Endogenous accumulation of glycine betaine confers improved low temperature resistance on transplastomic potato plants
Qiping Song A , Lili You B , Yang Liu A , Jiang Zhang B C and Xinghong Yang
A C
+ Author Affiliations
- Author Affiliations
A College of Life Science, State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, Shandong Agricultural University, Taian 271018, China.
B State Key Laboratory of Biocatalysis and Enzyme Engineering, College of Life Sciences, Hubei University, Wuhan 430062, China.
C Corresponding author. Email: xhyang@sdau.edu.cn; zhangjiang@hubu.edu.cn
Functional Plant Biology 47(12) 1105-1116 https://doi.org/10.1071/FP20059
Submitted: 28 February 2020 Accepted: 4 June 2020 Published: 21 July 2020
Abstract
Glycine betaine (GB) plays a crucial role in plant response to abiotic stress, and its accumulation in chloroplasts is more effective than in the cytosol in improving the resistance of transgenic plants. Here, we report that the codA gene from Arthrobacter globiformis, which encodes a choline oxidase catalysing the conversion of choline to GB, was successfully introduced into the plastid genome of potato (Solanum tuberosum L.). Transgenic plants with plastid expression of codA showed increased tolerance to low temperature stress compared with the wild type (WT). Further studies revealed that under low temperature stress condition, transgenic plants presented a significantly higher photosynthetic performance by regulating the electron transport and energy distribution in PSII, and higher antioxidant enzyme activities and lower O2– and H2O2 accumulation than did the WT plants. A higher expression of the COR genes was also observed in transgenic plants. Our results suggest that chloroplast biosynthesis of GB could be an effective strategy for the engineering of plants with increased resistance to low temperature stress.
Additional keywords: codA, low temperature stress, PSI and PSII efficiency, ROS, Solanum tuberosum.
References
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 | 15377225PubMed |
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
| The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.Crossref | GoogleScholarGoogle Scholar | 15012221PubMed |
Balouchi HR (2010) Screening wheat parents of mapping population for heat and drought tolerance, detection of wheat genetic variation. International Journal of Biological, Biomolecular, Agricultural, Food and Biotechnological Engineering 6, 56–66.
Bartoli CG, Simontacchi M, Tambussi E, Beltrano J, Montaldi E, Puntarulo S (1999) Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves. Journal of Experimental Botany 50, 375–383.
| Drought and watering-dependent oxidative stress: effect on antioxidant content in Triticum aestivum L. leaves.Crossref | GoogleScholarGoogle Scholar |
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504.
| Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins.Crossref | GoogleScholarGoogle Scholar | 24233012PubMed |
Chen THH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends in Plant Science 13, 499–505.
| Glycinebetaine: an effective protectant against abiotic stress in plants.Crossref | GoogleScholarGoogle Scholar |
Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 8, 175
| An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice.Crossref | GoogleScholarGoogle Scholar | 17577400PubMed |
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212, 808–816.
| In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley.Crossref | GoogleScholarGoogle Scholar | 11346955PubMed |
Ding Y, Jia Y, Shi Y, Zhang X, Song C, Gong Z, Yang S (2018) OST1‐mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO Journal 37, e98228
| OST1‐mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses.Crossref | GoogleScholarGoogle Scholar | 29507081PubMed |
Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxyl ammonium chloride: a simple assay for superoxide dismutase. Analytical Biochemistry 70, 616–620.
| Inhibition of nitrite formation from hydroxyl ammonium chloride: a simple assay for superoxide dismutase.Crossref | GoogleScholarGoogle Scholar | 817618PubMed |
Feng Y, Zhang M, Guo Q, Wang G, Gong J, Xu Y, Wang W (2014) Manipulation of monoubiquitin improves chilling tolerance in transgenic tobacco (Nicotiana tabacum). Plant Physiology and Biochemistry 75, 138–144.
| Manipulation of monoubiquitin improves chilling tolerance in transgenic tobacco (Nicotiana tabacum).Crossref | GoogleScholarGoogle Scholar | 24445300PubMed |
Geissler N, Hussin S, Koyro HW (2009) Interactive effects of NaCl salinity and elevated atmospheric CO2 concentration on growth, photosynthesis, water relations and chemical composition of the potential cash crop halophyte Aster tripolium L. Environmental and Experimental Botany 65, 220–231.
