Differential protein expression reveals salt tolerance mechanisms of Desmostachya bipinnata at moderate and high levels of salinity
Hina Asrar A , Tabassum Hussain A , Bilquees Gul A C , M. Ajmal Khan A and Brent L. Nielsen B
+ Author Affiliations
- Author Affiliations
A Institute of Sustainable Halophyte Utilisation, University of Karachi, Karachi-75270, Pakistan.
B Department of Microbiology and Molecular Biology, Brigham Young University, Provo, UT 84602, USA.
C Corresponding author. Email: bilqueesgul@uok.edu.pk
Functional Plant Biology 45(8) 793-812 https://doi.org/10.1071/FP17281
Submitted: 7 October 2017 Accepted: 26 January 2018 Published: 16 March 2018
Abstract
A proteomics approach was used to investigate salt tolerance mechanisms of Desmostachya bipinnata (L.) Stapf. Plants were subjected to 0 mM (control), 100 mM (moderate) and 400 mM (high) NaCl. Proteins were separated by two-dimensional gel electrophoresis and identified with available databases. Optimal plant fresh weight was found at moderate salinity but declined at high salinity. Water potential, osmotic potential, Na+/K+ ratio, leaf electrolyte leakage, sugars and proline were altered at high salinity. However, water potential, proline content and electrolyte leakage were maintained at moderate salinity; Na+ and K+ concentrations increased, whereas sugars and osmotic potential decreased. Comparative proteome analysis revealed 103 salt responsive proteins. At moderate salinity, most of the proteins involved in energy metabolism, transport, antioxidative defence and cell growth were either unchanged or increased. Proteins related to amino-acid metabolism were decreased while those associated with secondary metabolism were accumulated. At high salinity, amino-acid metabolism and dehydration responses were evident; proteins of energy metabolism, transport and stress defence were downregulated. These results suggest that an efficient defence system, improved transport of water and metabolites, increased cell wall lignification and regulation of energy and carbohydrate metabolism allowed better potential for plant growth under moderately saline conditions.
Additional keywords: comparative proteomics, K+ maintenance, osmotic adjustment, salt adaptation.
References
Adnan MY, Hussain T, Asrar H, Hameed A, Gul B, Nielsen BL, Khan MA (2016) Desmostachya bipinnata manages photosynthesis and oxidative stress at moderate salinity. Flora 225, 1–9.| Desmostachya bipinnata manages photosynthesis and oxidative stress at moderate salinity.Crossref | GoogleScholarGoogle Scholar |
Asrar H, Hussain T, Hadi SMS, Gul B, Nielsen BL, Khan MA (2017) Salinity induced changes in light harvesting and carbon assimilating complexes of Desmostachya bipinnata (L.) Staph. Environmental and Experimental Botany 135, 86–95.
| Salinity induced changes in light harvesting and carbon assimilating complexes of Desmostachya bipinnata (L.) Staph.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXjvFKjsQ%3D%3D&md5=d70225562bfac6a76d19cd73e9e1d531CAS |
Azri W, Barhoumi Z, Chibani F, Borji M, Bessrour M, Mliki A (2016) Proteomic responses in shoots of the facultative halophyte Aeluropus littoralis (Poaceae) under NaCl salt stress. Functional Plant Biology 43, 1028–1047.
| Proteomic responses in shoots of the facultative halophyte Aeluropus littoralis (Poaceae) under NaCl salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1yjtbvI&md5=d929f1394df989c4408ea7dd55d4ef51CAS |
Baginsky S (2009) Plant proteomics: concepts, applications, and novel strategies for data interpretation. Mass Spectrometry Reviews 28, 93–120.
| Plant proteomics: concepts, applications, and novel strategies for data interpretation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGlur4%3D&md5=bbd31ad538a99c1c99a2da32d4b5574aCAS |
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
| Rapid determination of free proline for water-stress studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlsVGitLk%3D&md5=f7b2057049704b3c887da5ccf7d39629CAS |
Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391, 485–488.
| Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtVCjtr4%3D&md5=1fbaebe4fcc5d95f979d01175866e915CAS |
Bouaziz D, Pirrello J, Amor HB, Hammami A, Charfeddine M, Dhieb A, Bouzayen M, Gargouri-Bouzid R (2012) Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato. Plant Physiology and Biochemistry 60, 98–108.
