Advertisement

Molecular Biology Reports

, Volume 47, Issue 2, pp 1459–1470 | Cite as

The dynamic responses of plant physiology and metabolism during environmental stress progression

  • Amit Kumar Singh
  • Shanmuhapreya Dhanapal
  • Brijesh Singh YadavEmail author
Review
  • 207 Downloads

Abstract

At adverse environmental conditions, plants produce various kinds of primary and secondary metabolites to protect themselves. Both primary and secondary metabolites play a significant role during the heat, drought, salinity, genotoxic and cold conditions. A multigene response is activated during the progression of these stresses in the plants which stimulate changes in various signaling molecules, amino acids, proteins, primary and secondary metabolites. Plant metabolism is perturbed because of either the inhibition of metabolic enzymes, shortage of substrates, excess demand for specific compounds or a combination of these factors. In this review, we aim to present how plants synthesize different kinds of natural products during the perception of various abiotic stresses. We also discuss how time-scale variable stresses influence secondary metabolite profiles, could be used as a stress marker in plants. This article has the potential to get the attention of researchers working in the area of quantitative trait locus mapping using metabolites as well as metabolomics genome-wide association.

Keywords

Environmental stress Secondary metabolites Signaling pathways Transcription factors Networks 

Notes

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Abdelrahman M, El-Sayed M, Jogaiah S, Burritt DJ, Tran LSP (2017) The “STAY-GREEN” trait and phytohormone signaling networks in plants under heat stress. Plant Cell Rep 36(7):1009–1025PubMedGoogle Scholar
  2. 2.
    Abdelrahman M, Jogaiah S, Burritt DJ, Tran LSP (2018) Legume genetic resources and transcriptome dynamics under abiotic stress conditions. Plant Cell Environ 41(9):1972–1983PubMedGoogle Scholar
  3. 3.
    Angelova Z, Georgiev S, Roos W (2006) Elicitation of plants. Biotechnol Biotechnol Equip 20:72–83Google Scholar
  4. 4.
    Arakawa O, Hori Y, Ogata R (1985) Relative effectiveness and interaction of ultraviolet-B, red and blue light in anthocyanin synthesis of apple fruit. Physiol Plant 64(3):323–327Google Scholar
  5. 5.
    Arbona V, Gómez-Cadenas A (2008) Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27(3):241Google Scholar
  6. 6.
    Arbona V, Manzi M, Ollas C, Gómez-Cadenas A (2013) Metabolomics as a tool to investigate abiotic stress tolerance in plants. Int J Mol Sci 14(3):4885–4911PubMedPubMedCentralGoogle Scholar
  7. 7.
    Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448(7156):938PubMedGoogle Scholar
  8. 8.
    Bahler BD, Steffen KL, Orzolek MD (1991) Morphological and biochemical comparison of a purple-leafed and a green-leafed pepper cultivar. HortScience 26(6):736Google Scholar
  9. 9.
    Boundsocq M, Barbier-Brygoo H, Lauriere C (2004) Identification of nine sucrose non-fermenting 1-related protein kinase 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J Biol Chem 279:41758–41766Google Scholar
  10. 10.
    Breckle SW (2002) Salinity, halophytes and salt affected natural ecosystems. Salinity: environment-plants-molecules. Springer, Dordrecht, pp 53–77Google Scholar
  11. 11.
    Bulgari Roberta, Franzoni Giulia, Ferrante Antonio (2019) Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy 9(6):306Google Scholar
  12. 12.
    Byrt CS, Munns R, Burton RA, Gilliham M, Wege S (2018) Root cell wall solutions for crop plants in saline soils. Plant Sci 269:47–55PubMedGoogle Scholar
  13. 13.
