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Proline, Glycinebetaine, and Trehalose Uptake and Inter-Organ Transport in Plants Under Stress

  • Suriyan Cha-um
  • Vandna Rai
  • Teruhiro TakabeEmail author
Chapter

Abstract

Proline, glycinebetaine, and trehalose function as compatible solutes and are upregulated in plants under abiotic stress. The uptake and inter-organ transport in plants are largely unknown. We review the current information on the transport of these osmoprotectants under abiotic stress. Proline metabolism involves several subcellular compartments. Proline concentrations are regulated by the interplay of biosynthesis, degradation, and transport processes. Among the proline transporter proteins, both general amino acid permeases and selective compatible solute transporters were identified. The review summarized our current knowledge on proline transport under abiotic stress conditions. Trehalose is a nonreducing disaccharide formed by two glucose molecules. Sugar transporters have essential roles in the appropriate distribution of carbohydrates throughout the plants. Trehalose transporter has been poorly characterized because it is difficult to predict the characteristics of sugar transporters based solely on the amino acid sequences. Transport properties of exogenous applied trehalose for abiotic stress tolerance have been discussed. Glycinebetaine is synthesized by two-step oxidations of choline with enzymes choline monooxygenase (CMO) and betaine aldehyde dehydrogenase (BADH). Different biosynthetic pathways among monocot and dicot plants were discussed. Expression and substrate specificity of betaine/proline transporters from various plants were compared. Exogenous application of glycinebetaine to plants under stress conditions improved abiotic stress tolerance and gained some attentions. Further application using the important plants both in laboratory and field will contribute to increase the crop production under stress environments.

References

  1. Abdallah MMS, Abdelgawad ZA, El-Bassiouny HMS (2016) Alleviation of the adverse effects of salinity stress using trehalose in two rice varieties. South Afri J Bot 103:275–282.  https://doi.org/10.1016/j.sajb.2015.09.019CrossRefGoogle Scholar
  2. Ahmad S, Raza I, Ali H, Shahzad AN, Rehman A, Sarwar N (2014) Response of cotton crop to exogenous application of glycinebetaine under sufficient and scare water conditions. Braz J Bot 37:407–415.  https://doi.org/10.1007/s40415-014-0092-zCrossRefGoogle Scholar
  3. Ahmed CB, Rouina BB, Sensoy S, Boukhriss M, Abdullah FB (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58:4216–4222.  https://doi.org/10.1021/jf9041479CrossRefPubMedGoogle Scholar
  4. Ali Q, Ashraf M (2011) Exogenously applied glycinebetaine enhances seed and seed oil quality of maize (Zea mays L.) under water deficit conditions. Environ Exp Bot 71:249–259.  https://doi.org/10.1016/j.envexpbot.2010.12.009CrossRefGoogle Scholar
  5. Andreasson C, Neve EPA, Ljungdahl PO (2004) Four permeases import proline and the toxic proline analogue azetidine-2-carboxylate into yeast. Yeast 21:193–199.  https://doi.org/10.1002/yea.1052CrossRefPubMedGoogle Scholar
  6. Ashraf MFMR, Foolad M (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
  7. Bell CI, Milford GFJ, Leigh RA (1996) Photoassimilate distribution in plants and crops: source-sink relationships. In: Zamski E, Schaffer AA (eds) Sugar beet. Marcel Dekker, Inc., New York, pp 691–707Google Scholar
  8. Boorer KJ, Frommer WB, Bush DR, Kreman M, Loo DDF, Wright EM (1996) Kinetics and specificity of a H+/amino acid transporter from Arabidopsis thaliana. J BioI Chem 271:2213–2220.  https://doi.org/10.1074/jbc.271.4.2213CrossRefGoogle Scholar
  9. Bourot S, Sire O, Trautwetter A, Touze T, Wu LF, Blanco C, Bernard T (2000) Glycine betaine-assisted protein folding in a lysA mutant of Escherichia coli. J Biol Chem 275:1050–1056.  https://doi.org/10.1074/jbc.275.2.1050CrossRefPubMedGoogle Scholar