| Ectopic expression of dehydration responsive element binding proteins (StDREB2) confers higher tolerance to salt stress in potato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOiu7jL&md5=5485ce31d65f2c2b334eb1cf7b558f68CAS |
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=90b0b14534fb4b0d25711d896ae5505eCAS |
Chen J, Cheng T, Wang P, Liu W, Xiao J, Yang Y, Hu X, Jiang Z, Zhang S, Shi J (2012) Salinity-induced changes in protein expression in the halophytic plant Nitraria sphaerocarpa. Journal of Proteomics 75, 5226–5243.
| Salinity-induced changes in protein expression in the halophytic plant Nitraria sphaerocarpa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVymsbnM&md5=24b54f7695697c3ba7c8946f5ab9f07cCAS |
Cheng T, Chen J, Zhang J, Shi S, Zhou Y, Lu L, Wang P, Jiang Z, Yang J, Zhang S (2015) Physiological and proteomic analyses of leaves from the halophyte Tangut nitraria reveals diverse response pathways critical for high salinity tolerance. Frontiers in Plant Science 6, 30
| Physiological and proteomic analyses of leaves from the halophyte Tangut nitraria reveals diverse response pathways critical for high salinity tolerance.Crossref | GoogleScholarGoogle Scholar |
Chi Y, Cheng Y, Vanitha J, Kumar N, Ramamoorthy R, Ramachandran S, Jiang S-Y (2011) Expansion mechanisms and functional divergence of the glutathione S-transferase family in sorghum and other higher plants. DNA Research 18, 1–16.
| Expansion mechanisms and functional divergence of the glutathione S-transferase family in sorghum and other higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1WgsLY%3D&md5=e4cdeb0b26664dd6119637dca4970b41CAS |
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=a26588d630f9eb958100d9569bfefee4CAS |
Diray-Arce J, Clement M, Gul B, Khan MA, Nielsen BL (2015) Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance. BMC Genomics 16, 353
| Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance.Crossref | GoogleScholarGoogle Scholar |
Dixon SJ, Stockwell BR (2014) The role of iron and reactive oxygen species in cell death. Nature Chemical Biology 10, 9–17.
| The role of iron and reactive oxygen species in cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFCjtrzO&md5=d2f8e1099fedb0d6bf3858e67d05b0deCAS |
Endo N, Yoshida K, Akiyoshi M, Yoshida Y, Hayashi N (2005) Putative UDP-galactose epimerase and metallothioneine of Paspalum vaginatum enhanced the salt tolerance of rice, Oryza sativa L. from transplanting to harvest stages. Breeding Science 55, 163–173.
| Putative UDP-galactose epimerase and metallothioneine of Paspalum vaginatum enhanced the salt tolerance of rice, Oryza sativa L. from transplanting to harvest stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXotFartb0%3D&md5=4ad7820486929de28e0f4692fbf3481bCAS |
Epstein E (1972) Physiological genetics of plant nutrition. In ‘Mineral nutrition of plants: principles and perspectives’. pp. 325–344. (John Wiley & Sons Inc.: New York)
Finnie C, Borch J, Collinge DB (1999) 14-3-3 proteins: eukaryotic regulatory proteins with many functions. Plant Molecular Biology 40, 545–554.
| 14-3-3 proteins: eukaryotic regulatory proteins with many functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvV2rsbk%3D&md5=8338e2c248fc30b0e52f4dbc5af2c983CAS |
Flowers TJ, Colmer TD (2015) Plant salt tolerance: adaptations in halophytes. Annals of Botany 115, 327–331.
| Plant salt tolerance: adaptations in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhvFChurbP&md5=f2de4c131e6b7c98efcb68fe5edc9ccbCAS |
Fortpied J, Gemayel R, Stroobant V, Van Schaftingen E (2005) Plant ribulosamine/erythrulosamine 3-kinase, a putative protein-repair enzyme. The Biochemical Journal 388, 795–802.
