Osmoprotectant-Related Genes in Plants Under Abiotic Stress: Expression Dynamics, In Silico Genome Mapping, and Biotechnology

  • Éderson Akio Kido
  • José Ribamar Costa Ferreira-Neto
  • Manassés Daniel da Silva
  • Vanessa Emanuelle Pereira Santos
  • Jorge Luís Bandeira da Silva Filho
  • Ana Maria Benko-Iseppon


Osmoprotectants are categorized as osmolytes, also known as compatible solutes, considering that they are small organic molecules that share characteristics, like low molecular weight, neutral charge, and low toxicity, even at high concentrations in cells. They are identified in different chemical classes, including polyamines (e.g., putrescine, spermidine, spermine), sugars (e.g., sucrose, trehalose, raffinose), sugar alcohols (e.g., myo-inositols), betaines (e.g., glycine betaine), and amino acids (e.g., proline). In plants exposed to abiotic stresses (salinity/drought), osmoprotectants help cellular turgor preservation and drive the water uptake gradient. Some osmoprotectants shield plants from damage through chaperone-like activities, helping in the conservation of membrane structures and protein functions, or scavenging for reactive oxygen species (ROS) generated by the stresses. Therefore, it is advantageous to understand how plants respond to abiotic stresses by regulating the expression of osmoprotectant-related genes. This chapter presents data on plant osmoprotectants, including their regulating genes, associated pathways, and transcriptional regulations in plants under abiotic stresses. There is also an overview of their in silico mapping (model plants/crops) and their biotechnological potential as transgenes. Furthermore, these approaches are new perspectives for the analysis and introgression of these related genes into cultivated plant species, improving advances in plant breeding and crop production.


Abiotic stress Osmolytes Transcriptomic Bioinformatic Transgenic 



The authors acknowledge the Brazilian institutions FINEP (Financiadora de Estudos e Projetos), FACEPE (Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco), and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for financial support and fellowships (CNPq 311894/2017-8). The authors also thank Ms. Suzana de Aragão Britto Kido for the English language revision.


  1. Ahn CH, Hossain MA, Lee E, Kanth BK, Park PB (2018) Increased salt and drought tolerance by D-pinitol production in transgenic Arabidopsis thaliana. Biochem Biophys Res Commun 504:315–320. Scholar
  2. Ahn CH, Park U, Park PB (2011) Increased salt and drought tolerance by D-pinitol production in transgenic Arabidopsis thaliana. Biochem Biophys Res Commun 415:669–674. Scholar
  3. Alavilli H, Awasthi JP, Rout GR, Sahoo L, Lee B, Panda SK (2016) Overexpression of a barley aquaporin gene, HvPIP2;5 confers salt and osmotic stress tolerance in yeast and plants. Front Plant Sci 7:1–12. Scholar
  4. Alcázar R, Planas J, Saxena T, Zarza X, Bortolotti C, Cuevas J, Bitrián M, Tiburcio AF, Altabella T (2010) Putrescine accumulation confers drought tolerance in transgenic Arabidopsis plants over-expressing the homologous Arginine decarboxylase 2 gene. Plant Physiol Biochem 48:547–552. Scholar
  5. Alet AI, Sanchez DH, Cuevas JC, del Valle S, Altabella T, Tiburcio AF, Marco F, Ferrando A, Espasandín FD, González ME, Carrasco P, Ruiz OA (2011) Putrescine accumulation in Arabidopsis thaliana transgenic lines enhances tolerance to dehydration and freezing stress. Plant Signal Behav 6:278–286. Scholar
  6. Alimohammadi M, Lahiani MH, Khodakovskaya MV (2015) Genetic reduction of inositol triphosphate (InsP3) increases tolerance of tomato plants to oxidative stress. Planta 242:123–135. Scholar
  7. Antoniou C, Fragkoudi I, Martinou A, Stavrinides MC, Fotopoulos V (2018) Spatial response of Medicago truncatula plants to drought and spider mite attack. Plant Physiol Biochem 130:658–662. Scholar
  8. Ardito F, Giuliani M, Perrone D, Troiano G, Lo Muzio L (2017) The crucial role of protein phosphorylation in cell signaling and its use as targeted therapy (Review). Int J Mol Med 40:271–280. Scholar
  9. Bae YS, Oh H, Rhee SG, Do Yoo Y (2011) Regulation of reactive oxygen species generation in cell signaling. Mol Cells 32:491–509. Scholar
  10. Bie X, She M, Li J, Ye X, Lin Z, Zhang S, Gao X, Wang K, Du L (2012) Combinational transformation of three wheat genes encoding fructan biosynthesis enzymes confers increased fructan content and tolerance to abiotic stresses in tobacco. Plant Cell Rep 31:2229–2238. Scholar