  10. Breitkreuz KE, Shelp BJ, Fischer WN, Schwacke R, Rentsch D (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett 450:280–284.  https://doi.org/10.1016/S0014-5793(99)00516-5CrossRefPubMedGoogle Scholar
  11. Bae H, Herman E, Bailey B, Bae H-J, Sicher R (2005) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol Plant 125(1):114–126CrossRefGoogle Scholar
  12. Cha-um S, Kirdmanee C (2010) Effect of glycinebetaine on proline, water use, and photosynthetic efficiencies, and growth of rice seedlings under salt stress. Turk J Agric Forest 34:517–527.  https://doi.org/10.3906/tar-0906-34CrossRefGoogle Scholar
  13. Cha-um S, Supaibulwatana K, Kirdmanee C (2006) Water relation, photosynthetic ability and growth of Thai jasmine rice (Oryza sativa L. ssp. indica cv. KDMK105) to salt stress by application of exogenous glycinebetaine and choline. J Agron Crop Sci 192:25–36.  https://doi.org/10.1111/j.1439-037X.2006.00186.xCrossRefGoogle Scholar
  14. Cha-um S, Samphumphuang T, Kidmanee C (2013) Glycinebetaine alleviates water deficit stress in indica rice using proline accumulation, photosynthetic efficiencies, growth performances and yield traits. Aust J Crop Sci 7:213–218Google Scholar
  15. Chen L, Bush DR (1997) LHTl, a lysine- and histidine-specific amino acid transporter in Arabidopsis. Plant Physiol 115:1127–1134.  https://doi.org/10.1104/pp.115.3.1127CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chen TH, 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.xCrossRefPubMedGoogle Scholar
  17. Chen WP, Li PH, Chen THH (2000) Glycinebetaine increase chilling-induced lipid peroxidation in Zea mays L. Plant Cell Environ 23:609–618.  https://doi.org/10.1046/j.1365-3040.2000.00570.xCrossRefGoogle Scholar
  18. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Mol Biol Rev 53:121–147. doi:0146-0749/89/010121-27Google Scholar
  19. Di Martino C, Pizzuto R, Pallotta M, De Santis A, Passarella S (2006) Mitochondrial transport in proline catabolism in plants: the existence of two separate translocators in mitochondria isolated from durum wheat seedlings. Planta 223:1123–1133.  https://doi.org/10.1007/s00425-005-0166-zCrossRefPubMedGoogle Scholar
  20. Duman F, Aksoy A, Aydin Z, Temizgul R (2011) Effects of exogenous glycinebetaine and trehalose on cadmium accumulation and biological responses of an aquatic plant (Lemna gibba L.). Water Air Pollut 217:545–556.  https://doi.org/10.1007/s11270-010-0608-5CrossRefGoogle Scholar
  21. Elthon TE, Stewart CR, Bonner WD (1984) Energetics of proline transport in corn mitochondria. Plant Physiol 7:951–955.  https://doi.org/10.1104/pp.75.4.951CrossRefGoogle Scholar
  22. Farooq M, Basra SMA, Wahid A, Cheema ZA, Cheema MA, Khaliq A (2008) Physiological role of exogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 194:325–333.  https://doi.org/10.1111/j.1439-037X.2008.00323.xCrossRefGoogle Scholar
  23. Farooq MA, Ali S, Hameed A, Bharwana SA, Rizwan M, Ishaque W, Farid M, Mahmood K, Iqbal Z (2016) Cadmium stress in cotton seedlings: physiological, photosynthesis and oxidative damages alleviated by glycinebetaine. South Afri J Bot 104:61–68.  https://doi.org/10.1016/j.sajb.2015.11.006CrossRefGoogle Scholar
  24. Fischer WN, Kwart M, Hummel S, Frommer WB (1995) Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J Biol Chem 270:16315–16320.  https://doi.org/10.1074/jbc.270.27.16315CrossRefPubMedGoogle Scholar
  25. Fischer WN, André B, Rentsch D, Krolkiewicz S, Tegeder M, Breitkreuz K, Frommer WB (1998) Amino acid transport in plants. Trends Plant Sci 3:188–195.  https://doi.org/10.1016/S1360-1385(98)01231-XCrossRefGoogle Scholar
  26. Fischer WN, Loo DDF, Koch W, Ludewig U, Boorer KJ, Tegeder M, Rentsch D, Wright EM, Frommer WB (2002) Low and high affinity amino acid H+-co transporters for cellular import of neutral and charged amino acids. Plant J 29:717–731.  https://doi.org/10.1046/j.1365-313X.2002.01248.xCrossRefPubMedGoogle Scholar
