Advertisement

Roles of Endogenous Glycinebetaine in Plant Abiotic Stress Responses

  • Pirjo S. A. MäkeläEmail author
  • Kari Jokinen
  • Kristiina Himanen
Chapter

Abstract

Studies of plant adaptation to saline or dry environments have for several years recognized the role of quaternary ammonium and tertiary sulfonium compounds as nontoxic compatible solutes. One of the most studied compounds is glycinebetaine (GB), earlier known as lycine or oxyneurine. GB is a nontoxic, odorless, tasteless, and colorless amino acid derivative. Several plant species accumulate GB naturally as a response to abiotic stresses. However, many crop species are not able to synthesize GB in physiologically meaningful concentrations. On the other hand, halophytes, plants that can tolerate a high concentration of salt in the soil, are known to synthesize GB in low concentrations even when they are not experiencing any stress. GB is synthesized in chloroplasts from choline via a two-step oxidation reaction. This synthesis pathway has been the target in many attempts to either introduce or increase GB synthesis in plants by a transgenesis approach. However, in many cases the availability of choline obtained through photorespiration has restricted GB synthesis. Furthermore, availability of nitrogen can also restrict GB synthesis, since GB contains approximately 12% nitrogen. GB has so far been considered a relatively inert compound in plants. Since GB does not interact with metabolic pathways in the plant, it remains available at the cellular level for its use. Thus, it can be hypothesized that plants could be able to utilize nitrogen through GB metabolism, for example, during stress recovery. On the other hand, GB synthesis is energetically expensive for plants. Synthesis of 1 GB mole costs approximately 50 ATP moles, whereas synthesis of 1 sucrose mole costs approximately 30 ATP moles. In comparison, osmotic adjustment with inorganic ions is less costly, e.g., 1 NaCl mole equals 3.5 ATP moles. The aim of this chapter is to provide an overview of endogenous GB in plants and the transgenesis approach for introducing and improving GB synthesis in plants.

References

  1. Annunziata MG, Ciarmiello LF, Woodrow P, Dell’Aversana E, Carillo P (2019) Spatial and temporal profile of glycine betaine accumulation in plants under abiotic stresses. Front Plant Sci 10:230.  https://doi.org/10.3389/fpls.2019.00230CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antoniou C, Savvides A, Christou A, Fotopoulos V (2016) Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr Opin Plant Biol 33:101–107.  https://doi.org/10.1016/j.pbi.2016.06.020CrossRefPubMedGoogle Scholar
  3. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216.  https://doi.org/10.1016/j.envexpbot.2005.12.006CrossRefGoogle Scholar
  4. Bäurle I (2016) Plant heat adaptation: priming in response to heat stress. F1000Res 5:pii: F1000 Faculty Rev-694.  https://doi.org/10.12688/f1000research.7526.1CrossRefGoogle Scholar
  5. Bot AJ, Nachtergaele FO, Young A (2000) Land resource potential and constraints at regional and country levels. World Soil Resources Reports 90. Land and Water Development Division, FAO, RomeGoogle Scholar
  6. Boyer JS (1982) Plant productivity and environment. Science 218:443–448.  https://doi.org/10.1126/science.218.4571.443CrossRefPubMedGoogle Scholar
  7. Burg MB, Ferraris JD (2008) Intracellular organic osmolytes: function and regulation. J Biol Chem 283:7309–7313.  https://doi.org/10.1074/jbc.R700042200CrossRefPubMedPubMedCentralGoogle Scholar
  8. Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Funct Plant Biol 35:412–426.  https://doi.org/10.1071/FP08108CrossRefGoogle Scholar
  9. Carrillo-Campos J, Riveros-Rosas H, Rodríguez-Sotres R, Muñoz-Clares RA (2018) Bona fide choline monoxygenases evolved in Amaranthaceae plants from oxygenases of unknown function: evidence from phylogenetics, homology modeling and docking studies. PLoS One 13:e0204711.  https://doi.org/10.1371/journal.pone.0204711CrossRefPubMedPubMedCentralGoogle Scholar
