The LmSAP gene isolated from the halotolerant Lobularia maritima improves salt and ionic tolerance in transgenic tobacco lines
Rania Ben Saad A , Ameny Farhat-Khemekhem B , Nihed Ben Halima A , Karim Ben Hamed C , Faical Brini A and Walid Saibi A D
+ Author Affiliations
- Author Affiliations
A Biotechnology and Plant Improvement Laboratory, Centre of Biotechnology of Sfax, University of Sfax, B.P ‘1177’, 3018, Sfax – Tunisia.
B Laboratory of Microorganisms and Biomolecules, Centre of Biotechnology of Sfax, University of Sfax, B.P 1177, 3018, Sfax – Tunisia.
C Laboratory of Extremophile Plants, Centre of Biotechnology of Borj Cedria, PO Box 901, 2050 Hammam-Lif, Tunisia.
D Corresponding author. Email: saibiwalid@gmail.com
Functional Plant Biology 45(3) 378-391 https://doi.org/10.1071/FP17202
Submitted: 18 July 2017 Accepted: 29 September 2017 Published: 30 October 2017
Abstract
The A20/AN1 zinc-finger domain-containing proteins of the stress-associated proteins (SAPs) family are fast emerging as potential candidates for biotechnological approaches to improve abiotic stress tolerance in plants. We identified LmSAP, one of the SAPs genes in Lobularia maritima (L.) Desv., a halophyte brassicaceae, through its transcript accumulation in response to salinity and ionic stresses. Sequence homology analysis revealed that LmSAP contains two conserved zinc-finger domains A20 and AN1. Phylogeny analyses showed that LmSAP exhibited high amino acid sequence identity to other plant SAPs. Heterologous expression of LmSAP in yeast increased cell tolerance to salt and osmotic stress. In addition, the overexpression of LmSAP conferred high salt and ionic tolerance to transgenic tobacco plants. Transgenic tobacco seedlings showed higher survival rates and antioxidant activities under salt and ionic stresses. Enhanced antioxidant activities paralleled lower malondialdehyde and superoxide anion O2− levels in the LmSAP transgenic seedlings. Overall, our results suggest that overexpression of LmSAP enhanced salt tolerance by maintaining ionic balance and limiting oxidative and osmotic stresses.
Additional keywords: A20/AN1 zinc finger protein, ionic stress, LmSAP gene, salt stress, transgenic tobacco.
References
Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVKis7s%3D&md5=a0bf6214b75895f2b7bd71bb3e0c4088CAS |
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1
| Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaH1MXhtFaqtg%3D%3D&md5=0e5c5473e5ff5a58bdf4f81e1c37612cCAS |
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=7defff6fc79bf274d695d8ed5adb8abcCAS |
Ben Saad R, Zouari N, Ben Ramdhan W, Azaza J, Meynard D, Guiderdoni E, Hassairi A (2010) Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger ‘AlSAP’ gene isolated from the halophyte grass Aeluropus littoralis. Plant Molecular Biology 72, 171–190.
| Improved drought and salt stress tolerance in transgenic tobacco overexpressing a novel A20/AN1 zinc-finger ‘AlSAP’ gene isolated from the halophyte grass Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsV2mtb%2FO&md5=5c41535352aeb932034af82892a03a4aCAS |
Ben Saad R, Ben-Ramdhan W, Zouari N, Azaza J, Mieulet D, Guiderdoni E, Ellouz R, Hassairi A (2012a) Marker-free transgenic durum wheat cv. Karim expressing the AlSAP gene exhibits a high level of tolerance to salinity and dehydration stresses. Molecular Breeding 30, 521–533.
| Marker-free transgenic durum wheat cv. Karim expressing the AlSAP gene exhibits a high level of tolerance to salinity and dehydration stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvFOks7c%3D&md5=3d4a6cd10bd6638398ab4f1da25618aeCAS |
Ben Saad R, Fabre D, Mieulet D, Meynard D, Dingkuhn M, Al-Doss A, Guiderdoni E, Hassairi A (2012b) Expression of the Aeluropus littoralis AlSAP gene in rice confers broad tolerance to abiotic stresses through maintenance of photosynthesis. Plant, Cell & Environment 35, 626–643.
| Expression of the Aeluropus littoralis AlSAP gene in rice confers broad tolerance to abiotic stresses through maintenance of photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Reports 27, 411–424.
| Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvFygt7k%3D&md5=0e0250d391fb2605249b1ceaab44233fCAS |
Bienz M (2006) The PHD finger, a nuclear protein-interaction domain. Trends in Biochemical Sciences 31, 35–40.
