Ultrastructural and biochemical changes induced by salt stress in Jatropha curcas seeds during germination and seedling development
Nara L. M. Alencar A B , Cibelle G. Gadelha A , Maria I. Gallão C , Mary A. H. Dolder D , José T. Prisco A E and Enéas Gomes-Filho A E F
+ Author Affiliations
- Author Affiliations
A Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Fortaleza 60 440 970, Brazil.
B Instituto Federal de Educação Ciência e Tecnologia do Ceará, Campus Crateús, Crateús 6 370 000, Brazil.
C Departamento de Biologia, Universidade Federal do Ceará, Fortaleza 60 440 554, Brazil.
D Departamento de Biologia Estrutural e Funcional, Instituto de Biologia, Universidade Estadual de Campinas, Campinas 13 083 862, Brazil.
E Instituto Nacional de Ciência e Tecnologia em Salinidade (INCTSal)/CNPq, Departamento de Bioquímica e Biologia Molecular, Universidade Federal do Ceará, Fortaleza 60 440 970 PO Box 6039, Brazil.
F Corresponding author. Email: egomesf@ufc.br
Functional Plant Biology 42(9) 865-874 https://doi.org/10.1071/FP15019
Submitted: 28 January 2015 Accepted: 24 May 2015 Published: 24 June 2015
Abstract
Jatropha curcas L. is a multipurpose species of the Euphorbiaceae family that is widespread in arid and semiarid regions. This study investigated the ultrastructural and biochemical changes induced by salt stress during J. curcas seed germination and seedling development. Salt stress negatively affected seed germination and increased Na+ and Cl– contents in endosperms and embryo-axis. Lipids represented the most abundant reserves (64% of the quiescent seed dry mass), and their levels were strongly decreased at 8 days after imbibition (DAI) under salinity stress. Proteins were the second most important reserve (21.3%), and their levels were also reduced under salt stress conditions. Starch showed a transient increase at 5 DAI under control conditions, which was correlated with intense lipid mobilisation during this period. Non-reducing sugars and free amino acids were increased in control seeds compared with quiescent seeds, whereas under the salt-stress conditions, minimal changes were observed. In addition, cytochemical and ultrastructural analyses confirmed greater alterations in the cellular reserves of seeds that had been germinated under NaCl stress conditions. Salt stress promoted delays in protein and lipid mobilisation and induced ultrastructural changes in salt-stressed endosperm cells, consistent with delayed protein and oil body degradation.
Additional keywords: lipid, protein, salinity stress, starch, oilseed, ultrastructure.
References
Alencar NLM, Inneco R, Gomes-Filho E, Gallão MI, Alvarez-Pizarro JC, Prisco JT, Oliveira AB (2012) Seed reserve composition and mobilization during germination and early seedling establishment of Cereus jamacaru D.C. ssp. jamacaru (Cactaceae). Anais da Academia Brasileira de Ciencias 84, 823–832.| Seed reserve composition and mobilization during germination and early seedling establishment of Cereus jamacaru D.C. ssp. jamacaru (Cactaceae).Crossref | GoogleScholarGoogle Scholar |
Andréo-Souza Y, Pereira AL, Silva FFSS, Ribeiro-Reis RC, Evangelista MRV, Castro RD, Dantas BF (2010) Efeito da salinidade na germinação de sementes e no crescimento inicial de mudas de pinhão-manso. Revista Brasileira de Sementes 32, 83–92.
| Efeito da salinidade na germinação de sementes e no crescimento inicial de mudas de pinhão-manso.Crossref | GoogleScholarGoogle Scholar |
Ashraf M, Zafar R, Ashraf MY (2003) Time-course changes in the inorganic and organic components of germinating sunflower achenes under salt (NaCl) stress. Flora 198, 26–36.
| Time-course changes in the inorganic and organic components of germinating sunflower achenes under salt (NaCl) stress.Crossref | GoogleScholarGoogle Scholar |
Baethgen WE, Alley MM (1989) A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant Kjeldahl digests. Communications in Soil Science and Plant Analysis 20, 961–969.
