Contrasted Responses to Root Hypoxia in Tomato Fruit at Two Stages of Development
Tóm tắt
The biochemical consequences of root hypoxia have been documented in many sink organs, but not extensively in fruit. Therefore, in the present study, the response to root hypoxia in tomato fruit (Solanum lycopersicum L.) was investigated at two developmental stages, during the cell division and the cell expansion phases. Our results showed that in dividing fruit, root hypoxia caused an exhaustion of carbon reserves and proteins. However, ammonium and major amino acids (glutamine, asparagine and γ–aminobutyric acid (GABA)) significantly accumulated. In expanding fruit, root hypoxia had no effect on soluble sugar, protein and glutamine contents, whereas starch content was significantly decreased, and asparagine and GABA contents slightly increased. Metabolite contents were well correlated with activities of the corresponding metabolising enzymes. Contrary to nitrogen metabolising enzymes (glutamine synthetase, asparagine synthetase and glutamate decraboxylase), the activities of enzymes involved in sugar metabolism (invertase, sucrose synthase, sucrose phosphate synthase and ADP glucose pyrophosphorylase) were significantly reduced by root hypoxia, in diving fruit. In expanding fruit, only a slight decrease in ADP glucose pyrophosphorylase and an increase in asparagine synthetase and glutamate decarboxylase activities were observed. Taken together, the present data revealed that the effects of root hypoxia are more pronounced in the youngest fruits as it is probably controlled by the relative sink strength of the fruit and by the global disturbance in plant functioning.
Tài liệu tham khảo
Aggarwal PK, Kalra N, Chander S, Pathak H (2006) Info Crop: a dynamic simulation model for the assessment of crop yields, losses due to pests, and environmental impact of agro-ecosystems in tropical environments. I. Model description. Agric Syst 89:1–25
Ahsan N, Lee DG, Lee SH, Kanga KY, Bahka JD, Choi MS, Lee IJ, Renaut J, Lee BH (2007) A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiol Plant 131:555–570
Alonso AP, Vigeolas H, Raymond P, Rolin D, Dieuaide-Noubhani M (2005) A new substrate cycle in plants. Evidence for a high glucose phosphate-to-glucose turnover from in vivo steady-state and pulse labeling experiments with [13 C] glucose and [14 C] glucose. Plant Physiol 138:2220–2232
Alonso AP, Raymond P, Rolin D, Dieuaide-Noubhani M (2007) Substrate cycles in the central metabolism of maize root tips under hypoxia. Phytochem 68:2222–2231
Ammerlaan AWS, Joosten MHAJ, Grange RI (1986) The starch content of tomato leaves grown under glass. Sci Hortic 28:1–9
Armstrong W (1979) Aeration in higher plants. In: Woolhouse HW (ed) Advances in Botanical Research. Academic, London, UK, pp 226–328
Bertin N (1995) Competition for assimilates and fruit position affect fruit set in indeterminate greenhouse tomato. Ann Bot 75:55–65
Bohner J, Bangerth F (1988) Effects of fruit set sequence and defoliation on cell number, cell size and hormone levels of tomato fruit (Lycopersicon esculentum Mill.) within a truss. Plant Growth Regula 7:141–155
Boyer JS (1982) Plant productivity and environment. Sci 218:443–448
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Bray EA, Bailey-Serres J, Weretilnyk E (2001) Responses to abiotic stresses. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologist, Rockville, MD, pp 1158–1203
Brouquisse R, James F, Raymond P, Pradet A (1991) Study of glucose starvation in excised maize root tips. Plant Physiol 96:619–626
Brouquisse R, James F, Raymond P, Pradet A (1992) Asparagine metabolism and nitrogen distribution during protein degradation in sugar-starved maize root tips. Planta 188:384–395
Brouquisse R, Gaudillere JP, Raymond P (1998) Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol 117:1281–1291
Cohen SA, De Antonis KM (1994) Applications of amino acids derivatization with 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate. Analysis of feed grains, intravenous solutions and glycoproteins. J Chromat 661:25–34
Crawford RMM, Brändle R (1996) Oxygen deprivation stress in a changing environment. J Exp Bot 47:145–159
D’Aoust MA, Yelle S, Nguyen-Quoc B (1999) Antisens inhibition of tomato fruit synthase decreases fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11:2407–2418
Delrot S, Atanassova R, Maurousset L (2000) Regulation of sugar, amino acidand peptide plant membrane transporters. Bioch Biophys Acta 1465:281–306
Devaux C, Baldet P, Joubès J, Dieuaide-Noubhani M, Just D, Chevalier C, Raymond P (2003) Physiological, biochemical and molecular analysis of sugar-starvation responses in tomato roots. J Exp Bot 54:1143–1151