  11. Bougouffa S, Radovanovic A, Essack M, Bajic VB (2014) DEOP: a database on osmoprotectants and associated pathways. Database 2014Google Scholar
  12. Brauc S, De Vooght E, Claeys M, Geuns JMC, Höfte M, Angenon G (2012) Overexpression of arginase in Arabidopsis thaliana influences defence responses against Botrytis cinerea. Plant Biol 14:39–45. Scholar
  13. Burdo B, Gray J, Goetting-Minesky MP, Wittler B, Hunt M, Li T, Velliquette D, Thomas J, Gentzel I, Dos Santos BM, Mejía-Guerra MK, Connolly LN, Qaisi D, Li W, Casas MI, Doseff AI, Grotewold E (2014) The Maize TFome - Development of a transcription factor open reading frame collection for functional genomics. Plant J 80:356–366. Scholar
  14. Cabid E, Leloir LF (1958) The biosynthesis of trehalose phosphate. J Biol Chem 231(1):259–275Google Scholar
  15. Caspi R, Billington R, Fulcher CA, Keseler IM, Kothari A, Krummenacker M, Latendresse M, Midford PE, Ong Q, Ong WK, Paley S, Subhraveti P, Karp PD (2018) The MetaCyc database of metabolic pathways and enzymes. Nucleic Acids Res 46:D633–D639. Scholar
  16. Chatterjee J, Majumder AL (2010) Salt-induced abnormalities on root tip mitotic cells of Allium cepa: prevention by inositol pretreatment. Protoplasma 245:165–172. Scholar
  17. Chen E, Zhang X, Yang Z, Wang X, Yang Z, Zhang C, Wu Z, Kong D, Liu Z, Zhao G, Butt HI, Zhang X, Li F (2017) Genome-wide analysis of the HD-ZIP IV transcription factor family in Gossypium arboreum and GaHDG11 involved in osmotic tolerance in transgenic Arabidopsis. Mol Gen Genomics 292:593–609. Scholar
  18. Chen J, Shang Y-T, Wang W-H, Chen X-Y, He E-M, Zheng H-L, Shangguan Z, He E-M (2016) Hydrogen sulfide-mediated polyamines and sugar changes are involved in hydrogen sulfide-induced drought tolerance in Spinacia oleracea seedlings. Front Plant Sci 7:1–1. Scholar
  19. Chen JB, Yang JW, Zhang ZY, Feng XF, Wang SM (2013) Two P5CS genes from common bean exhibiting different tolerance to salt stress in transgenic Arabidopsis. J Genet 92:461–469. Scholar
  20. Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257. Scholar
  21. Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J, Lu G (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499. Scholar
  22. Cheng YJ, Deng XP, Kwak SS, Chen W, Eneji AE (2013) Enhanced tolerance of transgenic potato plants expressing choline oxidase in chloroplasts against water stress. Bot Stud 54:1–9. Scholar
  23. Choubey A, Rajam MV (2018) RNAi-mediated silencing of spermidine synthase gene results in reduced reproductive potential in tobacco. Physiol Mol Biol Plants 24:1069–1081. Scholar
  24. Conde A, Soares F, Breia R, Gerós H (2018) Postharvest dehydration induces variable changes in the primary metabolism of grape berries. Food Res Int 105:261–270. Scholar
  25. Chevalier D, Morris ER, Walker JC (2009) 14-3-3 and FHA Domains Mediate Phosphoprotein Interactions. Annual Review of Plant Biology 60(1):67–91PubMedCrossRefGoogle Scholar
  26. Dastogeer KMG, Li H, Sivasithamparam K, Jones MGK, Wylie SJ (2018) Fungal endophytes and a virus confer drought tolerance to Nicotiana benthamiana plants through modulating osmolytes, antioxidant enzymes and expression of host drought responsive genes. Environ Exp Bot 149:95–108. Scholar
  27. de Freitas PAF, de Carvalho HH, Costa JH, Miranda RS, KDDC S, de Oliveira FDB, Coelho DG, Prisco JT, Gomes-Filho E (2019) Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep 38:403. Scholar
  28. de Ronde JA, Cress WA, Krüger GHJ, Strasser RJ, Van Staden J (2004) Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. J Plant Physiol 161:1211–1224. Scholar
  29. Devos KM, Brown JKM, Bennetzen JL (2002) Genome Size Reduction through Illegitimate Recombination Counteracts Genome Expansion in Arabidopsis. Genome Research 12(7):1075–1079PubMedPubMedCentralCrossRefGoogle Scholar
  30. Diedhiou C, Gaudet D, Liang Y, Sun J, Lu ZX, Eudes F, Laroche A (2012) Carbohydrate profiling in seeds and seedlings of transgenic triticale modified in the expression of sucrose: sucrose-1-fructosyltransferase (1-SST) and sucrose: fructan-6-fructosyltransferase (6-SFT). J Biosci Bioeng 114:371–378. Scholar
  31. Duan J, Liu P, Li Z, Zhang M, Ali J, Zhang H, Li J, Xiong H (2012) OsMIOX, a myo-inositol oxygenase gene, improves drought tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). Plant Sci 196:143–151. Scholar