  27. Foster J, Lee YH, Tegeder M (2008) Distinct expression of members of the LHT amino acid transporter family in flowers indicates specific roles in plant reproduction. Sex Plant Reprod 21:143–152.  https://doi.org/10.1007/s00497-008-0074-zCrossRefGoogle Scholar
  28. Frommer WB, Hummel S, Riesmeier JW (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc Natl Acad Sci 90:5944–5948.  https://doi.org/10.1073/pnas.90.13.5944CrossRefPubMedGoogle Scholar
  29. Frommer WB, Hummel S, Unseld M, Ninnemann O (1995) Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis. Proc Natl Acad Sci 92:12036–12040.  https://doi.org/10.1073/pnas.92.26.12036CrossRefPubMedGoogle Scholar
  30. Fujiwara T, Hori K, Ozaki K, Yokota Y, Mitsuya S, Ichiyanagi T, Hattori T, Takabe T (2008) Enzymatic characterization of peroxisomal and cytosolic betaine aldehyde dehydrogenases in barley. Physiol Plant 134:22–30.  https://doi.org/10.1111/j.1399-3054.2008.01122.xCrossRefPubMedGoogle Scholar
  31. Fujiwara T, Mitsuya S, Miyake H, Hattori T, Takabe T (2010) Characterization of a novel glycinebetaine/proline transporter gene expressed in the mestome sheath and lateral root cap cells in barley. Planta 232:133–143.  https://doi.org/10.1007/s00425-010-1155-4CrossRefPubMedGoogle Scholar
  32. Garg AK, Kim JK, Owens TG, Ranwala AP, Do Choi Y, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Nat Acad Sci 99:15898–15903.  https://doi.org/10.1073/pnas.252637799CrossRefPubMedGoogle Scholar
  33. Grallath S, Weimar T, Meyer A, Gumy C, Suter-Grotemeyer M, Neuhaus JM, Rentsch D (2005) The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol 137:117–126.  https://doi.org/10.1104/pp.104.055079CrossRefPubMedPubMedCentralGoogle Scholar
  34. Griffiths CA, Paul MJ, Foyer CH (2016) Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochim Biophys Acta 1857:1715–1725.  https://doi.org/10.1016/j.bbabio.2016.07.007CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gupta N, Thind SK, Bains NS (2014) Glycine betaine application modifies biochemical attributes of osmotic adjustment in drought stressed wheat. Plant Growth Regul 72:221–228.  https://doi.org/10.1007/s10725-013-9853-0CrossRefGoogle Scholar
  36. Han EK, Cotty F, Sottas C, Jiang H, Michels CA (1995) Characterization of AGT1 encoding a general α-glucoside transporter from Saccharomyces. Mol Microbiol 17:1093–1107.  https://doi.org/10.1111/j.1365-2958.1995.mmi_17061093.xCrossRefPubMedGoogle Scholar
  37. Harinasut P, Tsutsui K, Takabe T, Nomura M, Takabe T, Kishitani S (1996) Exogenous glycinebetaine accumulation and increased salt-tolerance in rice seedlings. Biosci Biotechnol Biochem 60:366–368.  https://doi.org/10.1271/bbb.60.366CrossRefPubMedGoogle Scholar
  38. Hasanuzzaman M, Alam MM, Rehman A, Hasanuzzaman M, Nahar K, Fujita M (2014, 2014) Exogenous proline and glycine betaine upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. BioMed Res Inter:17.  https://doi.org/10.1155/2014/757219Google Scholar
  39. Hibino T, Waditee R, Araki E, Ishikawa H, Aoki K, Tanaka Y, Takabe T (2002) Functional characterization of choline monooxygenase, an enzyme for betaine synthesis in plants. J Biol Chem 277:41352–41360.  https://doi.org/10.1074/jbc.M205965200CrossRefPubMedGoogle Scholar
  40. Hirner B, Fischer WN, Rentsch D, Kwart M, Frommer WB (1998) Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. Plant J 14:535–544.  https://doi.org/10.1046/j.1365-313X.1998.00151.xCrossRefPubMedGoogle Scholar
  41. Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHTI is a high affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946.  https://doi.org/10.1105/tpc.106.041012CrossRefPubMedPubMedCentralGoogle Scholar
  42. Ho CL, Saito K (2001) Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20:243–259.  https://doi.org/10.1007/s007260170042CrossRefPubMedGoogle Scholar
