Overexpression of human peroxisomal enoyl-CoA delta isomerase2 HsPECI2, an ortholog of bamboo expressed during gregarious flowering alters salinity stress responses and polar lipid content in tobacco
Vineeta Rai A B , Shayan Sarkar A , Suresh Satpati C and Nrisingha Dey A DA Division of Gene Function and Regulation, Institute of Life Sciences, Nalco Square, Bhubaneswar, 751 023, Odisha, India.
B Present address: Department of Biosciences and Bioengineering, Indian Institute of Technology Bombay, Powai, Mumbai 400 076, Maharashtra, India.
C Division of Translational Research and Technology Development, Institute of Life Sciences, Nalco Square, Bhubaneswar, 751 023, Odisha, India.
D Corresponding author. Email: nrisinghad@gmail.com
Functional Plant Biology 43(3) 232-243 https://doi.org/10.1071/FP15292
Submitted: 18 September 2015 Accepted: 20 November 2015 Published: 1 February 2016
Abstract
Peroxisomal enoyl-CoA delta isomerase2 (PECI2) is one of the key enzymes that has critical role in lipid metabolism and plant development during salt stress. Seven out of ten tobacco plants overexpressing human PECI2 (HsPECI2) with PTS1-sequence showed hypersensitivity to salt. Under salt-stress, T2 transformed plants (HsPECI2) displayed reduced primary root, delayed shoot-growth, and visibly smaller rosette leaves turning pale yellow as compared to the pKYLX71 vector control plant. Also, we found altered reactive oxygen species (ROS) levels and reduced catalase activity in 100 mM sodium chloride (NaCl) treated HsPECI2 transformed plant compared with the pKYLX71 counterpart. ESI-MS/MS data showed that the polar lipids were differentially modulated upon salt treatment in HsPECI2 transformed and pKYLX71 plants as compared with the respective untreated counterpart. Notably, the levels of monogalactosyldiacylglycerol and phosphatidic acid varied significantly, whereas phosphatidylcholine, phosphatidylserine and digalactosyldiacylglycerol contents were moderately upregulated. In parallel, abscisic acid (ABA) responsiveness assay confirmed insensitivity of HsPECI2 transformed plant towards ABA. Overall our data proclaim that HsPECI2 play multifunctional role in normal development and response to salinity stress apart from its primary role in β-oxidation.
Additional keywords: exogenous ABA, lipid profiling, peroxisomal enoyl-CoA delta isomerase2, salinity stress, tobacco transgenic plants.
References
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell 15, 63–78.| Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtFentg%3D%3D&md5=d1db55a43c919d94d343d9759a984f36CAS | 12509522PubMed |
Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
| Catalase in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXltVKis7s%3D&md5=a787c8d94f03cc2abe3e410eac513bf6CAS | 6727660PubMed |
Afzal I, Basara SMA, Faooq M, Nawaz A (2006) Alleviation of salinity stress in spring wheat by hormonal priming with ABA, salicylic acid and ascorbic acid. International Journal of Agriculture and Biology 8, 23–28.
Allenbach L, Poirier Y (2000) Analysis of the alternative pathways for the β-oxidation of unsaturated fatty acids using transgenic plants synthesizing polyhydroxyalkanoates in peroxisomes. Plant Physiology 124, 1159–1168.
| Analysis of the alternative pathways for the β-oxidation of unsaturated fatty acids using transgenic plants synthesizing polyhydroxyalkanoates in peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlWqsr0%3D&md5=545a6f255cf64c342a75cb64ca18eba7CAS | 11080293PubMed |
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=99fa8bbb1f5b69ffca6fc56116a2dc3fCAS | 15377225PubMed |
Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: β-oxidation in signalling and development. Trends in Plant Science 11, 124–132.
| Chewing the fat: β-oxidation in signalling and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFyjsr0%3D&md5=778a092bf0c74d11299749954b595dd3CAS | 16490379PubMed |
Barta A, Sommengruber K, Thompson D, Hartmuth K, Matzke M, Matzke A (1986) The expression of a napoline synthase human growth hormone chimeric gene in transformed tobacco and sunflower callus tissue. Plant Molecular Biology 6, 347–357.
| The expression of a napoline synthase human growth hormone chimeric gene in transformed tobacco and sunflower callus tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XktF2rs7s%3D&md5=4d200ad35a509de9901a6f1f09bd1b43CAS | 24307385PubMed |
Benavides MP, Marconi PL, Gallego SM, Comba ME, Tomaro ML (2000) Relationship between antioxidant defence systems and salt tolerance in Solanum tuberosum. Australian Journal of Plant Physiology 27, 273–278.
