Manipulating Metabolic Pathways for Development of Salt-Tolerant Crops

Chapter
First Online:

Abstract

Engineering plants for salt stress tolerance is a complex process due to the multiple-sided characteristics of stress coping mechanisms. The common approach was first identification of the components of signalling and regulatory pathways for salinity tolerance, then transformation of plants with one of those genes and phenotyping the transgenic plant subjected to salt stress at controlled conditions. Plant biology literature is full of research papers on the success of such plants to acclimate and survive under salinity; however, to date none of them was able to become a commercial variety having improved performance at field conditions. Disturbing or interfering with complex networks and pathways can result in unexpected effects on plant growth and development. Furthermore, tolerance against one stress would not be efficient to cope with different environmental stress factors which field-grown plants encounter during a single growth season.

Instead of targeting signalling or regulatory networks, manipulating metabolic routes for higher osmotic and ionic stress tolerance would be more realistic to mitigate negative impact of salt stress on crop plants. At field conditions coping well with osmotic and ionic stresses will double the chance of crop plants to overcome other challenges such as drought, nutrient and high temperature. Absolutely manipulating plant metabolism is also a complex task, but it is worth to put an effort since modifying common tolerance routes such as osmoregulation, antioxidant capacity and ion transport mechanisms will be more promising at field conditions for the whole plant life cycle. In this chapter we tried to collect and point out the recent information on metabolism in relation to salt stress tolerance and focused on more feasible efforts for the achievement of this purpose in crop plants at field conditions.

Keywords

Primary metabolism Cellular homeostasis Metabolite Abiotic stress Salinity tolerance Osmotic adjustment Reactive oxygen species Trade-offs Polyamine metabolism Sugar metabolism Halophytes Glycophytes 

Abbreviations

ABA

Abscisic acid

ADC

Arginine decarboxylase

GABA

Gamma amino butyric acid

GC-MS

Gas chromatography-mass spectrometry

H2O2

Hydrogen peroxide

HKT

High-affinity potassium transporter

LEA

Late embryogenesis abundant

LTP

Lipid transfer protein

MDH

Malate dehydrogenase

MTMM

Multi-trait mixed model

NaCl

Sodium chloride

NATA1

N-acetyltransferase activity 1

ODC

Ornithine decarboxylase

PA

Polyamine

PLC1

Phospholipase C1

PLD

Phospholipase D

Put

Putrescine

ROS

Reactive oxygen species

SAMDC

S-adenosylmethionine synthetase

SA

Salicylic acid

SFR

Sensitive to freezing

SKC1

Sodium ion transmembrane transporter activity 1

SnRK1

Sucrose nonfermenting-related kinase1

SOS1

Salt overly sensitive 1

Spd

Spermidine

Spm

Spermine

TCA

Tricarboxylic acid

T6P

Trehalose-6-phosphate

UDPGlc

Uridine-diphosphate-glucose

This is a preview of subscription content, log in to check access.