  32. Ebeed HT, Hassan NM, Aljarani AM (2017) Exogenous applications of Polyamines modulate drought responses in wheat through osmolytes accumulation, increasing free polyamine levels and regulation of polyamine biosynthetic genes. Plant Physiol Biochem 118:438–448. Scholar
  33. Espasandin FD, Maiale SJ, Calzadilla P, Ruiz OA, Sansberro PA (2014) Transcriptional regulation of 9-cis-epoxycarotenoid dioxygenase (NCED) gene by putrescine accumulation positively modulates ABA synthesis and drought tolerance in Lotus tenuis plants. Plant Physiol Biochem 76:29–35. Scholar
  34. 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. Scholar
  35. Fang H, Liu X, Thorn G, Duan J, Tian L (2014) Expression analysis of histone acetyltransferases in rice under drought stress. Biochemical and Biophysical Research Communications 443(2):400–405PubMedCrossRefGoogle Scholar
  36. Gagneul D, Ainouche A, Duhaze C, Lugan R, Larher FR, Bouchereau A (2007) A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiol 144:1598–1611. Scholar
  37. Garcia AAF, Kido EA, Meza AN, Souza HMB, Pinto LR, Pastina MM, Leite CS, Da Silva JAG, Ulian EC, Figueira A, Souza AP (2006) Development of an integrated genetic map of a sugarcane (Saccharum spp.) commercial cross, based on a maximum-likelihood approach for estimation of linkage and linkage phases. Theor Appl Genet 112:298–314. Scholar
  38. Georges F, Das S, Ray H, Bock C, Nokhrina K, Kolla VA, Keller W (2009) Over-expression of Brassica napus phosphatidylinositol-phospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. Plant Cell Environ 32:1664–1681. Scholar
  39. Gillaspy GE (2011) The cellular language of myo-inositol signaling. New Phytol 192:823–839. Scholar
  40. Goel D, Singh AK, Yadav V, Babbar SB, Murata N, Bansal KC (2011) Transformation of tomato with a bacterial codA gene enhances tolerance to salt and water stresses. J Plant Physiol 168:1286–1294. Scholar
  41. Gong X, Dou F, Cheng X, Zhou J, Zou Y, Ma F (2018) Genome-wide identification of genes involved in polyamine biosynthesis and the role of exogenous polyamines in Malus hupehensis Rehd. under alkaline stress. Gene 669:52–62. Scholar
  42. Goyal RK, Fatima T, Topuz M, Bernadec A, Sicher R, Handa AK, Mattoo AK (2016) Pathogenesis-related protein 1b1 (PR1b1) is a major tomato fruit protein responsive to chilling temperature and upregulated in high polyamine transgenic genotypes. Front Plant Sci 7:901. Scholar
  43. Guan C, Huang YH, Cui X, Liu SJ, Zhou YZ, Zhang YW (2018) Overexpression of gene encoding the key enzyme involved in proline-biosynthesis (PuP5CS) to improve salt tolerance in switchgrass (Panicum virgatum L.). Plant Cell Rep 37:1187–1199. Scholar
  44. Guo Z, Tan J, Zhuo C, Wang C, Xiang B, Wang Z (2014) Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. falcata that confers cold tolerance through up-regulating polyamine oxidation. Plant Biotechnol J 12:601–612. Scholar
  45. Han B, Fu L, Zhang D, He X, Chen Q, Peng M, Zhang J (2016) Interspecies and intraspecies analysis of trehalose contents and the biosynthesis pathway gene family reveals crucial roles of trehalose in osmotic-stress tolerance in cassava. Int J Mol Sci 17:1–18. Scholar
  46. Hazarika P, Rajam MV (2011) Biotic and abiotic stress tolerance in transgenic tomatoes by constitutive expression of S-adenosylmethionine decarboxylase gene. Physiol Mol Biol Plants 17:115–128. Scholar
  47. He X, Chen Z, Wang J, Li W, Zhao J, Wu J, Wang Z, Chen X (2015) A sucrose: fructan-6-fructosyltransferase (6-SFT) gene from Psathyrostachys huashanica confers abiotic stress tolerance in tobacco. Gene 570:239–247. Scholar
  48. He Y, He C, Li L, Liu Z, Yang A, Zhang J (2011) Heterologous expression of ApGSMT2 and ApDMT2 genes from Aphanothece halophytica enhanced drought tolerance in transgenic tobacco. Mol Biol Rep 38:657–666. Scholar
  49. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends in Plant Science 6(9):431–438PubMedCrossRefGoogle Scholar
  50. Hossain MA, Wani SH, Bhattacharjee S, Burritt DJ, Tran L-SP (2016) Drought stress tolerance in plants, Molecular and genetic perspectives, vol 2, 1st edn. Springer, Berlin. Scholar
  51. Ibragimova SM, Trifonova EA, Filipenko EA, Shymny VK (2015) Evaluation of salt tolerance of transgenic tobacco plants bearing the P5CS1 gene of Arabidopsis thaliana. Russ J Genet 51:1181–1188. Scholar
  52. Ishitani M, Majumder AL, Bornhouser A, Michalowski CB, Jensen RG, Bohnert HJ (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. Plant J 9:537–548.
