Comparative responses to water deficit stress and subsequent recovery in the cultivated beet Beta vulgaris and its wild relative B. macrocarpa
Inès Slama A C , Asma Jdey A , Aida Rouached A B , Ons Talbi A , Ahmed Debez A , Tahar Ghnaya A , Mohamed Anis Limami B and Chedly Abdelly A
+ Author Affiliations
- Author Affiliations
A Laboratoire des Plantes Extrêmophiles, BP 901, Centre de Biotechnologie, Technopole de Borj Cédria, Hammam-Lif 2050, Tunisia.
B University of Angers, UMR 1345 Research Institute of Horticulture and Seeds (INRA, Agrocampus-Ouest, University of Angers), SFR 4207 Quasav, 2 Bd Lavoisier, 49045 Angers Cedex, France.
C Corresponding author. Email: slama_ines@hotmail.fr
Crop and Pasture Science 67(5) 553-562 https://doi.org/10.1071/CP15145
Submitted: 11 May 2015 Accepted: 16 December 2015 Published: 5 April 2016
Abstract
The effects of water deficit stress and recovery on growth, photosynthesis, physiological and biochemical parameters were investigated in the cultivated Beta vulgaris and in two Tunisian provenances (Soliman and Enfidha) of its wild relative B. macrocarpa. Seedlings were cultivated for 4 weeks under optimal or limiting water supply (respectively, 100% and 25% of field capacity, FC). After 2 weeks of treatment, a lot of stressed plants were rehydrated to 100% FC. In the Control, B. vulgaris was more productive than B. macrocarpa, whereas Enfidha provenance showed the highest biomass production (1.6- and 3-fold compared with B. vulgaris and Soliman, respectively), under water deficit stress. A partial re-establishment of growth occurred in both species upon recovery at 100% FC. The sensitivity of B. vulgaris and Soliman provenance to drought was associated with the disturbance of leaf water status and the sharp decrease in net CO2 assimilation (–66% and –82% as compared with the Control, respectively). On the contrary, the better behaviour of Enfidha provenance was related to its better photosynthetic capacity and leaf relative water content, along with a higher accumulation of amino acids (proline, glycine, and glutamine) implied in the osmotic adjustment. Leaf hexose concentration increased significantly under drought stress in both species whereas leaf sucrose concentration declined only in drought-stressed B. vulgaris and Soliman provenance. Leaf glutamate dehydrogenase activity increased under water deficit in both species despite to a higher extent in B. vulgaris. As glutamate dehydrogenase is implied in catabolism of glutamate to oxoglutarate, it might contribute to provide stressed plants with carbon skeletons.
Enfidha provenance of the spontaneous species B. macrocarpa could be used in the marginal arid ecosystems in order to limit the deficit in fodder and to improve the pastoral value of these regions. In addition, this species could serve as a source of genes for genetic improvement to water deficit stress.
Additional keywords: amino acid, nitrogen metabolism, photosynthesis, soluble sugars, water statue.
References
Abdelly C (1997) Mécanismes d’une association de Luzernes spontanées et de halophytes pérennes en bordure de sebkha. Thèse de Doctorat, Faculty of Sciences of Tunis, Tunisia.Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptation to environmental stresses. The Plant Cell 7, 1099–1111.
| Adaptation to environmental stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1Sgt7Y%3D&md5=878e6e539d592b1562a5451d3ec87691CAS | 12242400PubMed |
Bouyoucos (1983) Les proprieties physiques du sol dependent de sa texture et de sa structure. In ‘Les Bases De La Production Végétale. Tome 1. Collection Science et Technique agricoles’. (Ed. D Soltner) pp. 67–87.
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=372a40a9e1124651656a9b395465700bCAS | 942051PubMed |
Chaves MM, Pereira JS, Maroco J, Rodrigues ML, Ricardo CPP, Osório ML, Carvalho I, Faria T, Pinheiro C (2002) How plants cope with water stress in the field: photosynthesis and growth. Annals of Botany 89, 907–916.
| How plants cope with water stress in the field: photosynthesis and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVeitb4%3D&md5=234ebee4c386f7c3a3772d25fc9fa3deCAS | 12102516PubMed |
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Science 135, 1–9.