| The PHD finger, a nuclear protein-interaction domain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosFKkug%3D%3D&md5=4c2ca6b09e37abca970163a65008a9b8CAS |
Borden KL (2000) RING domains: master builders of molecular scaffolds? Journal of Molecular Biology 295, 1103–1112.
| RING domains: master builders of molecular scaffolds?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnsFChsQ%3D%3D&md5=e4c1136d78bf552fab3d8bb327b1c257CAS |
Bose J, Rodrigo-Moreno A, Lai D, Xie Y, Shen W, Shabala S (2015) Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa. Annals of Botany 115, 481–494.
| Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoa.Crossref | GoogleScholarGoogle Scholar |
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=2821bcfbf01a16b0f1b14eb3a73c5812CAS |
Brini F, Yamamoto A, Jlaiel L, Takeda S, Hobo T, Dinh HQ, Hattori T, Masmoudi K, Hanin M (2011) Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis. Plant & Cell Physiology 52, 676–688.
| Pleiotropic effects of the wheat dehydrin DHN-5 on stress responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFKis78%3D&md5=223a618eb20daa9dd6176a0ed7ecab46CAS |
Bussler W (1972) Epstein, E.: Mineral nutrition of plants: principles and perspectives. John Wiley and Sons, Inc., New York, London, Sydney, Toronto. 1972. 412 Seiten, 23× 16 cm, zahlreiche Abbildungen, £ 4.85. Journal of Plant Nutrition and Soil Science 132, 158–159.
Charrier A, Planchet E, Cerveau D, Gimeno-Gilles C, Verdu I, Limami AM, Lelièvre E (2012) Overexpression of a Medicago truncatula stress-associated protein gene (MtSAP1) leads to nitric oxide accumulation and confers osmotic and salt stress tolerance in transgenic tobacco. Planta 236, 567–577.
| Overexpression of a Medicago truncatula stress-associated protein gene (MtSAP1) leads to nitric oxide accumulation and confers osmotic and salt stress tolerance in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyks7vP&md5=b96fdcd474fc8d47c071ef5a6558010eCAS |
Charrier A, Lelièvre E, Limami AM, Planchet E (2013) Medicago truncatula stress associated protein 1 gene (MtSAP1) overexpression confers tolerance to abiotic stress and impacts proline accumulation in transgenic tobacco. Journal of Plant Physiology 170, 874–877.
| Medicago truncatula stress associated protein 1 gene (MtSAP1) overexpression confers tolerance to abiotic stress and impacts proline accumulation in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit12js7k%3D&md5=8130a632de9cde54d4518cace7212342CAS |
Chen H, Nelson R, Sherwood J (1994) Enhanced recovery of transformants of Agrobacterium tumefaciens after freeze-thaw transformation and drug selection. BioTechniques 16, 664–668, 670.
Choi H, Han S, Shin D, Lee S (2012) Polyubiquitin recognition by AtSAP5, an A20-type zinc finger containing protein from Arabidopsis thaliana. Biochemical and Biophysical Research Communications 419, 436–440.
| Polyubiquitin recognition by AtSAP5, an A20-type zinc finger containing protein from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1Oru7Y%3D&md5=86fe334840b71dfb0e185a066c550f1bCAS |
Dansana PK, Kothari KS, Vij S, Tyagi AK (2014) OsiSAP1 overexpression improves water-deficit stress tolerance in transgenic rice by affecting expression of endogenous stress-related genes. Plant Cell Reports 33, 1425–1440.
| OsiSAP1 overexpression improves water-deficit stress tolerance in transgenic rice by affecting expression of endogenous stress-related genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVGns7fL&md5=53029480c5471f2859caa7a4140ad065CAS |
Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. The Plant Journal 4, 215–223.
| Proline biosynthesis and osmoregulation in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFyksbk%3D&md5=d508b038f8d5703bb863db349596cb87CAS |
Dixit AR, Dhankher OP (2011) A novel stress-associated protein ‘AtSAP10’from Arabidopsis thaliana confers tolerance to nickel, manganese, zinc, and high temperature stress. PLoS One 6, e20921
| A novel stress-associated protein ‘AtSAP10’from Arabidopsis thaliana confers tolerance to nickel, manganese, zinc, and high temperature stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnslCmsbs%3D&md5=e82cd70a961a4bb345af997d3cd69554CAS |
Duan W, Sun B, Li TW, Tan BJ, Lee MK, Teo TS (2000) Cloning and characterization of AWP1, a novel protein that associates with serine/threonine kinase PRK1 in vivo. Gene 256, 113–121.
| Cloning and characterization of AWP1, a novel protein that associates with serine/threonine kinase PRK1 in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVGitr0%3D&md5=4cc56ff05cff838c091ff8806294a5d8CAS |
Elble R (1992) A simple and efficient procedure for transformation of yeasts. BioTechniques 13, 18–20.