Dinar H, Stevens MA (1981) The relationship between starch accumulation and soluble solids contents of tomato fruit. J Am Soc Hort Sci 106:415–418
Farrar JF (1996) Sinks-integral parts of a whole plant. J Exp Bot 47:1273–1279
Geiger DR, Koch KE, Gruissem W (1993) Effect of environmental factors on whole plant assimilate partitioning and associated gene expression. J Exp Bot 47:1229–1238
Gharbi I, Ricard B, Rolin D, Maucourt M, Andrieu MH, Bizid E, Smiti S, Brouquisse R (2007) Effect of hexokinase activity on tomato root metabolism during prolonged hypoxia. Plant Cell Environ 30:508–517
Gillaspy G, Ben-David H, Gruissem W (1993) Fruit: a developmental perspective. Plant Cell 5:1439–1451
Grange RI, Andrews J (1994) Expansion rate of young tomato fruit growing in plants at positive water potential. Plant Cell Environ 17:181–187
Guan HP, Janes HW (1991) Light regulation of sink metabolism in tomato fruit. Plant Physiol 96:916–921
Ho LC (1988) Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Annu Rev Plant Physiol Plant Mol Biol 39:355–378
Horchani F, Aloui A, Brouquisse R, Aschi-Smiti S (2008a) Physiological responses of tomato plants (Solanum lycopersicum) as affected by root hypoxia. J Agron Crop Sci 194:297–303
Horchani F, Gallusci P, Baldet P, Cabasson C, Maucourt M, Rolin D, Aschi-Smiti S, Raymond P (2008b) Prolonged root hypoxia induces ammonium accumulation and decreases the nutritional quality of tomato fruits. J Plant Physiol 165:1352–1359
Horchani F, Khayati H, Raymond P, Brouquisse R, Aschi-Smiti S (2009) Contrasted effects of prolonged root hypoxia on tomato (Solanum lycopersicum) roots and fruits metabolism. J Agron Crop Sci 195:313–318
Horchani F, Aschi-Smiti S, Brouquisse R (2010) Involvement of nitrate reduction in the tolerance of tomato plants to prolonged root hypoxia. Acta Physiol Plant 32:1113–1123
Irving LJ, Sheng YB, Woolley D, Matthew C (2007) Physiological effects of waterlogging on two lucerne varieties grown under glasshouse conditions. J Agron Crop Sci 193:345–356
Jackson MB (2002) Long-distance signalling from roots to shoots assessed: the flooding story. J Exp Bot 53:175–18
Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot 96:501–505
King GA, Woollard DC, Irving DE, Borst WM (1990) Physiological changes in asparagus spear tips after harvest. Physiol Plant 80:393–400
Klieber A, Ratanachinakorn B, Simons DH (1996) Effect of low oxygen and high carbon dioxide on tomato cultivar “Bermuda” fruit physiology and composition. Sci Hort 65:251–261
Koch KE (1996) Carbohydrate modulates gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540
Mazelis M (1980) Amino acid catabolism. In: Stumpf PK, Conn EE (eds) The biochemistry of plants, vol 5. Academic, London, pp 541–567
Moing A, Escobar-Gutierrez A, Gaudillère JP (1994) Modeling carbon export out of mature peach leaves. Plant Physiol 106:591–600
Mustilli AC, Bowler C (1997) Turning in the signals controlling photoregulated gene expression in plants. EMBO J 16:5801–5806
Pezeshki SR (2001) Wetland plant responses to soil flooding. Environ Exp Bot 46:299–312
Rahayu YS, Walch-Liu P, Neumann G, Romheld V, Wiren N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO -3 induced stimulation of leaf growth. J Exp Bot 56:1143–1152
Ricard B, Coué I, Raymond P, Saglio PH, Saint-Ges V, Pradet A (1994) Plant metabolism under hypoxia and anoxia. Plant Physiol Biochem 32:1–10
Ricard B, Aschi-Smiti S, Gharbi I, Brouquisse R (2006) Cellular and molecular mechanisms of plant tolerance to waterlogging. In: Huang B (ed) Plant-Environment Interactions. Taylor and Francis, Boca Raton/London/New York, pp 177–208
Rolin D, Baldet P, Just D, Chevalier C, Biran M, Raymond P (2000) NMR study of low subcellular pH during the development of cherry tomato fruit. Aust J Plant Physiol 27:61–69
Saglio PH, Drew MC, Pradet A (1988) Metabolic acclimation to anoxia induced by low (2–4 kPa partial pressure) oxygen pretreatment (hypoxia) in root tips of Zea mays. Plant Physiol 86:61–66
Sasaki H, Ichimura K, Imada S, Yamaki S (2001) Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings. J Plant Physiol 158:847–852
Satya Narayan V, Nair PM (1990) Metabolism, enzymology and possible roles of 4-aminobutyrate in higher plants. Phytochem 26:367–375
Schaffer AA, Petreikov M (1997) Sucrose-to-starch metabolism in tomato fruit undergoing transient starch accumulation. Plant Physiol 113:739–746
Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot 79:3–20, Suppl. A
Voesenek LACJ, Rijinders JHGM, Peeters AJM, Van de Steeg HM, de Kroon H (2004) Plant hormones regulate fast shoot elongation under water: from genes to communities. Ecol 85:16–27
Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381
Zhang J, Davies WJ (1986) Chemical and hydraulic influences on the stomata of flooded plants. J Exp Bot 37:1479–1491