| Antioxidant responses of rice seedlings to salinity stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkslGjtr0%3D&md5=72d0bb57313e2d833e419377db546345CAS |
Dubey RS (1994) Protein synthesis by plants under stressful conditions. In ‘Hand book of plant and crop stress’. (Ed. Mohammad Pessarkli) pp. 277–299. (Marcel Decker Inc.: New York)
Glévarec G, Bouton S, Jaspard E, Riou MT, Cliquet JB, Suzuki A, Limami AM (2004) Respective roles of the glutamine synthetase/glutamate synthase cycle and glutamate dehydrogenase in ammonium and amino acid metabolism during germination and post-germination growth in the model legume Medicago truncatula. Planta 219, 286–297.
| Respective roles of the glutamine synthetase/glutamate synthase cycle and glutamate dehydrogenase in ammonium and amino acid metabolism during germination and post-germination growth in the model legume Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 14991406PubMed |
Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiology 99, 1443–1448.
| Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtV2jt7o%3D&md5=d68e3b46fc8b5b1aaccae575fd225ad3CAS | 16669056PubMed |
Hessini K, Ghandour M, Albouchi A, Soltani A, Koyro HW, Abdelly C (2008) Biomass production, photosynthesis, and leaf water relations of Spartina alterniflora under moderate water stress. Journal of Plant Research 121, 311–318.
| Biomass production, photosynthesis, and leaf water relations of Spartina alterniflora under moderate water stress.Crossref | GoogleScholarGoogle Scholar | 18389173PubMed |
Hessini K, Lachaal M, Cruz C, Soltani A (2009) Role of ammonium to limit nitrate accumulation and to increase water economy in Wild Swiss Chard. Journal of Plant Nutrition 32, 821–836.
| Role of ammonium to limit nitrate accumulation and to increase water economy in Wild Swiss Chard.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVCltrw%3D&md5=270c2e7c711d54ea019ead0eea9c3875CAS |
Huber SC (1989) Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiology 91, 656–662.
| Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXks1Kk&md5=6c1b7b46f451c88929c5de15b9137998CAS | 16667083PubMed |
Huber SC, Rogers HH, Mowry FL (1984) Effects of water stress on photosynthesis and carbon partitioning in soybean (Glycine max [L.] Merr.) plants grown in the field at different CO2 levels. Plant Physiology 76, 244–249.
| Effects of water stress on photosynthesis and carbon partitioning in soybean (Glycine max [L.] Merr.) plants grown in the field at different CO2 levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXls1Ontb0%3D&md5=2e73740fd00f8f626d2c332c9c6447c9CAS | 16663807PubMed |
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiology 136, 4159–4168.
| Exploring the temperature-stress metabolome of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVakug%3D%3D&md5=b696428a530567d8c1088f4bbcc1dc94CAS | 15557093PubMed |
Keller F, Ludlow MM (1993) Carbohydrate metabolism in drought-stressed leaves of pigeonpea (Cajanus cajan). Journal of Experimental Botany 44, 1351–1359.
| Carbohydrate metabolism in drought-stressed leaves of pigeonpea (Cajanus cajan).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVGksL4%3D&md5=2eaa4274efefb30abf504c470290e482CAS |
Kenis JD, Rouby MB, Edelman MO, Silvente ST (1994) Inhibition of nitrate reductase by water stress and oxygen in detached oat leaves: a possible mechanism of action. Journal of Plant Physiology 144, 735–739.
| Inhibition of nitrate reductase by water stress and oxygen in detached oat leaves: a possible mechanism of action.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisFKnsLs%3D&md5=7f33aef135ee07b3820b741b6ed8ead8CAS |
Kim JY, Mahe A, Brangeon J, Prioul JL (2000) A maize vacuolar invertase, IVR2, is induced by water stress. Organ/tissue specificity and diurnal modulation of expression. Plant Physiology 124, 71–84.
| A maize vacuolar invertase, IVR2, is induced by water stress. Organ/tissue specificity and diurnal modulation of expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVGhtro%3D&md5=2cd89bb61036dcc374b0c430ddba3dacCAS | 10982423PubMed |
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. Journal of Experimental Botany 63, 1593–1608.
| Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlKhs7w%3D&md5=0ef1754c537f422c238cb9109271a1b7CAS | 22291134PubMed |
Larcher W (2003) ‘Physiological plant ecology.’ 4th edn. (Springer Verlag: Berlin, Heidelberg, New York)
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell & Environment 25, 275–294.
| Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakur0%3D&md5=21b4e96614e6d6aff734b3f0b487f572CAS |
Lugan R, Niogret MF, Leport L, Guegan JP, Larher FR, Savoure A, Kopka J, Bouchereau A (2010) Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte. The Plant Journal 64, 215–229.
| Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVWgtrfK&md5=da101c34a34455a70ae72677bb5e6d41CAS | 21070405PubMed |
Lund RE (1989) A User’s Guide to MSUSTAT Statistical Analysis Package Microcomputer Version 4(12), p. 202.