  53. Jiang Y, Zhu S, Yuan J, Chen G, Lu G (2016) A betaine aldehyde dehydrogenase gene in quinoa (Chenopodium quinoa): structure, phylogeny, and expression pattern. Genes Geno 38:1013–1020. Scholar
  54. Johnson SM, Cummins I, Lim FL, Slabas AR, Knight MR (2015) Transcriptomic analysis comparing stay-green and senescent Sorghum bicolor lines identifies a role for proline biosynthesis in the stay-green trait. J Exp Bot 66:7061–7073. Scholar
  55. Joo J, Choi HJ, Lee YH, Lee S, Lee CH, Kim CH, Cheong JJ, Do Choi Y, Song SI (2014) Over-expression of BvMTSH, a fusion gene for maltooligosyltrehalose synthase and maltooligosyltrehalose trehalohydrolase, enhances drought tolerance in transgenic rice. BMB Rep 47:27–32. Scholar
  56. Joshi R, Ramanarao MV, Baisakh N (2013) Arabidopsis plants constitutively overexpressing a myo-inositol 1-phosphate synthase gene (SaINO1) from the halophyte smooth cordgrass exhibits enhanced level of tolerance to salt stress. Plant Physiol Biochem 65:61–66. Scholar
  57. Jung H, Chung PJ, Park SH, Redillas MCFR, Kim YS, Suh JW, Kim JK (2017) Overexpression of OsERF48 causes regulation of OsCML16, a calmodulin-like protein gene that enhances root growth and drought tolerance. Plant Biotechnol J 15:1295–1308. Scholar
  58. Kanamaru N, Ito Y, Komori S, Saito M, Kato H, Takahashi S, Omura M, Soejima J, Shiratake K, Yamada K, Yamaki S (2004) Transgenic apple transformed by sorbitol-6-phosphate dehydrogenase cDNA. Plant Science 167(1):55–61CrossRefGoogle Scholar
  59. Kathuria H, Giri J, Nataraja KN, Murata N, Udayakumar M, Tyagi AK (2009) Glycinebetaine-induced water-stress tolerance in codA-expressing transgenic indica rice is associated with up-regulation of several stress responsive genes. Plant Biotechnol J 7:512–526. Scholar
  60. Kaur H, Verma P, Petla BP, Rao V, Saxena SC, Majee M (2013) Ectopic expression of the ABA-inducible dehydration-responsive chickpea L-myo-inositol 1-phosphate synthase 2 (CaMIPS2) in Arabidopsis enhances tolerance to salinity and dehydration stress. Planta 237:321–335. Scholar
  61. Ke Q, Wang Z, Ji CY, Jeong JC, Lee HS, Li H, Xu B, Deng X, Kwak SS (2016) Transgenic poplar expressing codA exhibits enhanced growth and abiotic stress tolerance. Plant Physiol Biochem 100:75–84. Scholar
  62. Kido EA, Rc J, Neto F, Silva RLO, Belarmino LC, Neto JPB, Soares-cavalcanti NM, Pandolfi V, Silva MD, Nepomuceno AL, Benko-iseppon AM (2013) Expression dynamics and genome distribution of osmoprotectants in soybean: identifying important components to face abiotic stress. BMC Bioinformatics 14 (Suppl 1):S7PubMedPubMedCentralCrossRefGoogle Scholar
  63. Kido EA, Ferreira-Neto JRC, Pandolfi V, Souza AMS, Benko-Iseppon AM (2016) Drought stress tolerance in plants: insights from transcriptomic studies. In: Drought stress tolerance in plants, Molecular and genetic perspectives, vol 2. Springer, pp 153–186. Scholar
  64. Kim SH, Kim SH, Yoo SJ, Min KH, Nam SH, Cho BH, Yang KY (2013) Putrescine regulating by stress-responsive MAPK cascade contributes to bacterial pathogen defense in Arabidopsis. Biochem Biophys Res Commun 437:502–508. Scholar
  65. Kissoudis C, Kalloniati C, Flemetakis E, Madesis P, Labrou NE, Tsaftaris A, Nianiou-Obeidat I (2015) Stress-inducible GmGSTU4 shapes transgenic tobacco plants metabolome towards increased salinity tolerance. Acta Physiol Plant 37:1–11. Scholar
  66. Ku Y-S, Koo NS-C, Li FW-Y, Li M-W, Wang H, Tsai S-N, Sun F, Lim BL, Ko W-H, Lim BL, Lam H-M (2013) GmSAL1 hydrolyzes inositol-1,4,5-trisphosphate and regulates stomatal closure in detached leaves and ion compartmentalization in plant cells. PLoS One 8:e78181. Scholar
  67. Kusuda H, Koga W, Kusano M, Oikawa A, Saito K, Hirai MY, Yoshida KT (2015) Ectopic expression of myo-inositol 3-phosphate synthase induces a wide range of metabolic changes and confers salt tolerance in rice. Plant Sci 232:49–56. Scholar
  68. Lai SJ, Lai MC, Lee RJ, Chen YH, Yen HE (2014) Transgenic Arabidopsis expressing osmolyte glycine betaine synthesizing enzymes from halophilic methanogen promote tolerance to drought and salt stress. Plant Mol Biol 85:429–441. Scholar
  69. Li D, Zhang T, Wang M, Liu Y, Brestic M, Chen THH, Yang X (2019a) Genetic engineering of the biosynthesis of glycine betaine modulates phosphate homeostasis by regulating phosphate acquisition in tomato. Front Plant Sci 9:1–13. Scholar
  70. Li H, Mo YL, Cui Q, Yang XZ, Guo YL, Wei CH, Yang J, Zhang Y, Ma JX, Zhang X (2019b) Transcriptomic and physiological analyses reveal drought adaptation strategies in drought-tolerant and -susceptible watermelon genotypes. Plant Sci 278:32–43. Scholar