References

  1. Abebe T, Guenzi AC, Martin B et al (2003) Tolerance of mannitol accumulating transgenic wheat to water stress and salinity. Plant Physiol 131:1748–1755PubMedPubMedCentralCrossRefGoogle Scholar
  2. Albacete A, Ghanem ME, Martínez-Andújar C et al (2008) Hormonal changes in relation to biomass partitioning and shoot growth impairment in salinized tomato (Solanum lycopersicum L.) plants. J Exp Bot 59:4119–4131PubMedPubMedCentralCrossRefGoogle Scholar
  3. Albacete AA, Martínez-Andújar C, Pérez-Alfocea F (2014) Hormonal and metabolic regulation of source–sink relations under salinity and drought: from plant survival to crop yield stability. Biotechnol Adv 32:12–30PubMedCrossRefGoogle Scholar
  4. Alet AI, Sánchez DH, Cuevas JC et al (2012) New insights into the role of spermine in Arabidopsis thaliana under long-term salt stress. Plant Sci 182:94–100PubMedCrossRefGoogle Scholar
  5. Arbona V, Manzi M, Ollas C et al (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14:4885–4911PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baghalian K, Hajirezaei RM, Schreiber F (2014) Plant metabolic modelling: achieving new insight into metabolism and metabolic engineering. Plant Cell 26:3847–3866PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bargmann BOR, Laxalt AM, Riet B et al (2009) Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant Cell Physiol 50(1):78–89PubMedCrossRefGoogle Scholar
  8. Bianchi G, Gamba A, Limiroli R et al (1993) The unusual sugar composition in leaves of the resurrection plant Myrothamnus flabellifolia. Physiol Plant 87:223–226CrossRefGoogle Scholar
  9. Bor M, Ozdemir F, Turkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Sci 164:77–84CrossRefGoogle Scholar
  10. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257PubMedCrossRefGoogle Scholar
  11. Cabello JV, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70PubMedCrossRefGoogle Scholar
  12. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedCrossRefGoogle Scholar
  13. Cortina C, Culianez-Macia FA (2005) Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Sci 169:75–82CrossRefGoogle Scholar
  14. Darwish E, Testerink C, Khalil M et al (2009) Phospholipid signalling responses in salt-stressed rice leaves. Plant Cell Physiol 50:986–997PubMedPubMedCentralCrossRefGoogle Scholar
  15. Demidchik V, Maathuis FJM (2007) Physiological roles of non-selective cation channels in plants: from salt stress to signalling and development. New Phytol 175:387–404PubMedCrossRefGoogle Scholar
  16. DeWald DB, Torabinejad J, Jones CA et al (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 126:759–769PubMedPubMedCentralCrossRefGoogle Scholar
  17. Do TP, Drechsel O, Heyer GA et al (2014) Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought. Front Plant Sci 5(182):1–16Google Scholar
  18. Drennan P, Smith M, Goldsworthy D et al (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius welw. J Plant Physiol 142:493–496CrossRefGoogle Scholar
  19. Endler A, Kesten C, Schneider R et al (2015) A mechanism for sustained cellulose synthesis during salt stress. Cell 162:1353–1364PubMedCrossRefGoogle Scholar
  20. Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119–130PubMedCrossRefGoogle Scholar
  21. Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963PubMedCrossRefGoogle Scholar
  22. Flowers T, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115(3):419–431PubMedCrossRefGoogle Scholar
  23. Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28:1056–1071CrossRefGoogle Scholar
  24. Fusari CM, Kooke R, Lauxmann MA et al (2017) Genome-wide association mapping reveals that specific and pleiotropic regulatory mechanisms fine-tune central metabolism and growth in Arabidopsis. Plant Cell. https://doi.org/10.1105/tpc.17.00232
  25. Garcia AB, Engler J, Iyer S et al (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159–169PubMedPubMedCentralCrossRefGoogle Scholar
  26. Garg AK, Kim JK, Owens TG et al (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. PNAS 99:15898–15903PubMedPubMedCentralCrossRefGoogle Scholar
  27. Garlock RJ, Wong YS, Balan V et al (2012) AFEX pretreatment and enzymatic conversion of black locust (Robinia pseudoacacia L.) to soluble sugars. Bioenergy Res 5(2):306–318CrossRefGoogle Scholar
  28. Gasulla F, Vom Dorp K, Dombrink I et al (2013) The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J 75:726–741PubMedCrossRefGoogle Scholar