  43. Hussain M, Malik MA, Farooq M, Ashraf MY, Cheema MA (2008) Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. J Agron Crop Sci 194:193–199.  https://doi.org/10.1111/j.1439-037X.2008.00305.xCrossRefGoogle Scholar
  44. Igarashi Y, Yoshiba Y, Takeshita T, Nomura S, Otomo J, Yamaguchi-Shinozaki K, Shinozaki K (2000) Molecular cloning and characterization of a cDNA encoding proline transporter in rice. Plant Cell Physiol 41:750–756.  https://doi.org/10.1093/pcp/41.6.750CrossRefPubMedGoogle Scholar
  45. Iqbal N, Ashraf Y, Ashraf M (2011) Modulation of endogenous levels of some key organic metabolites by exogenous application of glycine betaine in drought stressed plants of sunflower (Helianthus annuus L.). Plant Growth Regul 63:7–12.  https://doi.org/10.1007/s10725-010-9506-5CrossRefGoogle Scholar
  46. Islam MM, Hoque MA, Okuma E, Banu MNA, Shimoishi Y, Nakamura Y, Murata Y (2009) Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. J Plant Physiol 166:1587–1597.  https://doi.org/10.1016/j.jplph.2009.04.002CrossRefPubMedGoogle Scholar
  47. Jonytienė V, Burbulis N, Kuprienė R, Blinstrubienė A (2012) Effect of exogenous proline and de-acclimation treatment on cold tolerance in Brassica napus shoots culture in vitro. J Food Agric Environ 10:327–330Google Scholar
  48. Kahlaoui B, Hachicha M, Misle E, Fidalgo F, Teixeira J (2018) Physiological and biochemical responses to the exogenous application of proline of tomato plants irrigated with saline water. J Saudi Soc Agric Sci 17:17–23.  https://doi.org/10.1016/j.jssas.2015.12.002CrossRefGoogle Scholar
  49. Kanamori Y, Saito A, Hagiwara-Komoda Y, Tanaka D, Mitsumasu K, Kikuta S, Watanabe M, Cornette R, Kikawada T, Okuda T (2010) The trehalose transporter 1 gene sequence is conserved in insects and encodes proteins with different kinetic properties involved in trehalose import into peripheral tissues. Insect Biochem Mol Biol 40:30e37.  https://doi.org/10.1016/j.ibmb.2009.12.006CrossRefGoogle Scholar
  50. Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress responses to high-osmolality environments. Arch Microbiol 170:319–330.  https://doi.org/10.1007/s002030050649CrossRefPubMedGoogle Scholar
  51. Kikawada T, Saito A, Kanamori Y, Nakahara Y, Iwata KI, Tanaka D, Watanabe M, Okuda T (2007) Trehalose transporter 1, a facilitated and high-capacity trehalose transporter, allows exogenous trehalose uptake into cells. Proc Nat Acad Sci 104:11585–11590.  https://doi.org/10.1073/pnas.0702538104CrossRefPubMedGoogle Scholar
  52. Kosar F, Akram NA, Sadiq M, Al-Qurainy F, Ashraf M (2018) Trehalose: a key organic osmolyte effectively involved in plant abiotic stress tolerance. J Plant Growth Regul:1–13.  https://doi.org/10.1007/s00344-018-9876-xCrossRefGoogle Scholar
  53. Krämer R (1998) Mitochondrial carrier proteins can reversibly change their transport mode: the cases of the aspartate/glutamate and the phosphate carrier. Exp Physiol 83:259–265.  https://doi.org/10.1113/expphysiol.1998.sp004111CrossRefPubMedGoogle Scholar
  54. Kwart M, Hirner B, Hummel S, Frommer WB (1993) Differential expression of two related amino acid transporters with differing substrate specificity in Arabidopsis thaliana. Plant J 4:993–1002.  https://doi.org/10.1046/j.1365-313X.1993.04060993.xCrossRefPubMedGoogle Scholar
  55. Lasko PF, Brandriss MC (1981) Proline transport in Saccharomyces cerevisiae. J Bacteriol 148:241–247PubMedPubMedCentralGoogle Scholar
  56. Lee YH, Tegeder M (2004) Selective expression of a novel high affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. Plant J 40:60–74.  https://doi.org/10.1111/j.1365-313X.2004.02186.xCrossRefPubMedGoogle Scholar
  57. Lee YH, Foster J, Chen J, Voll LM, Weber APM, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. Plant J 50:305–319.  https://doi.org/10.1111/j.1365-313X.2007.03045.xCrossRefPubMedGoogle Scholar
  58. Lehmann S, Funck D, Szabados L, Rentsch D (2010) Proline metabolism and transport in plant development. Amino Acids 39:949–962.  https://doi.org/10.1111/j.1365-313X.2004.02186.xCrossRefPubMedGoogle Scholar