  10. Castiglioni P, Bell E, Lund A, Rosenberg AF, Galligan M, Hinchey BS, Bauer S, Nelson D, Bensen RJ (2018) Identification of GB1, a gene whose constitutive overexpression increases glycinebetaine content in maize and soybean. Plant Direct 2:e00040.  https://doi.org/10.1002/pld3.40CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chen THH, Murata N (2011) Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20.  https://doi.org/10.1111/j.1365-3040.2010.02232.xCrossRefPubMedPubMedCentralGoogle Scholar
  12. Cromwell BT, Rennie SD (1954) The biosynthesis and metabolism of betaines in plants. 2. The biosynthesis of glycinebetaine (betaine) in higher plants. Biochem J 58:318–322.  https://doi.org/10.1042/bj0580318CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dudal R (1976) Inventory of major soils of the world with special reference to mineral stress. In: Wright M (ed) Plant adaptation of mineral stress in problems. Cornell University, Agriculture Experiment Station, IthacaGoogle Scholar
  14. FAO (2019) AQUASTAT. http://www.fao.org/nr/water/aquastat/sets/index.stm. Accessed 8 Apr 2019
  15. FAO, ITPS (2015) Status of the world’s soil resources: main report. FAO, RomeGoogle Scholar
  16. Fischer RA, Byerlee DR (1991) Trends of wheat production in the warmer areas: major issues and economic considerations. In: Saunders DA (ed) Wheat for nontraditional, warm areas. CIMMYT, Mexico, pp 3–27Google Scholar
  17. Gage DA, Nolte KD, Russell BL, Rathinasabapathi B, Hanson AD, Nuccio ML (2003) The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 16:487–496.  https://doi.org/10.1046/j.1365-313x.1998.00316.xCrossRefGoogle Scholar
  18. Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6:1746–1751.  https://doi.org/10.4161/psb.6.11.17801CrossRefPubMedPubMedCentralGoogle Scholar
  19. Grote EM, Ejeta G, Rhodes D (1994) Inheritance of glycinebetaine deficiency in sorghum. Crop Sci 34:1217–1220.  https://doi.org/10.2135/cropsci1994.0011183X003400050013xCrossRefGoogle Scholar
  20. Grumet R, Hanson AD (1986) Genetic evidence for an osmoregulatory function of glycinebetaine accumulation in barley. Aust J Plant Physiol 13:353–364.  https://doi.org/10.1071/PP9860353CrossRefGoogle Scholar
  21. Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553.  https://doi.org/10.1046/j.1365-3040.1998.00309.xCrossRefGoogle Scholar
  22. Hashemi FSG, Ismail MR, Rafii MY, Aslani F, Miah G, Muharam FM (2018) Critical multifunctional role of the betaine aldehyde dehydrogenase gene in plants. Biotechnol Biotechnol Equip 32:815–829.  https://doi.org/10.1080/13102818.2018.1478748CrossRefGoogle Scholar
  23. Hattori T, Mitsuya S, Fujiwara T, Jagendorf AT, Takabe T (2009) Tissue specificity of glycinebetaine synthesis in barley. Plant Sci 176:112–118.  https://doi.org/10.1016/j.plantsci.2008.10.003CrossRefGoogle Scholar
  24. 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 glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12:133–142.  https://doi.org/10.1046/j.1365-313X.1997.12010133.xCrossRefPubMedGoogle Scholar
  25. Holmström K, Somersalo S, Mandal A, Palva TE, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51:177–185.  https://doi.org/10.1093/jexbot/51.343.177CrossRefGoogle Scholar
  26. Hossain MA, Li Z-G, Hoque TS, Burritt DJ, Fujita M, Munné-Bosch S (2018) Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 255:399–412.  https://doi.org/10.1007/s00709-017-1150-8CrossRefPubMedGoogle Scholar
  27. Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G (2000) Genetic engineering of gycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 122:747–756.  https://doi.org/10.1104/pp.122.3.747CrossRefPubMedPubMedCentralGoogle Scholar
  28. IPCC (2017) Climate updates. What have we learnt since the IPCC 5th assessment report? The Royal Society, LondonGoogle Scholar