    Calzadilla PI, Vilas JM, Escaray FJ, Unrein F, Carrasco P, Ruiz OA (2019) The increase of photosynthetic carbon assimilation as a mechanism of adaptation to low temperature in Lotus japonicus. Sci Rep 9(1):863PubMedPubMedCentralGoogle Scholar
  14. 14.
    Chan LK, Koay SS, Boey PL, Bhatt A (2010) Effects of abiotic stress on biomass and anthocyanin production in cell cultures of Melastoma malabathricum. Biol Res 43(1):127–135PubMedGoogle Scholar
  15. 15.
    Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12(10):444–451PubMedGoogle Scholar
  16. 16.
    Colinet H, Larvor V, Laparie M, Renault D (2012) Exploring the plastic response to cold acclimation through metabolomics. Funct Ecol 26(3):711–722Google Scholar
  17. 17.
    Daneshmand F, Arvin MJ, Kalantari KM (2010) Physiological responses to NaCl stress in three wild species of potato in vitro. Acta Physiol Plant 32(1):91Google Scholar
  18. 18.
    de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21(8):677–685PubMedGoogle Scholar
  19. 19.
    Dong CH, Zolman BK, Bartel B, Lee BH, Stevenson B, Agarwal M, Zhu JK (2009) Disruption of Arabidopsis CHY1 reveals an important role of metabolic status in plant cold stress signaling. Mol Plant 2(1):59–72PubMedPubMedCentralGoogle Scholar
  20. 20.
    Du W, Lin H, Wu Y, Zhang J, Chen S, Fuglsang AT et al (2011) Phosphorylation of SOS3-like Calcium Binding Proteins by their interacting SOS2-like Protein Kinases is a common regulatory mechanism in Arabidopsis. Plant Physiol 156:111Google Scholar
  21. 21.
    Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C et al (2011) Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 23:111Google Scholar
  22. 22.
    Farriol M, Segovia T, Venereo Y, Orta X (1999) Importance of the polyamines: review of the literature. Nutr Hosp 14(3):101–113PubMedGoogle Scholar
  23. 23.
    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 Natl Acad Sci 99(25):15898–15903PubMedGoogle Scholar
  24. 24.
    Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H et al (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci 106(50):21425–21430PubMedGoogle Scholar
  25. 25.
    Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930PubMedPubMedCentralGoogle Scholar
  26. 26.
    Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9(8):399–405PubMedGoogle Scholar
  27. 27.
    Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34(1):35PubMedGoogle Scholar
  28. 28.
    Guo R, Shi L, Jiao Y, Li M, Zhong X, Gu F et al (2018) Metabolic responses to drought stress in the tissues of drought-tolerant and drought-sensitive wheat genotype seedlings. AoB Plants 10(2):ply016PubMedPubMedCentralGoogle Scholar
  29. 29.
    Gupta S, Yadav BS, Raj U, Freilich S, Varadwaj PK (2017) Transcriptomic analysis of soil grown T. aestivum cv. root to reveal the changes in expression of genes in response to multiple nutrients deficiency. Front Plant Sci 8:1025PubMedPubMedCentralGoogle Scholar
  30. 30.
    Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132(2):220–235PubMedGoogle Scholar
  31. 31.
    Hagemeyer J (2004) Ecophysiology of plant growth under heavy metal stress. Heavy metal stress in plants. Springer, Berlin, pp 201–222Google Scholar
  32. 32.
    Haider MS, Jogaiah S, Pervaiz T, Yanxue Z, Khan N, Fang J (2019) Physiological and transcriptional variations inducing complex adaptive mechanisms in grapevine by salt stress. Environ Exp Bot 162:455–467Google Scholar
  33. 33.
    Haider MS, Kurjogi MM, Khalil-ur-Rehman M, Pervez T, Songtao J, Fiaz M et al (2018) Drought stress revealed physiological, biochemical and gene-expressional variations in ‘Yoshihime’peach (Prunus Persica L.) cultivar. J Plant Interact 13(1):83–90Google Scholar
  34. 34.
    Hamilton ES, Jensen GS, Maksaev G, Katims A, Sherp AM, Haswell ES (2015) Mechanosensitive channel MSL8 regulates osmotic forces during pollen hydration and germination. Science 350(6259):438–441PubMedPubMedCentralGoogle Scholar