Benhassaine-Kesri G, Aid F, Demandre C, Kader JC, Mazliak P (2002) Drought stress affects chloroplast lipid metabolism in rape (Brassica napus) leaves. Physiologia Plantarum 115, 221–227.
| Drought stress affects chloroplast lipid metabolism in rape (Brassica napus) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltVGmsrY%3D&md5=5bd91cf4d5195b9e0a8194186102b9b3CAS | 12060239PubMed |
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=405f112ae90ea1ae3fd1156830d6cf31CAS | 18026957PubMed |
Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=436242ae9b449e7335b086f00b7e6e5fCAS | 942051PubMed |
Chen HC, Hwang SG, Chen SM, Shii CT, Cheng WH (2011) Abscisic acid-mediated heterophylly is regulated by differential expression of 9-cis-epoxycarotenoid dioxygenase 3 in lilies. Plant & Cell Physiology 52, 1806–1821.
| Abscisic acid-mediated heterophylly is regulated by differential expression of 9-cis-epoxycarotenoid dioxygenase 3 in lilies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12rsrrM&md5=29fbb2d0f25d00cbc6fe3250561ac61bCAS |
Church GM, Gilbert W (1984) Genomic sequencing. Proceedings of the National Academy of Sciences of the United States of America 81, 1991–1995.
| Genomic sequencing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXkt1Sit7k%3D&md5=fe71c141dae222c49a4bfe1c09219820CAS | 6326095PubMed |
Cooper TG, Beevers HJ (1969) Beta oxidation in glyoxysomes from castor bean endosperm. The Journal of Biological Chemistry 224, 3514–3520.
Darwish E, Testerink C, Khalil M, El-Shihy O, Munnik T (2009) Phospholipid signaling responses in salt-stressed rice leaves. Plant & Cell Physiology 50, 986–997.
| Phospholipid signaling responses in salt-stressed rice leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtFSnsb4%3D&md5=87d319fc1cf9730fa33a60ddbf8711adCAS |
del Río LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López‐Huertas E, Hernández AJ (1998) The activated oxygen role of peroxisomes in senescence. Plant Physiology 116, 1195–1200.
| The activated oxygen role of peroxisomes in senescence.Crossref | GoogleScholarGoogle Scholar | 9536035PubMed |
Delesalle VA, Mazer SJ (1996) Nutrient levels and salinity affects gender and floral traits in autogamous Sperguleria marian. International Journal of Plant Sciences 157, 621–631.
| Nutrient levels and salinity affects gender and floral traits in autogamous Sperguleria marian.Crossref | GoogleScholarGoogle Scholar |
Dey N, Maiti IB (1999) Structure and promoter/leader deletion analysis of mirabilis mosaic virus (MMV) full length transcript promoter in transgenic plants. Plant Molecular Biology 40, 771–782.
| Structure and promoter/leader deletion analysis of mirabilis mosaic virus (MMV) full length transcript promoter in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFektLg%3D&md5=e14f8bae2b8b3a861d103d36398d9b39CAS | 10487212PubMed |
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=4328701d354ef2168477e78532717995CAS |
Du ZY, Xiao S, Chen QF, Chye ML (2010) Depletion of the membrane-associated acyl-coenzyme A-binding protein ACBP1 enhances the ability of cold acclimation in Arabidopsis. Plant Physiology 152, 1585–1597.
| Depletion of the membrane-associated acyl-coenzyme A-binding protein ACBP1 enhances the ability of cold acclimation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsF2ltrs%3D&md5=a278a04d31e91e62f28d1c1b27e2e704CAS | 20107029PubMed |
Edelbaum O, Stein D, Holland N, Gafni Y, Livneh O, Novick D, Rubinstein M, Sela I (1992) Expression of active human interferon-beta in transgenic plants. Journal of Interferon & Cytokine Research 12, 449–453.