  71. Li HW, Zang BS, Deng XW, Wang XP (2011a) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018. Scholar
  72. Li S, Li F, Wang J, Zhang W, Meng Q, Chen THH, Murata N, Yang X (2011b) Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings. Plant Cell Environ 34:1931–1943. Scholar
  73. Li J, Witten DM, Johnstone IM, Tibshirani R (2012) Normalization, testing, and false discovery rate estimation for RNA-sequencing data. Biostatistics 13:523–538. Scholar
  74. Li L, Li L, Wang X, Zhu P, Wu H, Qi S (2017) Plant growth-promoting endophyte Piriformospora indica alleviates salinity stress in Medicago truncatula. Plant Physiol Biochem 119:211–223. Scholar
  75. Lisko KA, Torres R, Harris RS, Belisle M, Martha M (2013) Elevating vitamin C content via overexpression of myo-inositol oxygenase and L-gulono-1,4-lactone oxidase in Arabidopsis leads to enhanced biomass and tolerance to abiotic stresses. In Vitro Cell Dev Biol Plant 49(6):643–655. Scholar
  76. Liu X, Zhai S, Zhao Y, Sun B, Liu C, Yang A, Zhang J (2013) Overexpression of the phosphatidylinositol synthase gene (ZmPIS) conferring drought stress tolerance by altering membrane lipid composition and increasing ABA synthesis in maize. Plant, Cell & Environment 36(5):1037–1055Google Scholar
  77. Liu C, Zhang X, Zhang K, An H, Hu K, Wen J, Shen J, Ma C, Yi B, Tu J, Fu T (2015) Comparative analysis of the Brassica napus root and leaf transcript profiling in response to drought stress. Int J Mol Sci 16:18752–18777. Scholar
  78. Liu S, Hao H, Lu X, Zhao X, Wang Y, Zhang Y, Xie Z, Wang R (2017a) Transcriptome profiling of genes involved in induced systemic salt tolerance conferred by Bacillus amyloliquefaciens FZB42 in Arabidopsis thaliana. Sci Rep 7:1–13. Scholar
  79. Liu Z, Liu P, Qi D, Peng X, Liu G (2017b) Enhancement of cold and salt tolerance of Arabidopsis by transgenic expression of the S-adenosylmethionine decarboxylase gene from Leymus chinensis. J Plant Physiol 211:90–99. Scholar
  80. Liu ZM, Yue MM, Yang DY, Zhu SB, Ma NN, Meng QW (2017c) Over-expression of SlJA2 decreased heat tolerance of transgenic tobacco plants via salicylic acid pathway. Plant Cell Rep 36(4):529–542. Scholar
  81. Luo D, Niu X, Yu J, Yan J, Gou X, Lu BR, Liu Y (2012) Rice choline monooxygenase (OsCMO) protein functions in enhancing glycine betaine biosynthesis in transgenic tobacco but does not accumulate in rice (Oryza sativa L. ssp. japonica). Plant Cell Rep 31:1625–1635. Scholar
  82. Lv W-T, Lin B, Zhang M, Hua X-J (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933. Scholar
  83. Lyu JI, Park JH, Kim J-K, Bae C-H, Jeong W-J, Min SR, Liu JR (2018) Enhanced tolerance to heat stress in transgenic tomato seeds and seedlings overexpressing a trehalose-6-phosphate synthase/phosphatase fusion gene. Plant Biotechnol Rep 12:399–408. Scholar
  84. Matsumura H, Urasaki N, Yoshida K, Krüger DH, Kahl G, Terauchi R (2012) RNA Abundance Analysis. Life Sci 883:230. Scholar
  85. Missihoun TD, Willèe E, Guegan JP, Berardocco S, Shafiq MR, Bouchereau A, Bartels D (2014) Overexpression of ALDH10A8 and ALDH10A9 genes provides insight into their role in glycine betaine synthesis and affects primary metabolism in Arabidopsis thaliana. Plant Cell Physiol 56:1798–1807. Scholar
  86. Molina-Rueda JJ, Kirby EG (2015) Transgenic poplar expressing the pine GS1a show alterations in nitrogen homeostasis during drought. Plant Physiol Biochem 94:181–190. Scholar
  87. Momtaz OA, Hussein EM, Fahmy EM, Ahmed SE (2010) Expression of S-adenosyl methionine decarboxylase gene for polyamine accumulation in Egyptian cotton Giza 88 and Giza 90. GM Crops 1:257–266. Scholar
  88. Montilla-Bascón G, Rubiales D, Hebelstrup KH, Mandon J, Harren FJM, Montilla-Bascón G, Cristescu SM, Mur LAJ, Prats E (2017) Reduced nitric oxide levels during drought stress promote drought tolerance in barley and is associated with elevated polyamine biosynthesis. Sci Rep 7:1–15. Scholar
  89. Moschen S, Di Rienzo JA, Higgins J, Tohge T, Watanabe M, González S, Rivarola M, García-García F, Dopazo J, Hopp HE, Hoefgen R, Fernie AR, Paniego N, Fernández P, Heinz RA (2017) Integration of transcriptomic and metabolic data reveals hub transcription factors involved in drought stress response in sunflower (Helianthus annuus L.). Plant Mol Biol 94:549–564. Scholar
  90. Nambeesan S, AbuQamar S, Laluk K, Mattoo AK, Mickelbart MV, Ferruzzi MG, Mengiste T, Handa AK (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol 158:1034–1045. Scholar
  91. Niu GL, Gou W, Han XL, Qin C, Zhang LX, Abomohra AEF, Ashraf M (2018) Cloning and functional analysis of phosphoethanolamine methyltransferase promoter from maize (Zea mays L.). Int J Mol Sci 19:13. Scholar