  29. Ishitani M, Arakawa K, Mizuno K, Kishitani S, Takabe T (1993) Betaine aldehyde dehydrogenase in the graminae: levels in leaves of both betaine-accumulating and non accumulating cereal plants. Plant Cell Physiol 34:493–495.  https://doi.org/10.1093/oxfordjournals.pcp.a078445CrossRefGoogle Scholar
  30. Jin P, Zhang Y, Shan T, Huang Y, Xu J, Zheng Y (2015) Low-temperature conditioning alleviates chilling injury in loquat fruit and regulates glycine betaine content and energy status. J Agric Food Chem 63:3654–3365.  https://doi.org/10.1021/acs.jafc.5b00605CrossRefPubMedGoogle Scholar
  31. Khan MS, Yu X, Kikuchi A, Asahina M, Watanabe KN (2009) Genetic engineering of glycine betaine biosynthesis to enhance abiotic stress tolerance in plants. Plant Biotechnol 26:125–134.  https://doi.org/10.5511/plantbiotechnology.26.125CrossRefGoogle Scholar
  32. Khan MIR, Oqbal N, Masood A, Khan AN (2012) Variation in salt tolerance of wheat cultivars: role of glycinebetaine and ethylene. Pedosphere 22:746–754.  https://doi.org/10.1016/S1002-0160(12)60060-5CrossRefGoogle Scholar
  33. Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74.  https://doi.org/10.1016/j.plaphy.2014.03.026CrossRefPubMedGoogle Scholar
  34. Kishitani S, Watanabe K, Yasuda S, Arakawa K, Takabe T (1994) Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ 17:89–95.  https://doi.org/10.1111/j.1365-3040.1994.tb00269.xCrossRefGoogle Scholar
  35. Kumar S, Dhingra A, Daniell H (2004) Plastid-expressed betaine aldehyde dehydrogenase gene in carrot cultured cells, roots, and leaves confers enhanced salt tolerance. Plant Physiol 136:2843–2854.  https://doi.org/10.1104/pp.104.045187CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V, Huner NPA (2015) Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res 126:221–235.  https://doi.org/10.1007/s11120-015-0125-xCrossRefPubMedGoogle Scholar
  37. Leigh RA, Ahmad N, Wyn Jones RG (1981) Assessment of glycinebetaine and proline compartmentation by analysis of isolated beet vacuoles. Planta 153:34–41.  https://doi.org/10.1007/BF00385315CrossRefPubMedGoogle Scholar
  38. Li ZG, Gong M (2011) Mechanical stimulation-induced cross-adaptation in plants: an overview. J Plant Biol 54:358–364.  https://doi.org/10.1007/s12374-011-9178-3CrossRefGoogle Scholar
  39. Li D, Zhang T, Wang M, Liu Y, Brestic M, Chen T, Yang X (2019) Genetic engineering of the biosynthesis of glycine betaine modulates phosphate homeostasis by regulating phosphate acquisition in tomato. Front Plant Sci 9:1995.  https://doi.org/10.3389/fpls.2018.01995CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lv S, Yang A, Zhang K, Wang L, Zhang J (2007) Increase of glycinebetaine improves drought tolerance in cotton. Mol Breed 20:233–248.  https://doi.org/10.1007/s11032-007-9086-xCrossRefGoogle Scholar
  41. Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, Bsutkar P, Tivey ARN, Potter SC, Finn RD, Lopez R (2019) The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acid Res 47(W1):W636–W641.  https://doi.org/10.1093/nar/gkz268CrossRefPubMedGoogle Scholar
  42. Mäkelä P, Peltonen-Sainio P, Jokinen K, Pehu E, Setälä H, Hinkkanen R, Somersalo S (1996) Uptake and translocation of foliar-applied glycinebetaine in crop plants. Plant Sci 121:221–230.  https://doi.org/10.1016/S0168-9452(96)04527-XCrossRefGoogle Scholar
  43. Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512.  https://doi.org/10.1146/annurev-arplant-042916-041132CrossRefPubMedGoogle Scholar
  44. McNeil SD, Rhodes D, Russell BL, Nuccio ML, Shachar-Hill Y, Hanson AD (2000) Metabolic modeling identifies key constraints on an engineered glycine betaine synthesis pathway in tobacco. Plant Physiol 124:153–162.  https://doi.org/10.1104/pp.124.1.153CrossRefPubMedPubMedCentralGoogle Scholar
  45. Mehrabi Z, Ramankutty N (2017) The cost of heat waves and droughts for global crop production.  https://doi.org/10.1101/188151. Accessed 8 Apr 2019
  46. Misra N, Gupta AK (2005) Effect of salt stress on proline metabolism in two high yielding genotypes of green gram. Plant Sci 169:531–539.  https://doi.org/10.1016/j.plantsci.2005.02.013CrossRefGoogle Scholar