| A manual colorimetric procedure for measuring ammonium nitrogen in soil and plant Kjeldahl digests.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltleisbs%3D&md5=bbedbee3b7aca4443514344b60af5de4CAS |
Baranova EN, Gulevich AA, Polyakov VY (2006) Effects of NaCl, Na2SO4, and mannitol on storage lipid mobilization in the cotyledons and roots of purple alfalfa seedlings. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 53, 779–784.
| Effects of NaCl, Na2SO4, and mannitol on storage lipid mobilization in the cotyledons and roots of purple alfalfa seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFChsL3M&md5=adf227702d5029db5210011bbaff0876CAS |
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) ‘Seeds: physiology of development, germination and dormancy’. (3rd edn) (Springer: New York)
Díaz-López L, Gimeno V, Lidón V, Simón I, Martínez V, García-Sánchez F (2012) The tolerance of Jatropha curcas seedlings to NaCl: an ecophysiological analysis. Plant Physiology and Biochemistry 54, 34–42.
| The tolerance of Jatropha curcas seedlings to NaCl: an ecophysiological analysis.Crossref | GoogleScholarGoogle Scholar | 22377428PubMed |
DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350–356.
| Colorimetric method for determination of sugars and related substances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG28XjvFynsg%3D%3D&md5=9ff167b1d78f5432978ff16c07bbe999CAS |
Gaines TP, Parker MB, Gascho GJ (1984) Automated determination of chlorides in soil and plant tissue by sodium nitrate. Agronomy Journal 76, 371–374.
| Automated determination of chlorides in soil and plant tissue by sodium nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1Sjt7g%3D&md5=4eabdeaf8bfc5735a9903a601fb392adCAS |
Gao S, Ouyang C, Wang S, Xu Y, Tang L, Chen F (2008) Effects of salt stress on growth, antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. seedlings. Plant, Soil and Environment 54, 374–381.
Heller J (1996) ‘Physic nut. Jatropha curcas L.: promoting the conservation and use of underutilized and neglected crops.’ (International Plant Genetic Resources Institute: Gatersleben, Germany)
Hodge JE, Hofreiter BT (1962) ‘Determination of reducing sugars and carbohydrates.’ In ‘Methods in carbohydrate chemistry’. (Eds RL Whistler, ML Wolfrom) pp. 380–394. (Academic Press: London)
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Journal of Cell Biology 27, 137–138.
Laboriau LG (1983) ‘A germinação das sementes.’ (OEA: Washington DC)
Liu J, Guo WQ, Shi DC (2010) Seed germination, seedling survival, and physiological response of sunflowers under saline and alkaline conditions. Photosynthetica 48, 278–286.
| Seed germination, seedling survival, and physiological response of sunflowers under saline and alkaline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVahtr7K&md5=1aaa83a0a41b9661a023d2ecec687b96CAS |
Maguire JD (1962) Speed of germination-aid in selection and evaluation for seedling emergence and vigor. Crop Science 2, 176–177.
| Speed of germination-aid in selection and evaluation for seedling emergence and vigor.Crossref | GoogleScholarGoogle Scholar |
Marques EC, Freitas PAF, Alencar NLM, Prisco JT, Gomes-Filho E (2013) Increased Na+ and Cl– accumulation induced by NaCl salinity inhibits cotyledonary reserve mobilization and alters the source-sink relationship in establishing dwarf cashew seedlings. Acta Physiologiae Plantarum 35, 2171–2182.
| Increased Na+ and Cl– accumulation induced by NaCl salinity inhibits cotyledonary reserve mobilization and alters the source-sink relationship in establishing dwarf cashew seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFems7g%3D&md5=9390f2d805b131fbce0f9e21a31cda0cCAS |
Melo GM, Cunha PC, Pereira JAF, Willadino L, Ulisses C (2011) Anatomical changes in the leaves and roots of Jatropha curcas L. cultivated under saline stress. Revista Ciência Agronômica 42, 670–674.
| Anatomical changes in the leaves and roots of Jatropha curcas L. cultivated under saline stress.Crossref | GoogleScholarGoogle Scholar |
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Analytical Chemistry 31, 426–428.