  92. Nishiyama T, Fujita T, Shin-i T, Seki M, Nishide H, Uchiyama I (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: Implication for land plant evolution. Proceedings of the National Academy of Sciences 100(13):8007–8012CrossRefGoogle Scholar
  93. Nokhrina K, Ray H, Bock C, Georges F (2014) Metabolomic shifts in Brassica napus lines with enhanced BnPLC2 expression impact their response to low temperature stress and plant pathogens. GM Crops Food 5:120–131. Scholar
  94. Nyyssölä A, Kerovuo J, Kaukinen P, von Weymarn N, Reinikainen T (2000) Extreme Halophiles Synthesize Betaine from Glycine by Methylation. Journal of Biological Chemistry 275(29):22196–22201PubMedCrossRefGoogle Scholar
  95. Patra B, Ray S, Richter A, Majumder AL (2010) Enhanced salt tolerance of transgenic tobacco plants by co-expression of PcINO1 and McIMT1 is accompanied by increased level of myo-inositol and methylated inositol. Protoplasma 245:143–152. Scholar
  96. Pereira CS, Lins RD, Chandrasekhar I, Freitas LCG, Hu PH (2004) Interaction of the disaccharide trehalose with a phospholipid bilayer: a molecular dynamics study. Biophys J 86(4):2273–2285. Scholar
  97. Peremarti A, Bassie L, Christou P, Capell T (2009) Spermine facilitates recovery from drought but does not confer drought tolerance in transgenic rice plants expressing Datura stramonium S-adenosylmethionine decarboxylase. Plant Mol Biol 70:253–264. Scholar
  98. Provenzano M, Mocellin S (2007) Complementary techniques: validation of gene expression data by quantitative real time PCR. In: Microarray technology and cancer gene profiling. Springer, pp 66–73.
  99. Rajaeian S, Ehsanpour AA, Javadi M, Shojaee B (2017) Ethanolamine induced modification in glycine betaine and proline metabolism in Nicotiana rustica under salt stress. Biol Plant 61:797–800. Scholar
  100. Reddy PS, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kishor PK (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113. Scholar
  101. Ren XW, Yu DW, Yang SP, Gai JY, Zhu YL (2018) Effects of StP5CS gene overexpression on nodulation and nitrogen fixation of vegetable soybean under salt stress conditions. Legume Res 41:675–680. Scholar
  102. Ribeiro PR, Zanotti RF, Deflers C, Fernandez LG, de Castro RD, Ligterink W, Hilhorst HWM (2015) Effect of temperature on biomass allocation in seedlings of two contrasting genotypes of the oilseed crop Ricinus communis. J Plant Physiol 185:31–39. Scholar
  103. Rickes LN, Klumb EK, Benitez LC, Jacira E, Braga B (2019) Differential expression of the genes involved in responses to water-deficit stress in peach trees cv. Chimarrita grafted onto two different rootstocks. Bragantia 78(1):60–70. Scholar
  104. Sagor GHM, Berberich T, Takahashi Y, Niitsu M, Kusano T (2013) The polyamine spermine protects Arabidopsis from heat stress-induced damage by increasing expression of heat shock-related genes. Transgenic Res 22:595–605. Scholar
  105. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183CrossRefGoogle Scholar
  106. Saibi W, Feki K, Ben Mahmoud R, Brini F (2015) Durum wheat dehydrin (DHN-5) confers salinity tolerance to transgenic Arabidopsis plants through the regulation of proline metabolism and ROS scavenging system. Planta 242:1187–1194. Scholar
  107. Slama I, Abdelly C, Bouchereau A, Flowers T, Savouré A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Annals of Botany 115(3):433–447PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sankoff D (2001) Gene and genome duplication. Current Opinion in Genetics & Development 11 (6):681–684Google Scholar
  109. Saurabh S, Vidyarthi AS, Prasad D (2014) RNA interference: Concept to reality in crop improvement. Planta 239:543–564. Scholar
  110. Saxena SC, Salvi P, Kaur H, Verma P, Petla BP, Rao V, Kamble N, Majee M (2013) Differentially expressed myo-inositol monophosphatase gene (CaIMP) in chickpea (Cicer arietinum L.) encodes a lithium-sensitive phosphatase enzyme with broad substrate specificity and improves seed germination and seedling growth under abiotic stresses. J Exp Bot 64:5623–5639. Scholar
  111. Singh A, Jindal S, Longchar B, Khan F, Gupta V (2015) Overexpression of Artemisia annua sterol C-4 methyl oxidase gene, AaSMO1, enhances total sterols and improves tolerance to dehydration stress in tobacco. Plant Cell Tissue Organ Cult 121:167–181. Scholar
  112. Song C, Chung WS, Lim CO (2016) Overexpression of Heat Shock Factor Gene HsfA3 Increases Galactinol Levels and Oxidative Stress Tolerance in Arabidopsis. Mol Cells 39:477–483. Scholar