| Plant ribulosamine/erythrulosamine 3-kinase, a putative protein-repair enzyme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvVGht7w%3D&md5=86c8c03a4a94004fad24392bc9c50914CAS |
Galal TM, Shehata HS (2013) Morphological variations, biomass and ion accumulation of the aboveground shoots of Desmostachya bipinnata (L.) Stapf. Flora – Morphology, Distribution, Functional Ecology of Plants 208, 556–561.
| Morphological variations, biomass and ion accumulation of the aboveground shoots of Desmostachya bipinnata (L.) Stapf.Crossref | GoogleScholarGoogle Scholar |
Glenn E (1987) Relationship between cation accumulation and water content of salt-tolerant grasses and a sedge. Plant, Cell and Environment 10, 205–212.
Granot D (2008) Putting plant hexokinases in their proper place. Phytochemistry 69, 2649–2654.
| Putting plant hexokinases in their proper place.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlartbrL&md5=5790f3ac37435b028b87408489f25857CAS |
Guo X, Wu Y, Wang Y, Chen Y, Chu C (2009) OsMSRA4. 1 and OsMSRB1. 1, two rice plastidial methionine sulfoxide reductases, are involved in abiotic stress responses. Planta 230, 227–238.
| OsMSRA4. 1 and OsMSRB1. 1, two rice plastidial methionine sulfoxide reductases, are involved in abiotic stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVCmtbo%3D&md5=b54f1a696e46b1e12c9cc919c127b165CAS |
Han G, Wang M, Yuan F, Sui N, Song J, Wang B (2014) The CCCH zinc finger protein gene AtZFP1 improves salt resistance in Arabidopsis thaliana. Plant Molecular Biology 86, 237–253.
| The CCCH zinc finger protein gene AtZFP1 improves salt resistance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1GnurrP&md5=096fc85850e8305c9dee3c6cfebf5758CAS |
Jia H, Shao M, He Y, Guan R, Chu P, Jiang H (2015) Proteome dynamics and physiological responses to short-term salt stress in Brassica napus leaves. PLoS One 10, e0144808
| Proteome dynamics and physiological responses to short-term salt stress in Brassica napus leaves.Crossref | GoogleScholarGoogle Scholar |
Kelij S, Majd A, Nematzade G, Jonoubi P, Haghighi L (2013) Phenylalanine ammonialyase gene expression and activity in relation to lignin deposition in salt stressed Aeluropus littoralis. Advanced Studies in Biology 5, 403–412.
| Phenylalanine ammonialyase gene expression and activity in relation to lignin deposition in salt stressed Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar |
Khan NA, Khan MIR, Asgher M, Fatma M, Masood A, Syeed S (2014) Salinity tolerance in plants: revisiting the role of sulfur metabolites. Journal of Plant Biochemistry & Physiology 2, 1–8.
Kirschbaum MU (2011) Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiology 155, 117–124.
| Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagsb8%3D&md5=203b1e973238e73f1fc45e8aa42f5287CAS |
Koyro H-W, Hussain T, Huchzermeyer B, Khan MA (2013) Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. Environmental and Experimental Botany 91, 22–29.
| Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntF2msb0%3D&md5=b14c86cf191af4e19ef8c5240ecafe5cCAS |
Kramer PJ, Boyer JS (1995) ‘Water relations of plants and soils.’ pp. 16–41. (Academic Press: New York)
Kumari A, Das P, Parida AK, Agarwal PK (2015) Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Frontiers in Plant Science 6, 537
| Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar |
Maršálová L, Vítámvás P, Hynek R, Prášil IT, Kosová K (2016) Proteomic response of Hordeum vulgare cv. tadmor and Hordeum marinum to salinity stress: similarities and differences between a glycophyte and a halophyte. Frontiers in Plant Science 7, 1154
| Proteomic response of Hordeum vulgare cv. tadmor and Hordeum marinum to salinity stress: similarities and differences between a glycophyte and a halophyte.Crossref | GoogleScholarGoogle Scholar |
McQueen-Mason SJ, Cosgrove DJ (1995) Expansin mode of action on cell walls (analysis of wall hydrolysis, stress relaxation, and binding). Plant Physiology 107, 87–100.