  59. LiXin Z, ShengXiu L, ZongSuo L (2009) Differential plant growth and osmotic effects of two maize (Zea mays L.) cultivars to exogenous glycinebetaine application under drought stress. Plant Growth Regul 58:297–305.  https://doi.org/10.1007/s10725-009-9379-7CrossRefGoogle Scholar
  60. Luo Y, Li F, Wang GP, Yang XH, Wang W (2010) Exogenously-supplied trehalose protects thylakoid membranes of winter wheat from heat-induced damage. Biol Plant 54:495–501.  https://doi.org/10.1007/s10535-010-0087-yCrossRefGoogle Scholar
  61. Ma QQ, Wang W, Li YH, Li DQ, Zou Q (2006) Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine. J Plant Physiol 163:165–175.  https://doi.org/10.1016/j.jplph.2005.04.023CrossRefPubMedGoogle Scholar
  62. Ma XL, Wang YJ, Xie SL, Wang C, Wang W (2007) Glycinebetaine application ameliorates negative effects of drought stress in tobacco. Russ J Plant Physiol 54:472–479.  https://doi.org/10.1134/S1021443707040061CrossRefGoogle Scholar
  63. Ma C, Wang Z, Kong B, Lin T (2013) Exogenous trehalose differentially modulate antioxidant defense system in wheat callus during water deficit and subsequent recovery. Plant Growth Regul 70:275–285.  https://doi.org/10.1007/s10725-013-9799-2CrossRefGoogle Scholar
  64. Mäkelä P (2004) Agro -industrial uses of glycinebetaine. Sugar Technol 6:207–212.  https://doi.org/10.1007/BF02942500CrossRefGoogle Scholar
  65. 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. Biol Plant 43:471–475.  https://doi.org/10.1023/A:1026712426180CrossRefGoogle Scholar
  66. Mitsuya S, Kuwahara J, Ozaki K, Saeki E, Fujiwara T, Takabe T (2011) Isolation and characterization of a novel peroxisomal choline monooxygenase in barley. Planta 234:1215–1226.  https://doi.org/10.1007/s00425-011-1478-9CrossRefPubMedGoogle Scholar
  67. Morbach S, Kramer R (2002) Body shaping under water stress: osmosensing and osmoregulation of solute transport in bacteria. Chem Biol Chem 3:384–397.  https://doi.org/10.1002/1439-7633(20020503)3:5<384::AID-CBIC384>3.0.CO;2-HCrossRefGoogle Scholar
  68. Mostafa MG, Hossain MA, Fujita M, Tran LSP (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433.  https://doi.org/10.1038/srep11433CrossRefGoogle Scholar
  69. Moustakas M, Sperdouli I, Kouna T, Antonopoulou CI, Therios I (2011) Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. Plant Growth Regul 65:315.  https://doi.org/10.1007/s10725-011-9604-zCrossRefGoogle Scholar
  70. Mueckler M (1994) Facilitative glucose transporters. Eur J Biochem 219:713e725.  https://doi.org/10.1111/j.1432-1033.1994.tb18550.xCrossRefGoogle Scholar
  71. Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:596–604.  https://doi.org/10.1016/j.jplph.2012.01.004CrossRefPubMedGoogle Scholar
  72. 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. Met Eng 2:300–311.  https://doi.org/10.1006/mben.2000.0158CrossRefGoogle Scholar
  73. Okumoto S, Schmidt R, Tegeder M, Fischer WN, Rentsch D, Frommer WB, Koch W (2002) High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J Biol Chem 277:45338–45346.  https://doi.org/10.1074/jbc.M207730200CrossRefPubMedGoogle Scholar
  74. Okumoto S, Koch W, Tegeder M, Fischer WN, Biehl A, Leister D, Stierhof YD, Frommer WB (2004) Root phloem-specific expression of the plasma membrane amino acid proton cotransporter AAP3. J Exp Bot 55:2155–2168.  https://doi.org/10.1093/jxb/erh233CrossRefPubMedGoogle Scholar
  75. Osman HS (2015) Enhancing antioxidant-yield relationship of pea plant under drought at different growth stages by exogenously applied glycine betaine and proline. Ann Agric Sci 60:389–402.  https://doi.org/10.1016/j.aoas.2015.10.004CrossRefGoogle Scholar
  76. Ozden M, Demirel U, Karaman A (2009) Effects of proline on antioxidant system in leaves of grapevine (Vitis vinifera L.) exposed to oxidative stress by H2O2. Sci Hortic 119:163–168.  https://doi.org/10.1016/j.scienta.2008.07.031CrossRefGoogle Scholar