  113. Song J, Zhang R, Yue D, Chen X, Guo Z, Cheng C, Hu M, Zhang J, Zhang K (2018) Co-expression of ApGSMT2g and ApDMT2g in cotton enhances salt tolerance and increases seed cotton yield in saline fields. Plant Sci 274:369–382. Scholar
  114. Sun X, Xu L, Wang Y, Luo X, Zhu X, Kinuthia KB, Nie S, Feng H, Li C, Liu L (2016) Transcriptome-based gene expression profiling identifies differentially expressed genes critical for salt stress response in radish (Raphanus sativus L.). Plant Cell Rep 35:329–346. Scholar
  115. Sun Y, Fu L, Chen L, Wang X, Song Y, Li Z (2017) Characterization of two winter wheat varieties’ responses to freezing in a frigid region of the People’s Republic of China. Can J Plant Sci 97:808–815. Scholar
  116. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97. Scholar
  117. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426. Scholar
  118. Takabe T, Rai V, Hibino T (2006) Metabolic engineering of glycinebetaine. In: Abiotic stress toler plants. Springer, pp 137–151. Scholar
  119. Tan J, Wang C, Xiang B, Han R, Guo Z (2013) Hydrogen peroxide and nitric oxide mediated cold-and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ 36(2):288–299. Scholar
  120. Tang W, Sun J, Liu J, Liu F, Yan J (2014) RNAi-directed downregulation of betaine aldehyde dehydrogenase 1 (OsBADH1) results in decreased stress tolerance and increased oxidative markers without affecting glycine betaine biosynthesis in rice (Oryza sativa). Plant Molecular Biology 86(4-5):443–454PubMedCrossRefGoogle Scholar
  121. Tiwari LD, Mittal D, Mishra RC, Grover A (2015) Constitutive over-expression of rice chymotrypsin protease inhibitor gene OCPI2 results in enhanced growth, salinity and osmotic stress tolerance of the transgenic Arabidopsis plants. Plant Physiol Biochem 92:48–55. Scholar
  122. Tsutsumi K, Yamada N, Cha-um S, Tanaka Y, Takabe T (2015) Differential accumulation of glycinebetaine and choline monooxygenase in bladder hairs and lamina leaves of Atriplex gmelinii under high salinity. J Plant Physiol 176:101–107. Scholar
  123. Vaishnav A, Choudhary DK (2018) Regulation of Drought-Responsive Gene Expression in Glycine max L. merrill is mediated through Pseudomonas simiae strain AU. J Plant Growth Regul 38(1):333–342. Scholar
  124. Wang T, Lu L, Zhang C, Taylor C, Thompson JE (2003) Pleiotropic effects of suppressing deoxyhypusine synthase expression in Arabidopsis thaliana. Plant Molecular Biology 52(6):1223–1235PubMedCrossRefGoogle Scholar
  125. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics 10(1):57–63PubMedPubMedCentralCrossRefGoogle Scholar
  126. Wang J, Sun P, Chen C, Wang Y, Fu X, Liu J (2011) An arginine decarboxylase gene PtADC from Poncirus trifoliata confers abiotic stress tolerance and promotes primary root growth in Arabidopsis. Journal of Experimental Botany 62(8):2899–2914PubMedCrossRefGoogle Scholar
  127. Wang CL, Zhang SC, Qi SD, Zheng CC, Wu CA (2016a) Delayed germination of Arabidopsis seeds under chilling stress by overexpressing an abiotic stress inducible GhTPS11. Gene 575:206–212. Scholar
  128. Wang FW, Wang ML, Guo C, Wang N, Li XW, Chen H, Dong YY, Chen XF, Wang ZM, Li HY (2016b) Cloning and characterization of a novel betaine aldehyde dehydrogenase gene from Suaeda corniculata. Genetics and Molecular Research 15(2)Google Scholar
  129. Wang J, Lan X, Jiang S, Ma Y, Zhang S, Li Y, Li X, Lan H (2017) CaMKK1 from Chenopodium album positively regulates salt and drought tolerance in transgenic tobacco. Plant Cell Tissue Organ Cult 130:209–225. Scholar
  130. Wang J-Y, Lai L-D, Tong S-M, Li Q-L (2013) Constitutive and salt-inducible expression of SlBADH gene in transgenic tomato (Solanum lycopersicum L. cv. Micro-Tom) enhances salt tolerance. Biochem Biophys Res Commun 432:262–267. Scholar
  131. Wang Q, Xu W, Xue Q, Su W (2010) Transgenic Brassica chinensis plants expressing a bacterial codA gene exhibit enhanced tolerance to extreme temperature and high salinity. J Zhejiang Univ Sci B 11:851–861. Scholar
  132. Wang W, Liu JH (2016c) CsPAO4 of Citrus sinensis functions in polyamine terminal catabolism and inhibits plant growth under salt stress. Sci Rep 6:1–15. Scholar
  133. Wang X, Du Y, Yu D (2018) Trehalose phosphate synthase 5-dependent trehalose metabolism modulates basal defense responses in Arabidopsis thaliana. J Integrat Plant Biol 61:509. Scholar
  134. Wei C, Cui Q, Zhang XQ, Zhao YQ, Jia GX (2016) Three P5CS genes including a novel one from Lilium regale play distinct roles in osmotic, drought and salt stress tolerance. J Plant Biol 59:456–466. Scholar