  29. Ghaffari MR, Ghabooli M, Khatabi B et al (2016) Metabolic and transcriptional response of central metabolism affected by root endophytic fungus Piriformospora indica under salinity in barley. Plant Mol Biol 90:699–717PubMedCrossRefGoogle Scholar
  30. Gigon A, Matos AR, Laffray D et al (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Ann Bot 94:345–351PubMedPubMedCentralCrossRefGoogle Scholar
  31. Guo R, Yang Z, Li F et al (2015) Comparative metabolic responses and adaptive strategies of wheat (Triticum aestivum) to salt and alkali stress. BMC Plant Biol 15:170PubMedPubMedCentralCrossRefGoogle Scholar
  32. Guo R, Shi XL, Yan C et al (2017) Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biol 17(41):1–13Google Scholar
  33. Hamed KB, Ellouzi H, Talbi OZ et al (2013) Physiological response of halophytes to multiple stresses. Funct Plant Biol 40:883–896Google Scholar
  34. Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553CrossRefGoogle Scholar
  35. Henry C, Samuel Bledsoe SW, Griffiths CA et al (2015) Differential role for trehalose metabolism in salt-stressed maize. Plant Physiol 169:1072–1089PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hildebrandt TM, Nunes Nesi A, Araujo WL et al (2015) Amino acid catabolism in plants. Mol Plant 8:1563–1579PubMedCrossRefGoogle Scholar
  37. Hoang TML, Tran NT, Nguyen TKT et al (2016) Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy 6(54):1–23Google Scholar
  38. Jang IC, Oh SJ, Seo JS et al (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524PubMedPubMedCentralCrossRefGoogle Scholar
  39. Jayakannan M, Bose J, Babourina O et al (2013) Salicylic acid improves salinity tolerance in Arabidopsis by restoring membrane potential and preventing salt-induced K+ loss via a GORK channel. J Exp Bot 64:2255–2268PubMedPubMedCentralCrossRefGoogle Scholar
  40. Jayakannan M, Bose J, Babourina O et al (2015) The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J Exp Bot 66(7):1865–1875PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jones R, Ougham H, Howard T et al (2013) The molecular life of plants, 1st edn. Wiley Hoboken (New Jersey) USAGoogle Scholar
  42. Kim DW, Watanabe K, Murayama C et al (2014) Polyamine oxidase5 regulates Arabidopsis growth through thermospermine oxidase activity. Plant Physiol 165:1575–1590PubMedPubMedCentralCrossRefGoogle Scholar
  43. Li L, Wang F, Yan P et al (2017) A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice. New Phytol 214:1172–1187PubMedCrossRefGoogle Scholar
  44. Liu JP, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596PubMedPubMedCentralCrossRefGoogle Scholar
  45. Lou YR, Bor M, Yan J et al (2016) Arabidopsis NATA1 acetylates putrescine and decreases defence-related hydrogen peroxide accumulation. Plant Physiol 171(2):1443–1455PubMedPubMedCentralGoogle Scholar
  46. Maron GL, Pineros AM, Kochian VL et al (2016) Redefining ‘stress resistance genes’, and why it matters. J Exp Bot 67(19):5588–5591PubMedPubMedCentralCrossRefGoogle Scholar
  47. McLoughlin F, Arisz SA, Dekker HL et al (2013) Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem J 450:573–581PubMedCrossRefGoogle Scholar
  48. Mickelbart MV, Hasegawa PM, Bailey-Serres J (2015) Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet 16:237–251PubMedCrossRefGoogle Scholar
  49. Mittler R, Vanderauwera S, Gollery M et al (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  50. Mittova V, Tal M, Volokita M et al (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856PubMedCrossRefGoogle Scholar
  51. Morandini P (2009) Rethinking metabolic control. Plant Sci 176:441–451PubMedCrossRefGoogle Scholar
  52. Morandini P (2013) Control limits for accumulation of plant metabolites: brute force is no substitute for understanding. Plant Biotechnol J 11:253–267PubMedCrossRefGoogle Scholar
  53. Moschou PN, Roubelakis-Angelakis KA (2013) Polyamines and programmed cell death. J Exp Bot 65:1285–1296PubMedCrossRefGoogle Scholar
  54. Munnik T (2014) PI-PLC: phosphoinositide-phospholipase C in plant signalling. In: Wang X (ed) Phospholipases in plant signalling. Springer, Berlin, pp 27–54CrossRefGoogle Scholar
  55. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefGoogle Scholar
  56. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedCrossRefGoogle Scholar