| Expression of active human interferon-beta in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlejsg%3D%3D&md5=7f79fb34a7331ab6dece44b3ed9d5641CAS |
Fan W, Zhang M, Zhang H, Zhang P (2012) Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase. Plos One 7, e37344
| Improved tolerance to various abiotic stresses in transgenic sweet potato (Ipomoea batatas) expressing spinach betaine aldehyde dehydrogenase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnslyms7k%3D&md5=ee57d9e80eb914d7c712cbc7c2fd0f9aCAS | 22615986PubMed |
Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
| Improving crop salt tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1egtQ%3D%3D&md5=15fd10c082c113b67f5fda47e9e50420CAS | 14718494PubMed |
Fridovich I (1997) Superoxide anion radical (O2 •–), superoxide dismutases, and related matters. Journal of Biological Chemistry 272, 18515–18517.
| Superoxide anion radical (O2 •–), superoxide dismutases, and related matters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltVSgsrw%3D&md5=be0d26bcbd8d58660224dae899eab17aCAS | 9228011PubMed |
Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116, 571–580.
| Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1aju70%3D&md5=506776bc89741ede12b3fa8f934b3873CAS | 9490760PubMed |
Goepfert S, Vidoudez C, Tellgren-Roth C, Delessert S, Hiltunen JK, Poirier Y (2008) Peroxisomal Δ(3), Δ (2)-enoyl CoA isomerases and evolution of cytosolic paralogues in embryophytes. The Plant Journal 56, 728–742.
| Peroxisomal Δ(3), Δ (2)-enoyl CoA isomerases and evolution of cytosolic paralogues in embryophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGltQ%3D%3D&md5=884998f34489e766fa4334bd12c5d2cbCAS | 18657232PubMed |
Gossett DR, Millhollon EP, Lucas MC (1994) Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton. Crop Science 34, 706–714.
| Antioxidant response to NaCl stress in salt-tolerant and salt-sensitive cultivars of cotton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltlSiu7g%3D&md5=fa970e8a57e710269504bf63372f6b1aCAS |
Härtel H, Lokstein H, Dörmann P, Grimm B, Benning C (1997) Changes in the composition of the photosynthetic apparatus in the galactolipid deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiology 115, 1175–1184.
| Changes in the composition of the photosynthetic apparatus in the galactolipid deficient dgd1 mutant of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 9390443PubMed |
Hemavathi , Upadhyaya C, Akula N, Young K, Chun S, Kim D, Park S (2010) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnology Letters 32, 321–330.
| Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVKmsQ%3D%3D&md5=e7cc055dfe25b701515f9f78f04b0557CAS | 19821071PubMed |
Hiltunen J, Mursula A, Rottensteiner H, Wierenga R, Kastaniotis A, Gurvitz A (2003) The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae. FEMS Microbiology Reviews 27, 35–64.
| The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFCqsr8%3D&md5=ac948f99c65bc6f0ab6f8e416930bac6CAS | 12697341PubMed |
Hong Y, Zhang W, Wang X (2010) Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity. Plant, Cell & Environment 33, 627–635.
| Phospholipase D and phosphatidic acid signalling in plant response to drought and salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hu70%3D&md5=220cca3fa1dafb7591a701fbf76b5dd5CAS |
Jaspers P, Kangasjarvi J (2010) Reactive oxygen species in abiotic stress signaling. Physiologia Plantarum 138, 405–413.
| Reactive oxygen species in abiotic stress signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlOkt7s%3D&md5=94cc3d48c4677462e9a5a4e72a8d0de9CAS | 20028478PubMed |
Kachroo A, Kachroo P (2009) Fatty acid-derived signals in plant defense. Annual Review of Phytopathology 47, 153–176.
| Fatty acid-derived signals in plant defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1Gjt73O&md5=584e5748664ec5cb97ee3016cb174040CAS | 19400642PubMed |
Keskin BC, Sarikaya AT, Yuksel B, Memon AR (2010) Abscisic acid regulated gene expression in bread wheat. Annual Review of Phytopathology 4, 617–625.