  135. 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. Elsevier Ireland Ltd. Plant Sci 257:74–83CrossRefGoogle Scholar
  136. Wei JZ, Jerry Chatterton N, Larson SR (2001) Expression of sucrose:fructan 6-fructosyltransferase (6-SFT) and myo-inositol 1-phosphate synthase (MIPS) genes in barley (Hordeum vulgare) leaves. J Plant Physiol 158:635–643. Scholar
  137. Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2010) Spermidine levels are implicated in heavy metal tolerance in a spermidine synthase overexpressing transgenic european pear by exerting antioxidant activities. Transgenic Res 19:91–103. Scholar
  138. Wu H, Zhang Y, Zhang W, Pei X, Zhang C, Jia S, Li W (2015) Transcriptomic analysis of the primary roots of Alhagi sparsifolia in response to water stress. PLoS One 10:1–25. Scholar
  139. Wu S, Su Q, An L (2010) Isolation of choline monooxygenase (CMO) gene from Salicornia europaea and enhanced salt tolerance of transgenic tobacco with CMO genes. Indian J Biochem Biophys 47:298–305PubMedGoogle Scholar
  140. 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 9:1–14. Scholar
  141. Yadav R, Verma OP, Padaria JC (2018) Transcript profiling and gene expression analysis under drought stress in Ziziphus nummularia (Burm.f.) Wright & Arn. Mol Biol Rep 45:163–174. Scholar
  142. Yamada N, Takahashi H, Kitou K, Sahashi K, Tamagake H, Tanaka Y, Takabe T (2015) Suppressed expression of choline monooxygenase in sugar beet on the accumulation of glycine betaine. Plant Physiol Biochem 96:217–221. Scholar
  143. Yang C, Zhou Y, Fan J, Fu Y, Shen L, Yao Y, Li R, Fu S, Duran R, Hu X, Guo J (2015a) SpBADH of the halophyte Sesuvium portulacastrum strongly confers drought tolerance through ROS scavenging in transgenic Arabidopsis. Plant Physiol Biochem 96:377–387. Scholar
  144. Yang SL, Chen K, Wang SS, Gong M (2015b) Osmoregulation as a key factor in drought hardening-induced drought tolerance in Jatropha curcas. Biol Plant 59:529–536. Scholar
  145. Yang SL, Lan SS, Deng FF, Gong M (2016) Effects of calcium and calmodulin antagonists on chilling stress-induced proline accumulation in Jatropha curcas L. J Plant Growth Regul 35:815–826. Scholar
  146. Yang Y, Li X, Kong X, Ma L, Hu X, Yang Y (2015c) Transcriptome analysis reveals diversified adaptation of Stipa purpurea along a drought gradient on the Tibetan Plateau. Funct Integr Genomics 15:295–307. Scholar
  147. Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-um S (2017) Water-deficit tolerance in sweet potato [Ipomoea batatas (L.) Lam.] by foliar application of paclobutrazol: role of soluble sugar and free proline. Front Plant Sci 8:1–13. Scholar
  148. Yu C, Qiao G, Qiu W, Yu D, Zhou S, Shen Y, Yu G, Jiang J, Han X, Liu M, Zhang L, Chen F, Chen Y, Zhuo R (2018) Molecular breeding of water lily: engineering cold stress tolerance into tropical water lily. Horticulture Research 5(1)Google Scholar
  149. Zhai SM, Gao Q, Xue HW, Sui ZH, Yue GD, Yang AF, Zhang JR (2012) Overexpression of the phosphatidylinositol synthase gene from Zea mays in tobacco plants alters the membrane lipids composition and improves drought stress tolerance. Planta 235(1):69–84PubMedCrossRefGoogle Scholar
  150. Zhai H, Wang F, Si Z, Huo J, Xing L, An Y, He S, Liu Q (2015) A myo-inositol-1-phosphate synthase gene, IbMIPS1, enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. Plant Biotechnol J 14:592–602. Scholar
  151. Zhang J, Yang N, Li Y, Zhu S, Zhang S, Sun Y, Zhang HX, Wang L, Su H (2018) Overexpression of PeMIPS1 confers tolerance to salt and copper stresses by scavenging reactive oxygen species in transgenic poplar. Tree Physiol 38:1566–1577. Scholar
  152. Zhang RX, Qin LJ, Zhao DG (2017) Overexpression of the OsIMP gene increases the accumulation of inositol and confers enhanced cold tolerance in tobacco through modulation of the antioxidant enzymes’ activities. Genes (Basel) (7):8. Scholar
  153. Zhu J-Q, Zhang J-T, Tang R-J, Lv Q-D, Wang Q-Q, Yang L, Zhang H-X (2009) Molecular characterization of ThIPK2, an inositol polyphosphate kinase gene homolog from Thellungiella halophila, and its heterologous expression to improve abiotic stress tolerance in Brassica napus. Physiol Plant 136:407–425. Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Éderson Akio Kido
    • 1
  • José Ribamar Costa Ferreira-Neto
    • 1
  • Manassés Daniel da Silva
    • 1
  • Vanessa Emanuelle Pereira Santos
    • 1
  • Jorge Luís Bandeira da Silva Filho
    • 1
  • Ana Maria Benko-Iseppon
    • 1
  1. 1.Department of GeneticsFederal University of PernambucoRecifeBrazil

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