  47. Munns R (2010) Strategies for crop improvement in saline soils. In: Asraf M, Ozturk M, Athar HR (eds) Salinity and water stress. Improving crop efficiency. Tasks for Vegetation Science, vol 44. Springer, Dordrecht, pp 99–110.  https://doi.org/10.1007/978-1-4020-9065-3_11CrossRefGoogle Scholar
  48. Muñoz-Clares RA, Riveros-Rosas H, Garza-Ramos G, González-Segura L, Mújica-Jiménez C, Julián-Sánchez A (2014) Exploring the evolutionary route of the acquisition of betaine aldehyde dehydrogenase activity by plant ALDH10 enzymes: implications for the synthesis of the osmoprotectant glycine betaine. BMC Plant Biol 14:149.  https://doi.org/10.1186/1471-2229-14-149CrossRefPubMedPubMedCentralGoogle Scholar
  49. Nuccio ML, Russell BL, Moite KD, Rathinasabapathi B, Gage DA, Hanson AD (1998) The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 16:487–496.  https://doi.org/10.1046/j.1365-313x.1998.00316.xCrossRefPubMedPubMedCentralGoogle Scholar
  50. Nuccio ML, McNeil SD, Ziemak MJ, Hanson AD, Jain RK, Selvaraj G (2000) Choline import into chloroplasts limits glycine betaine synthesis in tobacco: analysis of plants engineered with a chloroplastic or a cytosolic pathway. Metab Eng 2:300–311.  https://doi.org/10.1006/mben.2000.0158CrossRefPubMedGoogle Scholar
  51. Paleg LG, Aspinall D (1981) The physiology and biochemistry of drought resistance in plants. Academic Press, SydneyGoogle Scholar
  52. Peel GJ, Mickelbart MV, Rhodes D (2010) Choline metabolism in glycinebetaine accumulating and non-accumulating near-isogenic lines of Zea mays and Sorghum bicolor. Phytochemistry 71:404–414.  https://doi.org/10.1016/j.phytochem.2009.11.002CrossRefPubMedGoogle Scholar
  53. Rady MOA, Semida WM, El-Mageed TAA, Hemida KA, Rady MM (2018) Up-regulation of antioxidative defense systems by glycine betaine foliar application in onion plants confer tolerance to salinity stress. Sci Hortic 240:614–622.  https://doi.org/10.1016/j.scienta.2018.06.069CrossRefGoogle Scholar
  54. Razavi F, Mahmoudi R, Rabiei V, Soleimani Aghdam M, Soleimani A (2018) Glycine betaine treatment attenuates chilling injury and maintains nutritional quality of hawthorn fruit during storage at low temperature. Sci Hortic 233:188–194.  https://doi.org/10.1016/j.scienta.2018.01.053CrossRefGoogle Scholar
  55. Robinson SP, Jones GP (1986) Accumulation of glycinebetaine in chloroplasts provides osmotic adjustment during salt stress. Aust J Plant Physiol 13:659–668.  https://doi.org/10.1071/PP9860659CrossRefGoogle Scholar
  56. Rosenzweig C, Parry ML (1994) Potential impact of climate change on world food supply. Nature 367:133–138.  https://doi.org/10.1038/367133a0CrossRefGoogle Scholar
  57. Sakai A, Larcher W (1987) Frost survival of plants. Springer, New York.  https://doi.org/10.1007/978-3-642-71745-1CrossRefGoogle Scholar
  58. Sakamoto A, Murata N (2001) The use of bacterial choline oxidase, a glycinebetaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiol 125:180–188.  https://doi.org/10.1104/pp.125.1.180CrossRefPubMedPubMedCentralGoogle Scholar
  59. Saneoka H, Nagasaka C, Hahn DT, Yang WJ, Premachandra GS, Joly RJ, Rhodes D (1995) Salt tolerance of glycinebetaine-deficient and -containing maize lines. Plant Physiol 107:631–638.  https://doi.org/10.1104/pp.107.2.631CrossRefPubMedPubMedCentralGoogle Scholar
  60. Shirasawa K, Takabe T, Takabe T, Kishitani S (2006) Accumulation of Glycinebetaine in Rice Plants that Overexpress Choline Monooxygenase from Spinach and Evaluation of their Tolerance to Abiotic Stress. Annals of Botany 98(3):565–571CrossRefGoogle Scholar
  61. Sies H (2017) Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: Oxidative eustress. Redox Biology 11:613–619.  https://doi.org/10.1016/j.redox.2016.12.035CrossRefPubMedPubMedCentralGoogle Scholar
  62. Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol 4:407–426.  https://doi.org/10.1007/s11157-015-9372-8CrossRefGoogle Scholar