  35. 35.
    Hanson J, Smeekens S (2009) Sugar perception and signaling—an update. Curr Opin Plant Biol 12(5):562–567PubMedPubMedCentralGoogle Scholar
  36. 36.
    Hegnauer R (1988) Biochemistry, distribution and taxonomic relevance of higher plant alkaloids. Phytochemistry 27(8):2423–2427Google Scholar
  37. 37.
    Hossain Z, López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2009) Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J Plant Physiol 166(13):1391–1404PubMedGoogle Scholar
  38. 38.
    Hou Q, Ufer G, Bartels D (2016) Lipid signalling in plant responses to abiotic stress. Plant Cell Environ 39(5):1029–1048PubMedGoogle Scholar
  39. 39.
    Hu CA, Delauney AJ, Verma DP (1992) A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci 89(19):9354–9358PubMedGoogle Scholar
  40. 40.
    Isah T (2019) Stress and defense responses in plant secondary metabolites production. Biol Res 52(1):39PubMedPubMedCentralGoogle Scholar
  41. 41.
    Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50(10):1223–1229PubMedGoogle Scholar
  42. 42.
    Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation–what is important for metabolic adjustment? Plant Biol 12(3):395–405PubMedGoogle Scholar
  43. 43.
    Jochum GM, Mudge KW, Thomas RB (2007) Elevated temperatures increase leaf senescence and root secondary metabolite concentrations in the understory herb Panax quinquefolius (Araliaceae). Am J Bot 94(5):819–826PubMedGoogle Scholar
  44. 44.
    Johnson HE, Broadhurst D, Goodacre R, Smith AR (2003) Metabolic fingerprinting of salt-stressed tomatoes. Phytochemistry 62(6):919–928PubMedGoogle Scholar
  45. 45.
    Katz E, Nisani S, Yadav BS, Woldemariam MG, Shai B, Obolski U et al (2015) The glucosinolate breakdown product indole-3-carbinol acts as an auxin antagonist in roots of Arabidopsis thaliana. Plant J 82(4):547–555PubMedGoogle Scholar
  46. 46.
    Kavi Kishor PB, Hong Z, Miao GH, Hu CA, Verma DPS (1995) 2161781. Overexpression of delta 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108(4):1387–1394Google Scholar
  47. 47.
    Kirakosyan A, Kaufman P, Warber S, Zick S, Aaronson K, Bolling S, Chul Chang S (2004) Applied environmental stresses to enhance the levels of polyphenolics in leaves of hawthorn plants. Physiol Plant 121(2):182–186PubMedGoogle Scholar
  48. 48.
    Kishor K, Polavarapu B, Hima Kumari P, Sunita MSL, Sreenivasulu N (2015) Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Front Plant Sci 6:544Google Scholar
  49. 49.
    Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3(1):224–235PubMedGoogle Scholar
  50. 50.
    Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63(4):1593–1608PubMedPubMedCentralGoogle Scholar
  51. 51.
    Kumar SV, Wigge PA (2010) H2A. Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140(1):136–147PubMedGoogle Scholar
  52. 52.
    Kurutas EB (2015) The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: current state. Nutr J 15(1):71Google Scholar
  53. 53.
    Lattanzio V (2013) Phenolic compounds: introduction. Natural products. Springer, Berlin, pp 1543–1580Google Scholar
  54. 54.
    Lattanzio V, Kroon PA, Quideau S, Treutter D (2008) Plant phenolics—secondary metabolites with diverse functions. Recent Adv Polyphen Res 1:1–35Google Scholar
  55. 55.
    Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14(6):1235–1251PubMedPubMedCentralGoogle Scholar
  56. 56.
    Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C (2015) Cell wall metabolism in response to abiotic stress. Plants 4(1):112–166PubMedPubMedCentralGoogle Scholar
  57. 57.