  77. Pao SS, Paulsen IT, Saier MH Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34PubMedPubMedCentralGoogle Scholar
  78. Park EJ, Jeknić Z, Chen HH (2006) Exogenous application of glycinebetaine increases chilling tolerance in tomato plants. Plant Cell Physiol 47:706–714.  https://doi.org/10.1093/pcp/pcj041CrossRefPubMedGoogle Scholar
  79. Paul MJ, Oszvald M, Jesus C, Rajulu C, Griffiths CA (2017) Increasing crop yield and resilience with trehalose 6-phosphate: targeting a feast–famine mechanism in cereals for better source–sink optimization. J Exp Bot 68:4455–4462.  https://doi.org/10.1093/jxb/erx083CrossRefPubMedGoogle Scholar
  80. Raza MAS, Saleem MF, Shah GM, Khan IH, Raza A (2014) Exogenous application of glycinebetaine and potassium for improving water relations and grain yield of wheat under drought. J Soil Sci Plant Nutr 14:348–364.  https://doi.org/10.4067/S0718-95162014005000028CrossRefGoogle Scholar
  81. Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446.  https://doi.org/10.1105/tpc.8.8.1437CrossRefPubMedPubMedCentralGoogle Scholar
  82. Rentsch D, Schmidt S, Tegeder M (2007) Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett 581:2281–2289.  https://doi.org/10.1016/j.febslet.2007.04.013CrossRefPubMedGoogle Scholar
  83. Rezaei MA, Jokar I, Ghorbanli M, Kaviani B, Kharabian-Masouleh A (2012) Morpho-physiological improving effects of exogenous glycine betaine on tomato (Lycopersicum esculentum Mill.) cv. PS under drought stress conditions. Plants Omics J 5:79–86Google Scholar
  84. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Ann Rev Plant Physiol Plant Mol Biol 44:357–384.  https://doi.org/10.1146/annurev.pp.44.060193.002041CrossRefGoogle Scholar
  85. Roeβler M, Müller V (2001) Osmoadaptation in bacteria and archaea: common principles and differences. Environ Microbiol 3:743–754.  https://doi.org/10.1046/j.1462-2920.2001.00252.xCrossRefGoogle Scholar
  86. Rohman MM, Begum S, Akhi AH, Ahsan AFMS, Uddin MS, Amiruzzaman M, Banik BR (2015) Protective role of antioxidants in maize seedlings under saline stress: exogenous proline provided better tolerance than betaine. Bothalia J 45:17–35Google Scholar
  87. Rolletschek H, Hosein F, Miranda M, Heim U, Gotz KP, Schlereth A, Borisjuk L, Saalbach I, Wobus U, Weber H (2005) Ectopic expression of an amino acid transporter (VfAAPI) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol 137:1236–1249.  https://doi.org/10.1104/pp.104.056523CrossRefPubMedPubMedCentralGoogle Scholar
  88. Redillas MCFR, Jeong JS, Kim YS, Jung H, Bang SW, Choi YD, Ha S-H, Reuzeau C, Kim J-K (2012) The overexpression of alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J 10(7):792–805CrossRefGoogle Scholar
  89. Sanders A, Collier R, Trethewy A, Gould G, Sieker R, Tegeder M (2009) AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J 59:540–552.  https://doi.org/10.1111/j.1365-313X.2009.03890.xCrossRefPubMedGoogle Scholar
  90. Schmidt R, Stransky H, Koch W (2007) The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226:805–813.  https://doi.org/10.1007/s00425-007-0527-xCrossRefPubMedGoogle Scholar
  91. Schwacke R, Grallath S, Breitkreuz KE, Stransky E, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. Plant Cell 11:377–392.  https://doi.org/10.1105/tpc.11.3.377CrossRefPubMedPubMedCentralGoogle Scholar
  92. Shahid MA, Balal RM, Pervez MA, Abbas T, Aqeel MJ, Javaid MM, Gacia-Sanchez F (2014) Exogenous proline and proline-enriched Lolium perenne leaf extract protects against phytotoxic effects of nickel and salinity in Pisum sativum by altering polyamine metabolism in leaves. Tuk J Bot 38:914–926.  https://doi.org/10.3906/bot-1312-13CrossRefGoogle Scholar
  93. Singh M, Singh VP, Dubey G, Prasad SM (2015) Exogenous proline application ameliorates toxic effects of arsenate in Solanum melongena L. seedlings. Ecotoxicol Environ Safe 117:164–173.  https://doi.org/10.1016/j.ecoenv.2015.03.021CrossRefGoogle Scholar
