrahám E, Cséplo A, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008 ) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis Plant J 53(1):11-28 Tan, B.C., Joseph, L.M., Deng, W.T., Liu, L., Li, Q.B., Cline, K., and McCarty, D.R (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family Plant J 35, 44-56 Tsuchisaka, A., and Theologis, A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members Plant Physiol 136, 2982-3000 Tsuchisaka A, Yu GX, Jin HL, Alonso JM, Ecker JR, Zhang XM, Gao S, Theologis A (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana Genetics 183, 979– 1003 Tsukagoshi, H., Busch, W., and Benfey, P.N (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root Cell 143, 606-616 157       Tyler, L., Thomas, S.G., Hu, J., Dill, A., Alonso, J.M., Ecker, J.R., and Sun, T.P (2004) Della proteins and gibberellin-regulated seed germination and floral development in Arabidopsis Plant Physiol 135, 1008-1019 Ubeda-Tomás, S., Swarup, R., Coates, J., Swarup, K., Laplaze, L., Beemster, G T., Hedden, P., Bhalerao, R and Bennett, M J (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis Nat Cell Biol 10, 625-628 Wang, Z.Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T., and Chory, J (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis Dev Cell 2, 505-513 Wang, Y., Li, K., and Li, X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana J Plant Physiol 166, 1637-1645 Wee, C.W., and Dinneny, J.R (2010) Tools for high-spatial and temporal-resolution analysis of environmental responses in plants Biotechnol Lett 32, 1361-1371 West, G., Inze, D., and Beemster, G.T (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress Plant Physiol 135, 1050-1058 Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., and Provart, N.J (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets PLoS One 2, e718 Wu, G., Cameron, J.N., Ljung, K., and Spalding, E.P (2010) A role for ABCB19mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome and phytochrome B Plant J 62, 179-191 158       Xi, W., Liu, C., Hou, X., and Yu, H (2010) MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis Plant Cell 22, 1733-1748 Xiong, L., Zhu, J (2002) Salt Tolerance.The Arabidopsis Book 1: e0048 doi:10.1199/tab.0048 Xiong L, Lee H, Ishitani M, Zhu JK (2002) Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis J Biol Chem 277:8588–96 Xu, S.L., Rahman, A., Baskin, T.I., and Kieber, J.J (2008) Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis Plant Cell 20, 3065-3079 Yamaguchi S (2008) Gibberellin metabolism and its regulation Annu Rev Plant Biol 59:225-51 doi: 10.1146/annurev.arplant.59.032607.092804 Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional Regulatory Networks in Cellular Responses and Tolerance to Dehydration and Cold Stresses Annu Rev Plant Biol 57:781-803 Yoo, S.D., Cho, Y., and Sheen, J (2009) Emerging connections in the ethylene signaling network Trends Plant Sci 14, 270-279 Zhang X, Garreton V, Chua NH (2005 ) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation Genes Dev Jul 1;19(13):1532-43 Zhao B, Li J (2012) Regulation of brassinosteroid biosynthesis and inactivation J Integr Plant Biol Oct;54(10):746-59 doi: 10.1111/j.1744-7909.2012.01168.x 159       Zhu, J.K (2002) Salt and drought stress signal transduction in plants Annu Rev Plant Biol 53, 247-273 Zhu, J K., Hasegawa, P M., Bressan, R A and Bohnert, P H J (1997) 'Molecular aspects of osmotic stress in plants', Critical Rev Plant Sciences 16(3): 253-277 Zhu JY, Sae-Seaw J, Wang ZY (2013) Brassinosteroid signalling Development 140(8):1615-20 doi: 10.1242/dev.060590 160     ... specificity in the expression pattern of the downstream targets of ethylene during salt stress, indicating the cell-type specific function of ethylene in regulating the salt response Further, we... the GFP signaling is very stable in Pro35S::EIN3:GFP in the first hours( Figure 25 B) Therefore, the transient accumulation of EIN3-GFP is not due to the stability feature of the protein but the. .. positive regulator in cell elongation during salt stress 122       Figure 29 Auxin signaling is involved in regulating salt- mediated cortical cell swelling downstream of ethylene signaling pathway

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