Kindl H (1993) Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved. Biochimie 75, 225–230.
| Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXkt1Cmtb8%3D&md5=89cab33e6b7c29ae686041088aa031b8CAS | 8507684PubMed |
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO Journal 22, 2623–2633.
| NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkt1WrtLY%3D&md5=1b19593b0552608365fb26efced37abcCAS | 12773379PubMed |
Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. Journal of Plant Physiology 160, 347–353.
| Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVKqu7g%3D&md5=ded2f0acb4c33e9a31bcfde66854acb7CAS | 12756914PubMed |
Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annual Review of Plant Physiology and Plant Molecular Biology 49, 199–222.
| Abscisic acid signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVShsb8%3D&md5=6c7bc45993c39480fc3e07f0434fa0eeCAS | 15012233PubMed |
Li W, Dickman MB (2004) Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2. Biotechnology Letters 26, 87–95.
| Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1ehsw%3D%3D&md5=40c2817199dda1d2e7e1529ac7312493CAS | 15000473PubMed |
Liu G, Li X, Jin S, Liu X, Zhu L, Nie Y, Zhang X (2014) Overexpression of rice NAC gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton. PLoS One 9, e86895
| Overexpression of rice NAC gene SNAC1 improves drought and salt tolerance by enhancing root development and reducing transpiration rate in transgenic cotton.Crossref | GoogleScholarGoogle Scholar | 24489802PubMed |
Luo MJ, Smeland TE, Shoukry K, Schulz H (1994) Δ3,5, Δ2,4-Dienoyl-CoA isomerase from rat liver mitochondria. Purification and characterization of a new enzyme involved in the beta-oxidation of unsaturated fatty acids. Journal of Biological Chemistry 269, 2384–2388.
Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. Journal of Experimental Botany 63, 305–317.
| NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yms7vN&md5=71be06c4287b4222e1f93f572e5fff5aCAS | 21984648PubMed |
Mansour MMF, Van Hasselt PR, Kuiper PJC (1994) Plasma membrane lipid alterations induced by NaCl in winter wheat roots. Physiologia Plantarum 92, 473–478.
| Plasma membrane lipid alterations induced by NaCl in winter wheat roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitFersbg%3D&md5=90e7c03f018e79af119c4b4ae1148174CAS |
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453–467.
| Reactive oxygen species homeostasis and signalling during drought and salinity stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltV2hur8%3D&md5=42f2cbcf2143d1c8e9db6fbe95dfa198CAS |
Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226–228.
| Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Cgt77M&md5=c1e1b7e9ac39d90225177e9b3522e6f1CAS | 20798281PubMed |
Morales MA, Sánchez-Blanco MJ, Olmos E, Torrecillas A, Alarcón JJ (1998) Changes in the growth, leaf water relations and cell ultrastructure in Argyranthemum coronopifolium plants under saline conditions. Journal of Plant Physiology 153, 174–180.
| Changes in the growth, leaf water relations and cell ultrastructure in Argyranthemum coronopifolium plants under saline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlslKqurY%3D&md5=d009610b0ae659eac78ebf3814997584CAS |
Munnik T, Irvine RF, Musgrave A (1998) Phospholipid signalling in plants. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism 1389, 222–272.
| Phospholipid signalling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhsFaqu7o%3D&md5=2adfd1524384d9389cff218358b012e3CAS |
Munns R (2002) Salinity, growth and phytohormones. In ‘Salinity: environment–plants–molecules’. (Eds A Läuchli, U Lüttge), pp. 271–290. (Kluwer Academic Publishers: Dordrecht, the Netherlands)
Norberg P, Engstrom L, Nilsson R, Liljenberg C (1992) Phase behavior and molecular species composition of oat root plasma membrane lipids: influence of induced dehydration tolerance. Biochimica et Biophysica Acta- Biomembranes 1112, 52–56.
| Phase behavior and molecular species composition of oat root plasma membrane lipids: influence of induced dehydration tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitlShsL4%3D&md5=9916501bc4ae12b424723a96351220deCAS |
Nyathi Y, Baker A (2006) Plant peroxisomes as a source of signalling molecules. Biochimica et Biophysica Acta - Molecular Cell Research 1763, 1478–1495.
| Plant peroxisomes as a source of signalling molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlakurzK&md5=2315730c85b9054f87fe74f74a737009CAS |
Ozfidan C, Turkan I, Sekmen AH, Seckin B (2012) Abscisic acid-regulated responses of aba2-1 under osmotic stress: the abscisic acid-inducible antioxidant defence system and reactive oxygen species production. Plant Biology 14, 337–346.
| Abscisic acid-regulated responses of aba2-1 under osmotic stress: the abscisic acid-inducible antioxidant defence system and reactive oxygen species production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltV2gt7c%3D&md5=edfcb2b92a23f264dc01745703b5f8c2CAS | 21973087PubMed |
Palosaari PM, Kilponen JM, Sormunen RT, Hassinen E, Hiltunen JK (1990) Δ3,Δ2-Enoyl-CoA isomerases. Characterization of the mitochondrial isoenzyme in the rat. Journal of Biological Chemistry 265, 3347–3353.