Parsons IR, Howe TK (1984) Effects of water stress on the water relations of Phaseolus vulgaris and the drought resistant Phaseolus acutifolius. Physiologia Plantarum 60, 197–202.
| Effects of water stress on the water relations of Phaseolus vulgaris and the drought resistant Phaseolus acutifolius.Crossref | GoogleScholarGoogle Scholar |
Pelleschi P, Rocher JP, Prioul JL (1997) Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant, Cell & Environment 20, 493–503.
| Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtVOgs74%3D&md5=9c69988b1d9e291fc5da1ea1a88184afCAS |
Pottier-Alapetite G (1979) Flore de la Tunisie. Angiospermes-Dicotyledones: Apetales-Dialypetales. Imprimerie Officielle de la République Tunisienne/Ministère de l’Enseignement Supérieur et de la Recherche Scientifique et Ministère de l’Agriculture, Tunis, 651 pp.
Ramanjulu S, Sudhakar C (1997) Drought tolerance is partly related to amino acid accumulation and ammonia assimilation: a comparative study in two mulberry genotypes differing in drought sensitivity. Journal of Plant Physiology 150, 345–350.
| Drought tolerance is partly related to amino acid accumulation and ammonia assimilation: a comparative study in two mulberry genotypes differing in drought sensitivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitVenu7w%3D&md5=a2f9a5cf1e139d4473fa8e14a64cd42dCAS |
Renault H, Roussel V, El Amrani A, Arzel M, Renault D, Bouchereau A, Deleu C (2010) The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biology 10, 20
| The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance.Crossref | GoogleScholarGoogle Scholar | 20122158PubMed |
Robinson SA, Slade AP, Fox GG, Phillips R, Ratcliffe RG, Stewart GR (1991) The role of glutamate dehydrogenase in nitrogen metabolism. Plant Physiology 95, 509–516.
| The role of glutamate dehydrogenase in nitrogen metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtl2qsLY%3D&md5=8cc1664100592b2cc05aa361464e9e42CAS | 16668014PubMed |
Sambatti JBM, Caylor KK (2007) When is breeding for drought tolerance optimal if drought is random? New Phytologist 175, 70–80.
| When is breeding for drought tolerance optimal if drought is random?Crossref | GoogleScholarGoogle Scholar |
Save R, Castell C, Terradas J (1999) Gas exchange and water relations. In ‘Ecology of Mediterranean evergreen ecological studies’. (Eds F Roda’, J Retama, A Gracia, J Bellot) pp. 135–147. (Springer: Berlin)
Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115, 433–447.
| Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress.Crossref | GoogleScholarGoogle Scholar | 25564467PubMed |
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89–97.
| Proline: a multifunctional amino acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1yit7s%3D&md5=62a4bd8434a55cb37ed97caa7fb60373CAS | 20036181PubMed |
Taiz L, Zeiger E (1998) ‘Plant physiology.’ 1st edn. (Sinauer Associates Inc.: Massachusetts, London)
Turner NC (1996) Further progress in crop water relations. Advances in Agronomy 58, 293–338.
| Further progress in crop water relations.Crossref | GoogleScholarGoogle Scholar |
Widodo , Patterson JH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany 60, 4089–4103.
| Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1WqtLnF&md5=1ffe77ffd0627f48b100af7019dee39dCAS | 19666960PubMed |
Xue X, Liu A, Hua X (2009) Proline accumulation and transcriptional regulation of proline biosynthesis and degradation in Brassica napus. BMB Reports 42, 28–34.
| Proline accumulation and transcriptional regulation of proline biosynthesis and degradation in Brassica napus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFGiurg%3D&md5=ca09fb64d562a710b4d0143cd427744eCAS | 19192390PubMed |