| Interactive effects of NaCl salinity and elevated atmospheric CO2 concentration on growth, photosynthesis, water relations and chemical composition of the potential cash crop halophyte Aster tripolium L.Crossref | GoogleScholarGoogle Scholar |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
| Superoxide dismutases: I. Occurrence in higher plants.Crossref | GoogleScholarGoogle Scholar | 16659839PubMed |
Guo YY, Tian SS, Liu SS, Wang WQ, Sui N (2018) Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 56, 861–872.
| Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress.Crossref | GoogleScholarGoogle Scholar |
Han Y, Chen Y, Yin S, Zhang M, Wang W (2015) Overexpression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants. Journal of Plant Physiology 173, 62–71.
| Overexpression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 25462079PubMed |
Hayashi H, Alia , Mustardy L, Deshnium P, Ida M, Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycine betaine and enhanced tolerance to salt and cold stress. The Plant Journal 12, 133–142.
| Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycine betaine and enhanced tolerance to salt and cold stress.Crossref | GoogleScholarGoogle Scholar | 9263456PubMed |
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125, 189–198.
| Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |
Huang S, Zuo T, Ni WZ (2020) Important roles of glycinebetaine in stabilizing the structure and function of the photosystem II complex under abiotic stresses. Planta 251, 36
| Important roles of glycinebetaine in stabilizing the structure and function of the photosystem II complex under abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 31903497PubMed |
Kang H, Zhang M, Zhou S, Guo Q, Chen F, Wu J, Wang W (2016) Overexpression of wheat ubiquitin gene, Ta-Ub2, improves abiotic stress tolerance of Brachypodium distachyon. Plant Science 248, 102–115.
| Overexpression of wheat ubiquitin gene, Ta-Ub2, improves abiotic stress tolerance of Brachypodium distachyon.Crossref | GoogleScholarGoogle Scholar | 27181952PubMed |
Li S, Li F, Wang J, Zhang W, Meng Q, Chen THH, Murata N, Yang X (2011) Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings. Plant, Cell & Environment 34, 1931–1943.
| Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings.Crossref | GoogleScholarGoogle Scholar |
Li M, Li Z, Li S, Guo S, Meng Q, Li G, Yang X (2014a) Genetic engineering of glycine betaine biosynthesis reduces the heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato. Plant Molecular Biology Reporter 32, 42–51.
| Genetic engineering of glycine betaine biosynthesis reduces the heat-enhanced photoinhibition by enhancing antioxidative defense and alleviating lipid peroxidation in tomato.Crossref | GoogleScholarGoogle Scholar |
Li M, Guo S, Xu Y, Meng Q, Li G, Yang X (2014b) Glycine betaine-mediated potentiation of HSP gene expression involved calcium signaling pathways in tobacco exposed to NaCl stress. Physiologia Plantarum 150, 63–75.
| Glycine betaine-mediated potentiation of HSP gene expression involved calcium signaling pathways in tobacco exposed to NaCl stress.Crossref | GoogleScholarGoogle Scholar | 23627631PubMed |
Li J, Wang YQ, Yu B, Song QP, Liu Y, Chen THH, Li G, Yang XH (2018) Ectopic expression of StCBF1 and ScCBF1 have different functions in response to freezing and drought stresses in Arabidopsis. Plant Science 270, 221–233.
| Ectopic expression of StCBF1 and ScCBF1 have different functions in response to freezing and drought stresses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29576075PubMed |
Li D, Zhang T, Wang M, Liu Y, Brestic M, Chen THH, Yang X (2019) Genetic engineering of the biosynthesis of glycine betaine modulates phosphate homeostasis by regulating phosphate acquisition in tomato. Frontiers in Plant Science 9, 1995
| Genetic engineering of the biosynthesis of glycine betaine modulates phosphate homeostasis by regulating phosphate acquisition in tomato.Crossref | GoogleScholarGoogle Scholar | 30687378PubMed |
Liu Z, Jia Y, Ding Y, Shi Y, Li Z, Guo Y, Gong Z, Yang S (2017) Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Molecular Cell 66, 117–128.e5.
Maehly AC, Chance B (1954) Catalases and peroxidases. Methods of Biochemical Analysis 1, 357–424.
Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin‐deactivating gene, GA2ox7, under high‐salinity stress in Arabidopsis. The Plant Journal 56, 613–626.
| The DDF1 transcriptional activator upregulates expression of a gibberellin‐deactivating gene, GA2ox7, under high‐salinity stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18643985PubMed |
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Archives of Biochemistry and Biophysics 444, 139–158.
| Cold, salinity and drought stresses: an overview.Crossref | GoogleScholarGoogle Scholar | 16309626PubMed |
Mäkelä P, Kärkkäinen J, Somersalo S (2000) Effect of glycinebetaine on chloroplast ultrastructure, chlorophyll and protein content, and RuBPCO activities in tomato grown under drought or salinity. Biologia Plantarum 43, 471–475.
| Effect of glycinebetaine on chloroplast ultrastructure, chlorophyll and protein content, and RuBPCO activities in tomato grown under drought or salinity.Crossref | GoogleScholarGoogle Scholar |
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
| Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 10938857PubMed |
Meng C, Sui N (2019) Overexpression of maize MYB-IF35 increases chilling tolerance in Arabidopsis. Plant Physiology and Biochemistry 135, 167–173.
| Overexpression of maize MYB-IF35 increases chilling tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30553138PubMed |
Nayyar H, Chander K, Kumar S, Bains T (2005) Glycine betaine mitigates cold stress damage in chickpea. Agronomy for Sustainable Development 25, 381–388.
| Glycine betaine mitigates cold stress damage in chickpea.Crossref | GoogleScholarGoogle Scholar |
Niu X, Xiong F, Liu J, Sui Y, Zeng Z, Lu BR, Liu Y (2014) Co-expression of ApGSMT and ApDMT promotes biosynthesis of glycine betaine in rice (Oryza sativa L.) and enhances salt and cold tolerance. Environmental and Experimental Botany 104, 16–25.
| Co-expression of ApGSMT and ApDMT promotes biosynthesis of glycine betaine in rice (Oryza sativa L.) and enhances salt and cold tolerance.Crossref | GoogleScholarGoogle Scholar |
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249–279.
| Ascorbate and glutathione: keeping active oxygen under control.Crossref | GoogleScholarGoogle Scholar | 15012235PubMed |
Ohnishi N, Murata N (2006) Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of D1 protein during photoinhibition in Synechococcus sp. PCC 7942. Plant Physiology 141, 758–765.
| Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of D1 protein during photoinhibition in Synechococcus sp. PCC 7942.Crossref | GoogleScholarGoogle Scholar | 16632587PubMed |
Park EJ, Jeknic Z, Chen THH (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant & Cell Physiology 47, 706–714.
| Exogenous application of glycinebetaine increases chilling tolerance in tomato plants.Crossref | GoogleScholarGoogle Scholar |
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology 35, 15–44.
| Photoinhibition of photosynthesis induced by visible light.Crossref | GoogleScholarGoogle Scholar |
Prasad KVSK, Saradhi (2004) Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. Plant Science 166, 1197–1212.
| Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts.Crossref | GoogleScholarGoogle Scholar |
Quan R, Shang M, Zhang H, Zhao Y, Zhang J (2004) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Science 166, 141–149.
| Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize.Crossref | GoogleScholarGoogle Scholar |
Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant, Cell & Environment 25, 163–171.
| The role of glycine betaine in the protection of plants from stress: clues from transgenic plants.Crossref | GoogleScholarGoogle Scholar |
Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Molecular Biology 66, 361–378.
| Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes.Crossref | GoogleScholarGoogle Scholar | 18158584PubMed |
Scheller HV, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221, 5–8.
| Photoinhibition of photosystem I.Crossref | GoogleScholarGoogle Scholar | 15782347PubMed |
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571–599.
| Plant cold acclimation: freezing tolerance genes and regulatory mechanisms.Crossref | GoogleScholarGoogle Scholar | 15012220PubMed |
Tian F, Wang W, Liang C, Wang X, Wang G, Wang W (2017) Overaccumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress. The Crop Journal 5, 73–82.
| Overaccumulation of glycine betaine makes the function of the thylakoid membrane better in wheat under salt stress.Crossref | GoogleScholarGoogle Scholar |
Tóth SZ, Schansker G, Kissimon J, Kovács L, Strasser RJ (2005) Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.). Journal of Plant Physiology 162, 181–194.
| Biophysical studies of photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 15779828PubMed |
Wang GP, Hui Z, Li F, Zhao MR, Zhang J, Wang W (2010) Improvement of heat and drought photosynthetic tolerance in wheat by overaccumulation of glycine betaine. Plant Biotechnology Reports 4, 213–222.
| Improvement of heat and drought photosynthetic tolerance in wheat by overaccumulation of glycine betaine.Crossref | GoogleScholarGoogle Scholar |
Wei D, Zhang W, Wang C, Meng Q, Li G, Chen THH, Yang X (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Science 257, 74–83.
| Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants.Crossref | GoogleScholarGoogle Scholar | 28224920PubMed |
Xie Y, Chen P, Yan Y, Bao C, Li X, Wang L, Shen X, Li H, Liu X, Niu C, Zhu C, Fang N, Shao Y, Zhao T, Yu J, Zhu J, Xu L, van Nocker S, Ma F, Guan Q (2018) An atypical R2R3 MYB transcription factor increases cold hardiness by CBF‐dependent and CBF‐independent pathways in apple. New Phytologist 218, 201–218.
| An atypical R2R3 MYB transcription factor increases cold hardiness by CBF‐dependent and CBF‐independent pathways in apple.Crossref | GoogleScholarGoogle Scholar | 29266327PubMed |
Yang X, Lu C (2006) Effects of exogenous glycinebetaine on growth, CO2 assimilation, and photosystem II photochemistry of maize plants. Physiologia Plantarum 127, 593–602.
| Effects of exogenous glycinebetaine on growth, CO2 assimilation, and photosystem II photochemistry of maize plants.Crossref | GoogleScholarGoogle Scholar |
Yang X, Wen X, Gong H, Lu Q, Yang Z, Tang Y, Liang Z, Lu C (2007) Genetic engineering of the biosynthesis of glycine betaine enhances thermo tolerance of photosystem II in tobacco plants. Planta 225, 719–733.
| Genetic engineering of the biosynthesis of glycine betaine enhances thermo tolerance of photosystem II in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 16953431PubMed |
Yang X, Liang Z, Wen X, Lu C (2008) Genetic engineering of the biosynthesis of glycine betaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Molecular Biology 66, 73–86.
| Genetic engineering of the biosynthesis of glycine betaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 17975734PubMed |
Yang DY, Ma NN, Zhuang KY, Zhu SB, Liu ZM, Yang XH (2017) Overexpression of tomato SlGGP-LIKE gene improves tobacco tolerance to methyl viologen mediated oxidative stress. Journal of Plant Physiology 209, 31–41.
| Overexpression of tomato SlGGP-LIKE gene improves tobacco tolerance to methyl viologen mediated oxidative stress.Crossref | GoogleScholarGoogle Scholar | 28012364PubMed |
Yang Z, Li JL, Liu LN, Xie Q, Sui N (2020) Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum. Frontiers in Plant Science 10, 1722
| Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum.Crossref | GoogleScholarGoogle Scholar | 32010174PubMed |
You L, Song Q, Wu Y, Li S, Jiang C, Chang L, Yang X, Zhang J (2019) Accumulation of glycine betaine in transplastomic potato plants expressing choline oxidase confers improved drought tolerance. Planta 249, 1963–1975.
| Accumulation of glycine betaine in transplastomic potato plants expressing choline oxidase confers improved drought tolerance.Crossref | GoogleScholarGoogle Scholar | 30900084PubMed |
Yu CW, Murphy TM, Sung WW, Lin CH (2002) H2O2 treatment induces glutathione accumulation and chilling tolerance in mung bean. Functional Plant Biology 29, 1081–1087.
| H2O2 treatment induces glutathione accumulation and chilling tolerance in mung bean.Crossref | GoogleScholarGoogle Scholar |
Zhang XY, Liang C, Wang GP, Luo Y, Wang W (2010) The protection of wheat plasma membrane under cold stress by glycine betaine overproduction. Biologia Plantarum 54, 83–88.
| The protection of wheat plasma membrane under cold stress by glycine betaine overproduction.Crossref | GoogleScholarGoogle Scholar |
Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2011) Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K‐1 leaves. Physiologia Plantarum 143, 396–407.
| Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K‐1 leaves.Crossref | GoogleScholarGoogle Scholar | 21883255PubMed |
Zhang T, Liang J, Wang M, Li D, Liu Y, Chen THH, Yang X (2019) Genetic engineering of the biosynthesis of glycinebetaine enhances the fruit development and size of tomato. Plant Science 280, 355–366.
| Genetic engineering of the biosynthesis of glycinebetaine enhances the fruit development and size of tomato.Crossref | GoogleScholarGoogle Scholar | 30824015PubMed |
Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu J (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiology 171, 2744–2759.
Zhou R, Yu X, Ottosen CO, Rosenqvist E, Zhao L, Wang Y, Yu W, Zhao T, Wu Z (2017) Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress. BMC Plant Biology 17, 24
| Drought stress had a predominant effect over heat stress on three tomato cultivars subjected to combined stress.Crossref | GoogleScholarGoogle Scholar | 28122507PubMed |