| Expansin mode of action on cell walls (analysis of wall hydrolysis, stress relaxation, and binding).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVOms7s%3D&md5=287586397872242184f46ad7e6d96f65CAS |
Meychik NR, Nikolaeva YI, Yermakov IP (2013) Physiological response of halophyte (Suaeda altissima (L.) Pall.) and glycophyte (Spinacia oleracea L.) to salinity. American Journal of Plant Sciences 4, 427–435.
| Physiological response of halophyte (Suaeda altissima (L.) Pall.) and glycophyte (Spinacia oleracea L.) to salinity.Crossref | GoogleScholarGoogle Scholar |
Pandey A (2013) An overview of Desmostachya bipinnata. Journal of Drug Discovery and Therapeutics 1, 67–68.
Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. Journal of Proteome Research 9, 2584–2599.
| Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvVKrur8%3D&md5=07aa6f3813cfc040eed09984fc72a103CAS |
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environmental Science and Pollution Research International 22, 4056–4075.
| Effect of salinity stress on plants and its tolerance strategies: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFGls7jN&md5=ca3172ac9a70fb82b0c9af3860626620CAS |
Redillas MC, Park S-H, Lee JW, Kim YS, Jeong JS, Jung H, Bang SW, Hahn T-R, Kim J-K (2012) Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnology Reports 6, 89–96.
| Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress.Crossref | GoogleScholarGoogle Scholar |
Saito T, Kobayashi NI, Tanoi K, Iwata N, Suzuki H, Iwata R, Nakanishi TM (2013) Expression and functional analysis of the CorA-MRS2-ALR-type magnesium transporter family in rice. Plant and Cell Physiology 54, 1673–1683.
| Expression and functional analysis of the CorA-MRS2-ALR-type magnesium transporter family in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1SmtbfN&md5=123e74ed1730727737f1901fdb203465CAS |
Shukla PS, Agarwal P, Gupta K, Agarwal PK (2015) Molecular characterization of an MYB transcription factor from a succulent halophyte involved in stress tolerance. AoB Plants 7, plv054
| Molecular characterization of an MYB transcription factor from a succulent halophyte involved in stress tolerance.Crossref | GoogleScholarGoogle Scholar |
Sobhanian H, Motamed N, Jazii FR, Nakamura T, Komatsu S (2010) Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant. Journal of Proteome Research 9, 2882–2897.
| Salt stress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1OntrY%3D&md5=27c78c1ecf7fe73e342540b1dcc03c65CAS |
Tronchet M, Balague C, Kroj T, Jouanin L, Roby D (2010) Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis. Molecular Plant Pathology 11, 83–92.
| Cinnamyl alcohol dehydrogenases-C and D, key enzymes in lignin biosynthesis, play an essential role in disease resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslOitLg%3D&md5=f8e0d292796b1112d1caa4eeea5610a3CAS |
Wang X, Yang P, Gao Q, Liu X, Kuang T, Shen S, He Y (2008) Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta 228, 167–177.
| Proteomic analysis of the response to high-salinity stress in Physcomitrella patens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtVamtrs%3D&md5=37b69c50f85c627851e1151d1ba234b8CAS |
Wang J, Meng Y, Li B, Ma X, Lai Y, Si E, Yang K, Xu X, Shang X, Wang H (2015) Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus. Plant, Cell and Environment 38, 655–669.
| Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvVKjtrc%3D&md5=0f443619182b6aa359da899595044003CAS |
Weissbach H, Resnick L, Brot N (2005) Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1703, 203–212.
| Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvFOqsw%3D%3D&md5=d93663310f30d2a36c02336f4172289aCAS |
Yemm E, Willis A (1954) The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57, 508–514.
| The estimation of carbohydrates in plant extracts by anthrone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG2cXlvFOmtw%3D%3D&md5=f6b7ad29fd8e8973fc8c7333d73eda5dCAS |
Yu J, Chen S, Zhao Q, Wang T, Yang C, Diaz C, Sun G, Dai S (2011) Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. Journal of Proteome Research 10, 3852–3870.
| Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpvVyhsbc%3D&md5=11129e42c589dc216fa4c6443e18ba77CAS |
Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. Journal of Proteome Research 11, 49–67.
| Mechanisms of plant salt response: insights from proteomics.Crossref | GoogleScholarGoogle Scholar |