Panavas T, Rubinstein B (1998) Oxidative events during programmed cell death of daylily (Hemerocallis hybrid) petals. Plant Science 134, 1–9.
Pei ZM, Kuchitsu K, Ward JM, Schwarz M, Schroeder I (1997) Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants. Plant, Cell & Environment 9, 409–423.
| Differential abscisic acid regulation of guard cell slow anion channels in Arabidopsis wild-type and abi1 and abi2 mutants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXitFWqu7c%3D&md5=0c94e40cb7455f706561d0b23aac86e2CAS |
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Research 29, e45
| A new mathematical model for relative quantification in real-time RT–PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=79c488a0ef278e2273a84ed788c02263CAS | 11328886PubMed |
Poirier Y, Antonenkov VD, Glumoff T, Hiltunen JK (2006) Peroxisomal β-oxidation–a metabolic pathway with multiple functions. Biochimica et Biophysica Acta - Molecular Cell Research 1763, 1413–1426.
Rai V, Dey N (2012) Identification of programmed cell death related genes in bamboo. Gene 497, 243–248.
| Identification of programmed cell death related genes in bamboo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFWktL4%3D&md5=340029e5a5eb9dedfb7642a724647bf9CAS | 22326529PubMed |
Rai V, Ghosh JS, Pal A, Dey N (2011) Identification of genes involved in bamboo fiber development. Gene 478, 19–27.
| Identification of genes involved in bamboo fiber development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltVGmu7s%3D&md5=a98715018c3fea4205718f3894a73bd6CAS | 21272623PubMed |
Rao MS, Reddy JK (2001) Peroxisomal beta-oxidation and steatohepatitis. Seminars in Liver Disease 21, 43–56.
| Peroxisomal beta-oxidation and steatohepatitis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXivFGns7c%3D&md5=97ca47e2ea55b158662b42a84e67dd19CAS | 11296696PubMed |
Reifarth F, Christen G, Seeliger AG, Dörmann P, Benning C, Renger G (1997) Modification of the water oxidizing complex in leaves of the dgd1 mutant of Arabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol. Biochemistry 36, 11769–11776.
| Modification of the water oxidizing complex in leaves of the dgd1 mutant of Arabidopsis thaliana deficient in the galactolipid digalactosyldiacylglycerol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlvVCntb8%3D&md5=6372fc535028467a3b2f0d70e84282f1CAS | 9305967PubMed |
Reumann S, Ma C, Lemke S, Babujee L (2004) AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes. Plant Physiology 136, 2587–2608.
| AraPerox. A database of putative Arabidopsis proteins from plant peroxisomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrurY%3D&md5=bd1df058769b207ce67c2883a9d5e523CAS | 15333753PubMed |
Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374–380.
Sambrook J, Fitsch E, Maniatis T (1989) ‘Molecular cloning: a laboratory manual.’ (Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY)
Schardl CL, Byrd AD, Benzion G, Altschuler MA, Hildebrand DF, Hunt AG (1987) Design and construction of a versatile system for the expression of foreign genes in plants. Gene 61, 1–11.
| Design and construction of a versatile system for the expression of foreign genes in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhtVOitbk%3D&md5=a6c48bd8cc9164cf4fb6e5fe919e4768CAS | 3443303PubMed |
Swamy PM, Smith BN (1999) Role of abscisic acid in plant stress tolerance. Current Science 76, 1220–1227.