  57. Munns R, Gilliham M (2015) Salinity tolerance of crops – what is the cost? New Phytol 208:668–673PubMedCrossRefGoogle Scholar
  58. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  59. Munns R, James RA, Xu B et al (2012) Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30:360–364PubMedCrossRefGoogle Scholar
  60. Nuccio ML, Wu J, Mowers R et al (2015) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat Biotechnol 33(8):862–874PubMedCrossRefGoogle Scholar
  61. Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243PubMedPubMedCentralCrossRefGoogle Scholar
  62. Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J 79:584–596PubMedCrossRefGoogle Scholar
  63. Ozgur R, Uzilday B, Sekmen AH et al (2013) Reactive oxygen species regulation and antioxidant defence in halophytes. Funct Plant Biol 40:832–847Google Scholar
  64. Pandey M, Penna S (2017) Time course of physiological, biochemical, and gene expression changes under short-term salt stress in Brassica juncea L. Crop J 5(3):219–230CrossRefGoogle Scholar
  65. Paul MJ, Primavesi LF, Jhurreea D et al (2008) Trehalose metabolism and signalling. Annu Rev Plant Biol 59:417–441PubMedCrossRefGoogle Scholar
  66. Peng Z, He S, Sun J et al (2016) Na+ compartmentalization related to salinity stress tolerance in upland cotton (Gossypium hirsutum) seedlings. Sci Rep 6:34548PubMedPubMedCentralCrossRefGoogle Scholar
  67. Pieslinger AM, Hoepflinger MC, Tenhaken R (2010) Cloning of glucuronokinase from Arabidopsis thaliana, the last missing enzyme of the myo-inositol oxygenase pathway to nucleotide sugars. J Biol Chem 285:2902–2910PubMedCrossRefGoogle Scholar
  68. Pitzschke A, Datta S, Persak H (2014) Salt stress in Arabidopsis: lipid transfer protein AZI1 and its control by mitogen-activated protein kinase MPK3. Mol Plant 7(4):722–738PubMedCrossRefGoogle Scholar
  69. Pottosin I, Shabala S (2014) Polyamines: control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signalling. Front Plant Sci 5(154):1–16Google Scholar
  70. Ramadan T, Flowers TJ (2004) Effects of salinity and benzyl adenine on development and function of microhairs of Zea mays L. Planta 219:639–648PubMedCrossRefGoogle Scholar
  71. Ren ZH, Gao JP, Li LG et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146PubMedCrossRefGoogle Scholar
  72. Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384CrossRefGoogle Scholar
  73. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613PubMedCrossRefGoogle Scholar
  74. Roitsch T, Balibrea ME, Hofmann M et al (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524PubMedCrossRefGoogle Scholar
  75. Rosa M, Prado C, Podazza G et al (2009) Soluble sugars—metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393PubMedPubMedCentralCrossRefGoogle Scholar
  76. Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869–875PubMedCrossRefGoogle Scholar
  77. Roy M, Wu R (2002) Over expression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride stress tolerance. Plant Sci 163:987–992CrossRefGoogle Scholar
  78. Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124PubMedCrossRefGoogle Scholar
  79. Sakamoto A, Murata A (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019PubMedCrossRefGoogle Scholar
  80. Sanchez DH, Siahpoosh MR, Roessner U et al (2007) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol Plant 132:209–219Google Scholar
  81. Sekmen AH, Bor M, Ozdemir F et al (2014) Current concepts about salinity and salinity tolerance in plants. In: Tuteja N, Gill SS (eds) Climate change and plant abiotic stress tolerance. Wiley-VCH Verlag GmbH Co. KGaA, Weinheim, pp 163–188Google Scholar
  82. Shabala S (2009) Salinity and programmed cell death: unravelling mechanisms for ion specific signalling. J Exp Bot 60:709–711PubMedCrossRefGoogle Scholar
  83. Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 112:1209–1221PubMedPubMedCentralCrossRefGoogle Scholar
  84. Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669PubMedCrossRefGoogle Scholar
  85. Shabala S, Munns R (2012) Salinity stress: physiological constraints and adaptive mechanisms. In: Shabala S (ed) Plant stress physiology, 1st edn. CABI, Wallingford, pp 59–93CrossRefGoogle Scholar
  86. Shabala S, Munns R (2017) Salinity stress: physiological constraints and adaptive mechanisms. In: Shabala S (ed) Plant stress physiology, 2nd edn. CABI, Wallingford, pp 24–63CrossRefGoogle Scholar
  87. Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222PubMedCrossRefGoogle Scholar