    Lehfeldt C, Shirley AM, Meyer K, Ruegger MO, Cusumano JC, Viitanen PV et al (2000) Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell 12(8):1295–1306PubMedPubMedCentralGoogle Scholar
  58. 58.
    Lin D, Xiao M, Zhao J, Li Z, Xing B, Li X et al (2016) An overview of plant phenolic compounds and their importance in human nutrition and management of type 2 diabetes. Molecules 21(10):1374PubMedCentralGoogle Scholar
  59. 59.
    Liu JX, Howell SH (2016) Managing the protein folding demands in the endoplasmic reticulum of plants. New Phytol 211(2):418–428PubMedGoogle Scholar
  60. 60.
    Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D et al (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221PubMedGoogle Scholar
  61. 61.
    Marschner H (1995) The soil root interface (rhizosphere) in relation to mineral nutrition. In: Mineral nutrition of higher plants. Academic Press, CambridgeGoogle Scholar
  62. 62.
    Mignolet-Spruyt L, Xu E, Idänheimo N, Hoeberichts FA, Mühlenbock P, Brosché M et al (2016) Spreading the news: subcellular and organellar reactive oxygen species production and signalling. J Exp Bot 67(13):3831–3844PubMedGoogle Scholar
  63. 63.
    Molinari HBC, Marur CJ, Bespalhok Filho JC, Kobayashi AK, Pileggi M, Júnior RPL et al (2004) Osmotic adjustment in transgenic citrus rootstock Carrizo citrange (Citrus sinensis Osb × Poncirus trifoliata L. Raf.) overproducing proline. Plant Sci 167(6):1375–1381Google Scholar
  64. 64.
    Morison JIL, Lawlor DW (1999) Interactions between increasing CO2 concentration and temperature on plant growth. Plant Cell Environ 22(6):659–682Google Scholar
  65. 65.
    Morkunas I, Woźniak A, Mai VC, Rucińska-Sobkowiak R, Jeandet P (2018) The role of heavy metals in plant response to biotic stress. Molecules 23(9):2320PubMedCentralGoogle Scholar
  66. 66.
    Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681Google Scholar
  67. 67.
    Narayan MS, Thimmaraju R, Bhagyalakshmi N (2005) Interplay of growth regulators during solid-state and liquid-state batch cultivation of anthocyanin producing cell line of Daucus carota. Process Biochem 40(1):351–358Google Scholar
  68. 68.
    Ng S, De Clercq I, Van Aken O, Law SR, Ivanova A, Willems P et al (2014) Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Mol Plant 7(7):1075–1093PubMedGoogle Scholar
  69. 69.
    Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147(3):1251–1263PubMedPubMedCentralGoogle Scholar
  70. 70.
    Norén L, Kindgren P, Stachula P, Rühl M, Eriksson ME, Hurry V, Strand Å (2016) Circadian and plastid signaling pathways are integrated to ensure correct expression of the CBF and COR genes during photoperiodic growth. Plant Physiol 171(2):1392–1406PubMedPubMedCentralGoogle Scholar
  71. 71.
    Obrenović S (1990) Effect of Cu(II) smallcap˜ D-penicillamine on phytochrome-mediated betacyanin formation in Amaranthus caudatus seedlings. Plant Physiol Biochem (Paris) 28(5):639–646Google Scholar
  72. 72.
    Ochoa-Velasco CE, Avila-Sosa R, Navarro-Cruz AR, López-Malo A, Palou E (2017) Biotic and abiotic factors to increase bioactive compounds in fruits and vegetables. Food bioconversion. Academic Press, Cambridge, pp 317–349Google Scholar
  73. 73.
    Pedranzani H, Racagni G, Alemano S, Miersch O, Ramírez I, Peña-Cortés H et al (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41(2):149–158Google Scholar
  74. 74.
    Piasecka A, Kachlicki P, Stobiecki M (2019) Analytical methods for detection of plant metabolomes changes in response to biotic and abiotic stresses. Int J Mol Sci 20(2):379PubMedCentralGoogle Scholar
  75. 75.
    Pitta-Alvarez SI, Spollansky TC, Giulietti AM (2000) The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzyme Microb Technol 26(2–4):252–258PubMedGoogle Scholar
  76. 76.