  94. Sorkheh K, Shiran B, Khodambashi M, Rouhi V, Mosavei S, Sofo A (2012) Exogenous proline alleviates the effects of H2O2-induced oxidative stress in wild almond species. Russ J Plant Physiol 59:788–798.  https://doi.org/10.1134/S1021443712060167CrossRefGoogle Scholar
  95. Stambuk BU, Panek AD, Crowe JH, Crowe LM, de Araujo PS (1998) Expression of high-affinity trehalose–H+ symport in Saccharomyces cerevisiae. Biochim et Biophys Acta -Gen Sub 1379:118–128.  https://doi.org/10.1016/S0304-4165(97)00087-1CrossRefGoogle Scholar
  96. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97.  https://doi.org/10.1016/j.tplants.2009.11.009CrossRefPubMedPubMedCentralGoogle Scholar
  97. Tabuchi T, Okada T, Takashima Y, Azuma T, Nanmori T, Yasuda T (2006) Transcriptional response of glycinebetaine-related genes to salt stress and light in leaf beet. Plant Biotechnol 23:317–320.  https://doi.org/10.5511/plantbiotechnology.23.317CrossRefGoogle Scholar
  98. Tanner J (2008) Structural biology of proline catabolism. Amino Acids 35:719–730.  https://doi.org/10.1007/s00726-008-0062-5CrossRefPubMedPubMedCentralGoogle Scholar
  99. Tapia H, Young L, Fox D, Bertozzi CR, Koshland D (2015) Increasing intracellular trehalose is sufficient to confer desiccation tolerance to Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 112:6122–6127.  https://doi.org/10.1073/pnas.1506415112CrossRefPubMedPubMedCentralGoogle Scholar
  100. Teh CH, Mahmood M, Shaharuddin NA, Ho CL (2015) In vitro shoot apices as simple model to study the effect of NaCl and the potential of exogenous proline and glutathione in mitigating salinity stress. Plant Growth Regul 75:771–781.  https://doi.org/10.1007/s10725-014-9980-2CrossRefGoogle Scholar
  101. Ueda A, Shi W, Sanmiya K, Shono M, Takabe T (2001) Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol 42:1282–1289.  https://doi.org/10.1093/pcp/pce166CrossRefPubMedGoogle Scholar
  102. Ueda A, Yamamoto-Yamane Y, Takabe T (2007) Salt stress enhances proline utilization in the apical region of barley roots. Biochem Biophys Res Commun 355:61–66.  https://doi.org/10.1016/j.bbrc.2007.01.098CrossRefPubMedGoogle Scholar
  103. Ueda A, Shi W, Shimada T, Miyake H, Takabe T (2008) Altered expression of barley proline transporter causes different growth responses in Arabidopsis. Planta 227:277–286.  https://doi.org/10.1007/s00425-007-0615-yCrossRefPubMedGoogle Scholar
  104. Verslues PE, Sharp RE (1999) Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiol 119:1349–1360.  https://doi.org/10.1104/pp.119.4.1349CrossRefPubMedPubMedCentralGoogle Scholar
  105. Waditee R, Hibino T, Tanaka Y, Nakamura T, Incharoensakdi A, Hayakawa S, Suzuki S, Futsuhara Y, Kawamitsu Y, Takabe T, Takabe T (2002) Functional characterization of betaine/proline transporters in betaine-accumulating mangrove. J Biol Chem 277:18373–18382.  https://doi.org/10.1074/jbc.M112012200CrossRefPubMedGoogle Scholar
  106. Waditee R, Bhuiyan MNH, Rai V, Aoki K, Tanaka Y, Hibino T, Suzuki S, Takano J, Jagendorf AT, Takabe T, Takabe T (2005) Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc Nat Acad Sci 102:1318–1323.  https://doi.org/10.1073/pnas.0409017102CrossRefPubMedGoogle Scholar
  107. Waditee R, Bhuiyan NH, Hirata E, Hibino T, Tanaka Y, Shikata M, Takabe T (2007) Metabolic engineering for betaine accumulation in microbes and plants. J Biol Chem 282:34185–34193.  https://doi.org/10.1074/jbc.M704939200CrossRefPubMedGoogle Scholar
  108. Weigelt K, Kiister H, Radchuk R, Miiller M, Weichert H, Fait A, Fernie AR, Saalbach I, Weber H (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant J 55:909–926.  https://doi.org/10.1111/j.1365-313X.2008.03560.xCrossRefPubMedGoogle Scholar
  109. Wood JM (2006) Osmosensing by bacteria. Sci STKE 357:pe43.  https://doi.org/10.1126/stke.3572006pe43CrossRefGoogle Scholar