Torres MA, Dangl JL, Jones JD (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences of the United States of America 99, 517–522.
| Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xlt1CqsQ%3D%3D&md5=59c35b06495f04502c176a2b28154f05CAS | 11756663PubMed |
Turek I, Marondedze C, Wheeler JI, Gehring C, Irving HR (2014) Plant natriuretic peptides induce proteins diagnostic for an adaptive response to stress. Frontiers in Plant Science 5, 661
| Plant natriuretic peptides induce proteins diagnostic for an adaptive response to stress.Crossref | GoogleScholarGoogle Scholar | 25505478PubMed |
Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods in Enzymology 428, 419–438.
| Mechanisms of high salinity tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCisLY%3D&md5=bd57f27e0c71f38b6799f35800339d70CAS | 17875432PubMed |
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress response. Journal of Biological Chemistry 277, 31994–32002.
| Profiling membrane lipids in plant stress response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslOqu7w%3D&md5=bf1430de24a9e6311c0411b74bffa77dCAS | 12077151PubMed |
Xiao S, Gao W, Chen QF, Ramalingam S, Chye ML (2008) Overexpression of membrane-associated acyl-CoA-binding protein ACBP1 enhances lead tolerance in Arabidopsis. The Plant Journal 54, 141–151.
| Overexpression of membrane-associated acyl-CoA-binding protein ACBP1 enhances lead tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXltlertbY%3D&md5=fdbfdd1e85b9233b1e152e101bd7fe82CAS | 18182029PubMed |
Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Developmental Cell 1, 771–781.
| Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptFOntbY%3D&md5=df4c0971bb61e92c4da5fafd75f47f9aCAS | 11740939PubMed |
Yang YL, Xu SJ, An LZ, Chen NL (2007) NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat. Journal of Plant Physiology 164, 1429–1435.
| NADPH oxidase-dependent hydrogen peroxide production, induced by salinity stress, may be involved in the regulation of total calcium in roots of wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlKkt7fL&md5=12032b15bc86e23725fbdb2c23aed124CAS |
Yang Y, Tang RJ, Jiang CM, Li B, Kang T, Liu H, Zhao N, Ma XJ, Yang L, Chen SL, Zhang HX (2015) Overexpression of the PtSOS2 gene improves tolerance to salt stress in transgenic poplar plants. Plant Biotechnology Journal 13, 962–973.
| Overexpression of the PtSOS2 gene improves tolerance to salt stress in transgenic poplar plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtl2murvI&md5=6bfe833bc6b6ef13a0144ce4c70d84f7CAS | 25641517PubMed |
Ye N, Jia L, Zhang J (2012) ABA signal in rice under stress conditions. Rice 5, 1
| ABA signal in rice under stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XovVWrtbY%3D&md5=da4d9dc2832affcb3b4dfd564e6fcd29CAS | 24764501PubMed |
Yordanov I, Velikova V, Tsonev T (2003) Plant responses to drought and stress tolerance. Bulgarian Journal of Plant Physiology Special issue, 187–206.
Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JD, Doke N (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. The Plant Cell 15, 706–718.
| Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVektLc%3D&md5=814e2e7a19fd61633e6a0b5582edde4dCAS | 12615943PubMed |
Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J, Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytologist 188, 762–773.
| Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFKnurzN&md5=be3f9d4d53439d3390c4f177074e3401CAS | 20796215PubMed |
Zhang D, Yu W, Geisbrecht BV, Gould SJ, Sprecher H, Schulz H (2002) Functional characterization of Δ3, Δ2-enoyl-CoA isomerases from rat liver. Journal of Biological Chemistry 277, 9127–9132.
| Functional characterization of Δ3, Δ2-enoyl-CoA isomerases from rat liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xitl2ksrc%3D&md5=ada5d2ec5e1ea6de3b8abcfc0cee8b7dCAS | 11781327PubMed |
Zhang H, Zhai J, Mo J, Li D, Song F (2012) Overexpression of rice sphingosine-1-phoshpate lyase gene OsSPL1 in transgenic tobacco reduces salt and oxidative stress tolerance. Journal of Integrative Plant Biology 54, 652–662.
| Overexpression of rice sphingosine-1-phoshpate lyase gene OsSPL1 in transgenic tobacco reduces salt and oxidative stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Glu7jE&md5=301cd5cab85822981c07429eaaa294f3CAS | 22889013PubMed |
Zhang J, Liu H, Sun J, Li B, Zhu Q, Chen S, Zhang H (2012) Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PLoS One 7, e30355
| Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVyrsb0%3D&md5=4da08a06007a86840de791c1e8381874CAS | 22279586PubMed |
Zolman BK, Martinez N, Millius A, Adham AR, Bartel B (2008) Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes. Genetics 180, 237–251.
| Identification and characterization of Arabidopsis indole-3-butyric acid response mutants defective in novel peroxisomal enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1aqtrbF&md5=17732d5de6ad5e37714d90267e7fdc1eCAS | 18725356PubMed |