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Ghneim-Herrera T, Selvaraj MG, Meynard D, Fabre D, Peña A, Ben Romdhane W, Ben Saad R, Ogawa SA, Rebolledo MC, Ishitani M, Tohme J, Al-Doss A, Guiderdoni E, Hassairi A (2017) Expression of the Aeluropus littoralis AlSAP gene enhances rice yield under field drought at the reproductive stage. Frontiers in Plant Science 8, 994
| Expression of the Aeluropus littoralis AlSAP gene enhances rice yield under field drought at the reproductive stage.Crossref | GoogleScholarGoogle Scholar |
Giri J, Vij S, Dansana PK, Tyagi AK (2011) Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytologist 191, 721–732.
| Rice A20/AN1 zinc-finger containing stress-associated proteins (SAP1/11) and a receptor-like cytoplasmic kinase (OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFWjtLzO&md5=d5b50bfbacd545ddabc677201d9f2543CAS |
Giri J, Dansana PK, Kothari KS, Sharma G, Vij S, Tyagi AK (2013) SAPs as novel regulators of abiotic stress response in plants. BioEssays 35, 639–648.
| SAPs as novel regulators of abiotic stress response in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1CisLg%3D&md5=fa799c705e02e2f9878592b59a2209dfCAS |
Gómez-Gómez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends in Plant Science 7, 251–256.
| Flagellin perception: a paradigm for innate immunity.Crossref | GoogleScholarGoogle Scholar |
Gruber F, Falkner FG, Dorner F, Hämmerle T (2001) Quantitation of viral DNA by real-time PCR applying duplex amplification, internal standardization, and two-color fluorescence detection. Applied and Environmental Microbiology 67, 2837–2839.
| Quantitation of viral DNA by real-time PCR applying duplex amplification, internal standardization, and two-color fluorescence detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Citbs%3D&md5=e40651342f302c87fd38d8a884931386CAS |
Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Current Opinion in Biotechnology 14, 177–193.
| Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVGlu78%3D&md5=c64ccdaf73748f27c86ab45cf8936829CAS |
Hishiya A, Iemura S, Natsume T, Takayama S, Ikeda K, Watanabe K (2006) A novel ubiquitin‐binding protein ZNF216 functioning in muscle atrophy. EMBO Journal 25, 554–564.
| A novel ubiquitin‐binding protein ZNF216 functioning in muscle atrophy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFGqtr8%3D&md5=f2872b3907b0fb87a5e5ebeb8b0165aeCAS |
Hoekema A, Hirsch P, Hooykaas P, Schilperoort R (1983) A binary plant vector strategy based on separation of vir-and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303, 179–180.
| A binary plant vector strategy based on separation of vir-and T-region of the Agrobacterium tumefaciens Ti-plasmid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktVWhsrY%3D&md5=b2ee5a8e0f4dc230c13e9a622e335210CAS |
Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Research 35, W585–W587.
| WoLF PSORT: protein localization predictor.Crossref | GoogleScholarGoogle Scholar |
Huang J, Wang MM, Jiang Y, Bao YM, Huang X, Sun H, Xu DQ, Lan HX, Zhang HS (2008) Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance. Gene 420, 135–144.
| Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXos12hu70%3D&md5=8b5ef7149331a140c3f3badf4cf76fefCAS |
Jia H, Li J, Zhang J, Ren Y, Hu J, Lu M (2016) Genome-wide survey and expression analysis of the stress-associated protein gene family in desert poplar, Populus euphratica. Tree Genetics & Genomes 12, 78
| Genome-wide survey and expression analysis of the stress-associated protein gene family in desert poplar, Populus euphratica.Crossref | GoogleScholarGoogle Scholar |
Jin Y, Wang M, Fu J, Xuan N, Zhu Y, Lian Y, Jia Z, Zheng J, Wang G (2007) Phylogenetic and expression analysis of ZnF-AN1 genes in plants. Genomics 90, 265–275.
| Phylogenetic and expression analysis of ZnF-AN1 genes in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXns1Khtrk%3D&md5=931e46598eec53a4a682334466b3c26cCAS |
Kang M, Fokar M, Abdelmageed H, Allen RD (2011) Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity. Plant Molecular Biology 75, 451–466.
| Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitlegtro%3D&md5=6859bacc9ca2c8077977816c1d23b708CAS |
Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Molecular Biology 66, 445–462.
| Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVWrtLs%3D&md5=1a6ae61688b62de49f04fe2b8ab6b4a4CAS |
Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. Journal of Experimental Botany 62, 4731–4748.
| Role of DREBs in regulation of abiotic stress responses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejsrbE&md5=c5a2fca726cfb9c436867b95107eaa7dCAS |
Li Xj, Wu YL, Yang BP, Wang JG, Zhang SZ, Zhang MQ (2014) Function analysis of sugarcane A20/AN1 zinc-finger protein gene in transgenic tobacco. Crop Science 54, 2724–2734.
| Function analysis of sugarcane A20/AN1 zinc-finger protein gene in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar |
Liu J, Yang X, Yang X, Xu M, Liu J, Xue M, Ma P (2017) Isolation and characterization of LcSAP, a Leymus chinensis gene which enhances the salinity tolerance of Saccharomyces cerevisiae. Molecular Biology Reports 44, 5–9.
| Isolation and characterization of LcSAP, a Leymus chinensis gene which enhances the salinity tolerance of Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVOjsrzO&md5=c3d0d4091b1b0d336a3b818b652617dcCAS |
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=c6e730b8bcaab07d1e52bd2affd3622dCAS |
Lloret A, Conejero A, Leida C, Petri C, Gil-Muñoz F, Burgos L, Badenes ML, Ríos G (2017) Dual regulation of water retention and cell growth by a stress-associated protein (SAP) gene in Prunus. Scientific Reports 7, 332
| Dual regulation of water retention and cell growth by a stress-associated protein (SAP) gene in Prunus.Crossref | GoogleScholarGoogle Scholar |
Maehly A, Chance B (1954) Catalases and peroxidases. Methods of Biochemical Analysis 1, 357–424.
Marè C, Mazzucotelli E, Crosatti C, Francia E, Stanca AM, Cattivelli L (2004) Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley. Plant Molecular Biology 55, 399–416.
| Hv-WRKY38: a new transcription factor involved in cold- and drought-response in barley.Crossref | GoogleScholarGoogle Scholar |
Martin RC, Glover CK, Baldwin JC, Dombrowski JE (2012) Identification and characterization of a salt stress-inducible zinc finger protein from Festuca arundinacea. BMC Research Notes 5, 66
| Identification and characterization of a salt stress-inducible zinc finger protein from Festuca arundinacea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlslejtLg%3D&md5=4775df905ba1eecc4af9eaa20bf2e49eCAS |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=f57d29645e044474f2197910ad0c0190CAS |
Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proceedings of the National Academy of Sciences of the United States of America 101, 6309–6314.
| Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKnurw%3D&md5=7d6678d13b02e415ec50da13aab43546CAS |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=a7a93041f5d2a381378a028388646d91CAS |
Paul A, Kumar S (2015) An A20/AN1-zinc-finger domain containing protein gene in tea is differentially expressed during winter dormancy and in response to abiotic stress and plant growth regulators. Plant Gene 1, 1–7.
| An A20/AN1-zinc-finger domain containing protein gene in tea is differentially expressed during winter dormancy and in response to abiotic stress and plant growth regulators.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Shu73O&md5=77de432b73bf6d8ab99fe3d83e1e9ea6CAS |
Rogers SO, Bendich AJ, Gelvin S, Schilperoort R (1988) Plant molecular biology manual. pp. 1–19.
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S Krawetz, S Misener) pp. 365–386. (Humana Press: Clifton, NJ, USA)
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
Sayed MA, Schumann H, Pillen K, Naz AA, Léon J (2012) AB-QTL analysis reveals new alleles associated to proline accumulation and leaf wilting under drought stress conditions in barley (Hordeum vulgare L.). BMC Genetics 13, 61
| AB-QTL analysis reveals new alleles associated to proline accumulation and leaf wilting under drought stress conditions in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1GktL0%3D&md5=0b7218736e05af924ab6b9e1e62a12efCAS |
Scebba F, Sebastiani L, Vitagliano C (1999) Protective enzymes against activated oxygen species in wheat (Triticum aestivum L.) seedlings: responses to cold acclimation. Journal of Plant Physiology 155, 762–768.
| Protective enzymes against activated oxygen species in wheat (Triticum aestivum L.) seedlings: responses to cold acclimation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhslOqsLs%3D&md5=435e7afc5607bf4f492bdbb6661b26e7CAS |
Sokal RR, Rohlf FJ (1969) ‘The principles and practice of statistics in biological research.’ (WH Freeman & Co.: San Francisco, CA, USA)
Solanke AU, Sharma MK, Tyagi AK, Sharma AK (2009) Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato. Molecular Genetics and Genomics 282, 153–164.
| Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVKlu7o%3D&md5=c0084ba127444fc8a9a41ac398cf8c57CAS |
Soni R, Carmichael JP, Murray JA (1993) Parameters affecting lithium acetate-mediated transformation of Saccharomyces cerevisiae and development of a rapid and simplified procedure. Current Genetics 24, 455–459.
| Parameters affecting lithium acetate-mediated transformation of Saccharomyces cerevisiae and development of a rapid and simplified procedure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhslWi&md5=196d37e8af7b5871c4113dcabf568cceCAS |
Sreedharan S, Shekhawat UKS, Ganapathi TR (2012) MusaSAP1, a A20/AN1 zinc finger gene from banana functions as a positive regulator in different stress responses. Plant Molecular Biology 80, 503–517.
| MusaSAP1, a A20/AN1 zinc finger gene from banana functions as a positive regulator in different stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFSqsLbE&md5=58c21ac27a45bbf1fe0bd8daf24576d2CAS |
Ströher E, Wang XJ, Roloff N, Klein P, Husemann A, Dietz KJ (2009) Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Molecular Plant 2, 357–367.
| Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Suetake I, Shinozaki F, Miyagawa J, Takeshima H, Tajima S (2004) DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction. Journal of Biological Chemistry 279, 27816–27823.
| DNMT3L stimulates the DNA methylation activity of Dnmt3a and Dnmt3b through a direct interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvFGmsr8%3D&md5=37f135665b2890996b2d9a31eaf18514CAS |
Sun ZYJ, Bhanu MK, Allan MG, Arthanari H, Wagner G, Hanna J (2016) Solution structure of the Cuz1 AN1 zinc finger domain: an exposed LDFLP motif defines a subfamily of AN1 proteins. PLoS One 11, e0163660
| Solution structure of the Cuz1 AN1 zinc finger domain: an exposed LDFLP motif defines a subfamily of AN1 proteins.Crossref | GoogleScholarGoogle Scholar |
Taipale M, Jarosz DF, Lindquist S (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nature Reviews. Molecular Cell Biology 11, 515–528.
| HSP90 at the hub of protein homeostasis: emerging mechanistic insights.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntFSmt7c%3D&md5=3da65cf72dc1da94b87f95332017ee54CAS |
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
| MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=0304eb60d01d281ee6e41bc3d051047bCAS |
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Biology 50, 571–599.
| Plant cold acclimation: freezing tolerance genes and regulatory mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1yktrw%3D&md5=c0c855375f5a25f1d24d0268b82b44eeCAS |
Verdaguer B, Kochko A, Beachy RN, Fauquet C (1996) Isolation and expression in transgenic tobacco and rice plants, of the cassava vein mosaic virus (CVMV) promoter. Plant Molecular Biology 31, 1129–1139.
| Isolation and expression in transgenic tobacco and rice plants, of the cassava vein mosaic virus (CVMV) promoter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmvFWqt7s%3D&md5=5252884eac8212dc558c4c2699d7eeb2CAS |
Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger (s) in rice and their phylogenetic relationship with Arabidopsis. Molecular Genetics and Genomics 276, 565–575.
| Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger (s) in rice and their phylogenetic relationship with Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKiu7nF&md5=9e4e73b7de831238d019d0453cf04300CAS |
Vij S, Tyagi AK (2008) A20/AN1 zinc-finger domain-containing proteins in plants and animals represent common elements in stress response. Functional & Integrative Genomics 8, 301–307.
| A20/AN1 zinc-finger domain-containing proteins in plants and animals represent common elements in stress response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntVWiurk%3D&md5=2950f14df58fba9f5909e408dbf9c680CAS |
Wang Y, Zhang L, Zhang L, Xing T, Peng J, Sun S, Chen G, Wang X (2013) A novel stress-associated protein SbSAP14 from Sorghum bicolor confers tolerance to salt stress in transgenic rice. Molecular Breeding 32, 437–449.
| A novel stress-associated protein SbSAP14 from Sorghum bicolor confers tolerance to salt stress in transgenic rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlaktLjF&md5=c8f61f755e863c05e5472158f7c617a8CAS |
Zouari N, Ben Saad R, Legavre T, Azaza J, Sabau X, Jaoua M, Masmoudi K, Hassairi A (2007) Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Gene 404, 61–69.
| Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFyku7nE&md5=8bf2ca0dc77fb89a40d8fc92f79d0e60CAS |
Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. Evolving Genes and Proteins 97, 97–166.
| Evolutionary divergence and convergence in proteins.Crossref | GoogleScholarGoogle Scholar |