  88. Slama I, Abdelly C, Bouchereau A et al (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115:433–447PubMedPubMedCentralCrossRefGoogle Scholar
  89. Stitt M, Gibon Y, Lunn JE et al (2007) Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment. Funct Plant Biol 34:526CrossRefGoogle Scholar
  90. Suárez R, Calderón C, Iturriaga G (2009) Enhanced tolerance to multiple abiotic stresses in transgenic alfalfa accumulating trehalose. Crop Sci 49:1791–1799CrossRefGoogle Scholar
  91. Sun X, Cahill J, Van Hautegem T et al (2017) Altered expression of maize PLASTOCHRON1 enhances biomass and seed yield by extending cell division duration. Nat Commun 8(14752):1–11Google Scholar
  92. Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97PubMedCrossRefGoogle Scholar
  93. Taji T, Seki M, Satou M et al (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709PubMedPubMedCentralCrossRefGoogle Scholar
  94. Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105:1–6PubMedCrossRefGoogle Scholar
  95. Takahashi Y, Cong R, Sagor GHM et al (2010) Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep 29:955–965PubMedCrossRefGoogle Scholar
  96. Takahashi F, Tilbrook J, Trittermann C et al (2015) Comparison of leaf sheath transcriptome profiles with physiological traits of bread wheat cultivars under salinity stress. PLoS One 10(8):1–23Google Scholar
  97. Tavladoraki P, Rossi MN, Saccuti G et al (2006) Heterologous expression and biochemical characterization of a polyamine oxidase from Arabidopsis involved in polyamine back conversion. Plant Physiol 141:1519–1532PubMedPubMedCentralCrossRefGoogle Scholar
  98. Thoen MPM, Davila Olivas NH, Kloth KJ et al (2017) Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping. New Phytol 213:1346–1362PubMedCrossRefGoogle Scholar
  99. Velarde-Buendía AM, Shabala S, Cvikrova M et al (2012) Salt-sensitive and salt-tolerant barley varieties differ in the extent of potentiation of the ROS-induced K+ efflux by polyamines. Plant Physiol Biochem 61:18–23PubMedCrossRefGoogle Scholar
  100. Wang H, Zhang M, Guo R et al (2012) Effects of salt stress on ion balance and nitrogen metabolism of old and young leaves in rice (Oryza sativa L.) BMC Plant Biol 12(194):1–11Google Scholar
  101. Wang K, Hersh LH, Benning C (2016a) Sensitive to freezing2 aids in resilience to salt and drought in freezing-sensitive tomato. Plant Physiol 172:1432–1442PubMedPubMedCentralCrossRefGoogle Scholar
  102. Wang JQ, Sun H, Dong LQ et al (2016b) The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant Biotechnol J 14:1986–1997PubMedPubMedCentralCrossRefGoogle Scholar
  103. White AC, Rogers A, Rees M et al (2015) How can we make plants grow faster? A source–sink perspective on growth rate. J Exp Bot 67:31–45PubMedCrossRefGoogle Scholar
  104. Wu D, Cai S, Chen M et al (2013) Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS One 8(1):1–11Google Scholar
  105. Xia JX, Zhou YH, Shi K et al (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66(10):2839–2856PubMedCrossRefGoogle Scholar
  106. Xiao W, Hu S, Zhou X et al (2017) A glucuronokinase gene in Arabidopsis, AtGlcAK, is involved in drought tolerance by modulating sugar metabolism. Plant Mol Biol Report 35:298–311CrossRefGoogle Scholar
  107. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830PubMedCrossRefGoogle Scholar
  108. Yolcu S, Özdemir F, Güler A et al (2016) Histone acetylation influences the transcriptional activation of POX in Beta vulgaris L. and Beta maritima L. under salt stress. Plant Physiol Biochem 100:37–46PubMedCrossRefGoogle Scholar
  109. Yu A, Lepere G, Jay F et al (2013) Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. PNAS USA 110:2389–2394PubMedPubMedCentralCrossRefGoogle Scholar
  110. Zarza X, Atanasov KE, Marco F et al (2017) Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant Cell Environ 40:527–542PubMedCrossRefGoogle Scholar
  111. Zepeda-Jazo I, Velarde-Buendía AM, Enríquez-Figueroa R et al (2011) Polyamines interact with hydroxyl radicals in activating Ca2+ and K+ transport across the root epidermal plasma membranes. Plant Physiol 157:2167–2180PubMedPubMedCentralCrossRefGoogle Scholar
  112. Züst T, Agrawal AA (2017) Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annu Rev Plant Biol 68:513–534PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyUniversity of EgeİzmirTurkey

Personalised recommendations