  63. Stadmiller SS, Gorensek-Benitez AH, Guseman AJ, Pielak GJ (2017) Osmotic shock induced protein destabilization in living cells and its reversal by glycine betaine. J Mol Biol 429:1155–1161.  https://doi.org/10.1016/j.jmb.2017.03.001CrossRefPubMedPubMedCentralGoogle Scholar
  64. Subbarao GV, Wheeler RM, Levine LH, Stutte GW (2001) Glycine betaine accumulation, ionic and water relations of red-beet at contrasting levels of sodium supply. J Plant Physiol 158:767–776.  https://doi.org/10.1078/0176-1617-00309CrossRefPubMedGoogle Scholar
  65. Trossat C, Rathinasabapathi B, Hanson AD (1997) Transgenically expressed betaine aldehyde dehydrogenase efficiently catalyses ozidation of dimethylsulfoniopropionaldehyde and omega-aminoaldehydes. Plant Physiol 113:1457–1461.  https://doi.org/10.1104/pp.113.4.1457CrossRefPubMedPubMedCentralGoogle Scholar
  66. Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86.  https://doi.org/10.1186/s12870-016-0771-yCrossRefPubMedPubMedCentralGoogle Scholar
  67. Walter J, Jentsch A, Beierkuhnlein C, Kreyling J (2013) Ecological stress memory and cross stress tolerance in plants in the fact of climate extremes. Environ Exp Bot 94:3–8.  https://doi.org/10.1016/j.envexpbot.2012.02.009CrossRefGoogle Scholar
  68. Wang GP, Zhang XY, Li F, Luo Y, Wang W (2010) Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis. Photosynthetica 48:117–126.  https://doi.org/10.1007/s11099-010-0016-5CrossRefGoogle Scholar
  69. Wang L, Shan T, Xie B, Ling C, Shao S, Jin P, Zheng Y (2019) Glycine betaine reduces chilling injury in peach fruit by enhancing phenolic and sugar metabolisms. Food Chem 272:530–538.  https://doi.org/10.1016/j.foodchem.2018.08.085CrossRefPubMedGoogle Scholar
  70. Wei DD, Zhang W, Wang CC, Meng QW, Li G, Chen THH, Yang XH (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci 257:74–83.  https://doi.org/10.1016/j.plantsci.2017.01.012CrossRefGoogle Scholar
  71. Xu Z, Sun M, Jiang X, Sun H, Dang X, Cong H, Qiao F (2018) Glycinebetaine biosynthesis in response to osmotic stress depends on jasmonate signaling in watermelon suspension cells. Front Plant Sci 9:1469.  https://doi.org/10.3389/fpls.2018.01469CrossRefPubMedPubMedCentralGoogle Scholar
  72. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830.  https://doi.org/10.1242/jeb.01730CrossRefPubMedGoogle Scholar
  73. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222.  https://doi.org/10.1126/science.7112124CrossRefGoogle Scholar
  74. Yang G, Rhodes D, Joly RJ (1996) Effects of high temperature on membrane stability and chlorophyll fluorescence in glycinebetaine-deficient and glycinebetaine-containing maize lines. Aust J Plant Physiol 23:437–443.  https://doi.org/10.1071/PP9960437CrossRefGoogle Scholar
  75. Yao W, Xu T, Farooq SU, Jin P, Zheng Y (2018) Glycine betaine treatment alleviates chilling injury in zucchini fruit (Cucurbita pepo L.) by modulating antioxidant enzymes and membrane fatty acid metabolism. Postharvest Biol Technol 144:20–28.  https://doi.org/10.1016/j.postharvbio.2018.05.007CrossRefGoogle Scholar
  76. Zhu J-K (2002) S D S S T P. Annual Review of Plant Biology 53(1):247–273CrossRefGoogle Scholar
  77. Zhu J-K (2016) Abiotic stress signalling and responses in plants. Cell 167:313–324.  https://doi.org/10.1016/j.cell.2016.08.029CrossRefPubMedPubMedCentralGoogle Scholar
  78. Zorrilla-López U, Masip G, Arjó G, Bai C, Banakar R, Bassie L, Berman J, Farre G, Miralpeiz B, Perez-Massot E, Sabalza M, Sanahuja G, Vamvaka E, Twyman R, Christou P, Zhu C, Capell T (2013) Engineering metabolic pathways in plants by multigene transformation. Int J Dev Biol 57:565–576.  https://doi.org/10.1387/ijdb.130162pcCrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Pirjo S. A. Mäkelä
    • 1
    Email author
  • Kari Jokinen
    • 2
  • Kristiina Himanen
    • 1
  1. 1.Department of Agricultural SciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Luke Natural Resources Institute FinlandHelsinkiFinland

Personalised recommendations