| Use of dinitrosalicylic acid reagent for determination of reducing sugar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1MXmtFKiuw%3D%3D&md5=41d2051b1bc1da7f9d9e2cbfbb2a93c7CAS |
Muccifora S, Guerranti R, Muzzi C, Hope-Onyekwere NS, Pagani R, Leoncini LR, Bellani LM (2010) Ultrastructural and biochemical investigations of protein mobilization of Mucuna pruriens (L.) DC. cotyledons and embryo axis. Protoplasma 239, 15–21.
| Ultrastructural and biochemical investigations of protein mobilization of Mucuna pruriens (L.) DC. cotyledons and embryo axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1GjtrY%3D&md5=8032aedd75e64c460dd232dc70aec89fCAS | 19859786PubMed |
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
| Mechanisms of salinity tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=e2ba555e0946a244ab5e98e4f2e7cc4dCAS | 18444910PubMed |
Pompelli MF, Marques RF (2014) GerminaQuant version 1.0. Computer software, patent of INPI/Brazil n° BR512014000630-1.
Reale L, Ricci A, Ferranti F, Torricelli R, Venanzoni R, Falcinelli M (2012) Cytohistological analysis and mobilization of reserves in Jatropha curcas L. seed. Crop Science 52, 830–835.
| Cytohistological analysis and mobilization of reserves in Jatropha curcas L. seed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvVeltLs%3D&md5=7a79afcdfa35e01e3c92c82c2199b141CAS |
Sánchez-Linares L, Gavilanes-Ruíz M, Díaz-Pontones D, Guzmán-Chávez F, Calzada-Alejo V, Zurita-Villegas V, Luna-Loaiza V, Moreno-Sánchez R, Bernal-Lugo I, Sánchez-Nieto S (2012) Early carbon mobilization and radicle protrusion in maize germination. Journal of Experimental Botany 63, 4513–4526.
| Early carbon mobilization and radicle protrusion in maize germination.Crossref | GoogleScholarGoogle Scholar | 22611232PubMed |
Silva EN, Vieira SA, Ribeiro RV, Ponte LFA, Ferreira-Silva SL, Silveira JAG (2013) Contrasting physiological responses of Jatropha curcas plants to single and combined stresses of salinity and heat. Journal of Plant Growth Regulation 31, 1–11.
| Contrasting physiological responses of Jatropha curcas plants to single and combined stresses of salinity and heat.Crossref | GoogleScholarGoogle Scholar |
Vidal BC (1970) Dichroism in collagen bundles stained with Xylidine Ponceau 2R. Analytical Histochemistry 15, 289–296.
Voigt EL, Almeida TD, Chagas RM, Ponte LFA, Viégas RA, Silveira JAG (2009) Source-sink regulation of cotyledonary reserve mobilization during cashew (Anacardium occidentale) seedling establishment under NaCl salinity. Journal of Plant Physiology 166, 80–89.
| Source-sink regulation of cotyledonary reserve mobilization during cashew (Anacardium occidentale) seedling establishment under NaCl salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Knurc%3D&md5=28fa9df4e5d15b30081b4d33592bd4cbCAS | 18448194PubMed |
Watson ML (1958) Staining of tissue sections for electron microscopy with heavy metals. The Journal of Biophysical and Biochemical Cytology 4, 475–478.
| Staining of tissue sections for electron microscopy with heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG1c7gs1Klsg%3D%3D&md5=5b6cedac20aee99a302410281b03a29cCAS | 13563554PubMed |
Yang MF, Liu YJ, Liu Y, Chen H, Chen F, Shen SH (2009) Proteomic analysis of oil mobilization in seed germination and post-germination development of Jatropha curcas. Journal of Proteome Research 8, 1441–1451.
| Proteomic analysis of oil mobilization in seed germination and post-germination development of Jatropha curcas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVWltg%3D%3D&md5=68e84f432e6f635f9743fef13f1a7a5fCAS | 19152324PubMed |
Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst (London) 80, 209–213.
| The determination of amino acids with ninhydrin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2MXjsFClug%3D%3D&md5=3a003e1f5c6c997c1cf51e31301c95e4CAS |