  110. Wood IS, Trayhurn P (2003) Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins. British J Nutr 89:3e9.  https://doi.org/10.1079/BJN2002763CrossRefGoogle Scholar
  111. Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, Smith LT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Physiol A Mol Integr Physiol 130:437–460.  https://doi.org/10.1016/S1095-6433(01)00442-1CrossRefPubMedGoogle Scholar
  112. Wyn Jones RG, Storey R (1981) Betaines. In: Paleg LG, Aspinall D (eds) The physiology and biochemistry of drought resistance in plants, Academic Press, Sydney, pp 171–204Google Scholar
  113. Xing W, Rajashekar CB (1999) Alleviation of water stress in beans by exogenous glycine betaine. Plant Sci 48:185–195.  https://doi.org/10.1016/S0168-9452(99)00137-5CrossRefGoogle Scholar
  114. Yamada N, Promden W, Yamane K, Tamagake H, Hibino T, Tanaka Y, Takabe T (2009) Preferential accumulation of betaine uncoupled to choline monooxygenase in young leaves of sugar beet–importance of long-distance translocation of betaine under normal and salt-stressed conditions. J Plant Physiol 166:2058–2070.  https://doi.org/10.1016/j.jplph.2009.06.016CrossRefPubMedGoogle Scholar
  115. Yamada N, Cha-um S, Kageyama H, Promden W, Tanaka Y, Kirdmanee C, Takabe T (2011a) Isolation and characterization of proline/betaine transporter gene from oil palm. Tree Physiol 31:462–468.  https://doi.org/10.1093/treephys/tpr017CrossRefPubMedGoogle Scholar
  116. Yamada N, Sakakibara S, Tsutsumi K, Waditee R, Tanaka Y, Takabe T (2011b) Expression and substrate specificity of betaine/proline transporters suggest a novel choline transport mechanism in sugar beet. J Plant Physiol 168:1609–1616.  https://doi.org/10.1016/j.jplph.2011.03.007CrossRefPubMedGoogle Scholar
  117. Yang L, Zhao X, Zhu H, Paul M, Zu Y, Tang Z (2014) Exogenous trehalose largely alleviates ionic unbalance, ROS bust, and PCD occurrence induced by high salinity in Arabidopsis seedlings. Front Plant Sci 5:570.  https://doi.org/10.3389/fpls.2014.00570CrossRefPubMedPubMedCentralGoogle Scholar
  118. Zhang M, Huang H, Dai S (2014) Isolation and expression analysis of proline metabolism-related genes in Chrysanthemum lavandulifolium. Gene 537:203–213.  https://doi.org/10.1016/j.gene.2014.01.002CrossRefPubMedGoogle Scholar
  119. Zhao XX, Ma QQ, Liang C, Fang Y, Wang YQ, Wang W (2007) Effect of glycinebetaine on function of thylakoid membranes in wheat flag leaves under drought stress. Biol Plant 51:584–588.  https://doi.org/10.1007/s10535-007-0128-3CrossRefGoogle Scholar
  120. Zheng JL, Zhao LY, Wu CW, Shen B, Zhu AY (2015) Exogenous proline reduces NaCl-induced damage by mediating ionic and osmotic adjustment and enhancing antioxidant defense in Eurya emarginata. Acta Physiol Plant 37:181.  https://doi.org/10.1007/s11738-015-1921-9CrossRefGoogle Scholar
  121. Zhou Y, Zhu W, Bellur PS, Rewinkel D, Becker DF (2008) Direct linking of metabolism and gene expression in the proline utilization a protein from Escherichia coli. Amino Acids 35:711–718.  https://doi.org/10.1007/s00726-008-0053-6CrossRefPubMedPubMedCentralGoogle Scholar
  122. Zouari M, Ahmed CB, Elloumi N, Bellassoued K, Delmail D, Labrousse P, Abdallah FB, Rouina BB (2016a) Impact of proline application on cadmium accumulation, mineral nutrition and enzymatic antioxidant defense system of Olea europaea L. cv Chemlali exposed to cadmium stress. Ecotoxicol Environ Safe 128:195–205.  https://doi.org/10.1016/j.ecoenv.2016.02.024CrossRefGoogle Scholar
  123. Zouari M, Ahmed CB, Zorrig W, Elloumi N, Delmail D, Rouina BB, Labrousse P, Abdallah FB (2016b) Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.). Ecotoxicol Environ Safe 128:100–108.  https://doi.org/10.1016/j.ecoenv.2016.02.015CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA)Pathum ThaniThailand
  2. 2.National Research Center on Plant Biotechnology, IARINew DelhiIndia
  3. 3.Research Institute, Meijo UniversityNagoyaJapan

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