    Sangwan V, Örvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31(5):629–638PubMedGoogle Scholar
  77. 77.
    Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim Biophys Acta (BBA) 1819(2):104–119Google Scholar
  78. 78.
    Scholz M, Gatzek S, Sterling A, Fiehn O, Selbig J (2004) Metabolite fingerprinting: detecting biological features by independent component analysis. Bioinformatics 20(15):2447–2454PubMedGoogle Scholar
  79. 79.
    Seneviratne M, Rajakaruna N, Rizwan M, Madawala HMSP, Ok YS, Vithanage M (2019) Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review. Environ Geochem Health 41(4):1813–1831PubMedGoogle Scholar
  80. 80.
    Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT (2004) Root growth maintenance during water deficits: physiology to functional genomics. J Exp Bot 55(407):2343–2351PubMedGoogle Scholar
  81. 81.
    Shiozaki N, Hattori I, Gojo R, Tezuka T (1999) Activation of growth and nodulation in a symbiotic system between pea plants and leguminous bacteria by near-UV radiation. J Photochem Photobiol B 50(1):33–37Google Scholar
  82. 82.
    Sicher RC, Timlin D, Bailey B (2012) Responses of growth and primary metabolism of water-stressed barley roots to rehydration. J Plant Physiol 169(7):686–695PubMedGoogle Scholar
  83. 83.
    Singh AK (2017) Discovery and role of molecular markers involved in gene mapping, molecular breeding, and genetic diversity. Plant bioinformatics. Springer, Cham, pp 303–328Google Scholar
  84. 84.
    Singh AK, Chamovitz DA (2019) Role of Cop9 Signalosome subunits in the environmental and hormonal balance of plant. Biomolecules 9(6):224PubMedCentralGoogle Scholar
  85. 85.
    Singh S, Sinha S (2005) Accumulation of metals and its effects in Brassica juncea (L.) Czern (cv. Rohini) grown on various amendments of tannery waste. Ecotoxicol Environ Saf 62(1):118–127PubMedGoogle Scholar
  86. 86.
    Sheflin AM, Chiniquy D, Yuan C, Goren E, Kumar I, Braud M et al (2019) Metabolomics of sorghum roots during nitrogen stress reveals compromised metabolic capacity for salicylic acid biosynthesis. Plant Direct 3(3):e00122PubMedPubMedCentralGoogle Scholar
  87. 87.
    Slama I, Abdelly C, Bouchereau A, Flowers T, Savoure A (2015) Diversity, distribution and roles of osmoprotective compounds accumulated in halophytes under abiotic stress. Ann Bot 115(3):433–447PubMedPubMedCentralGoogle Scholar
  88. 88.
    Slocum RD, Kaur-Sawhney R, Galston AW (1984) The physiology and biochemistry of polyamines in plants. Arch Biochem Biophys 235(2):283–303PubMedGoogle Scholar
  89. 89.
    Solíz-Guerrero JB, De Rodriguez DJ, Rodríguez-García R, Angulo-Sánchez JL, Méndez-Padilla G (2002) Quinoa saponins: concentration and composition analysis. In: Janick J, Whipkey A (eds) Trends in new crops and new uses. ASHS Press, Alexandria, pp 110–114Google Scholar
  90. 90.
    Somssich M, Khan GA, Persson S (2016) Cell wall heterogeneity in root development of Arabidopsis. Front Plant Sci 7:1242PubMedPubMedCentralGoogle Scholar
  91. 91.
    Steinfath M, Strehmel N, Peters R, Schauer N, Groth D, Hummel J et al (2010) Discovering plant metabolic biomarkers for phenotype prediction using an untargeted approach. Plant Biotechnol J 8(8):900–911PubMedGoogle Scholar
  92. 92.
    Swarbreck S, Colaço R, Davies J (2013) Plant calcium-permeable channels. Plant Physiol 163:113Google Scholar
  93. 93.
    Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97Google Scholar
  94. 94.
    Tan DX, Manchester L, Esteban-Zubero E, Zhou Z, Reiter R (2015) Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules 20(10):18886–18906PubMedPubMedCentralGoogle Scholar
  95. 95.
    Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX, Luan S (2015) Tonoplast CBL–CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad Sci 112(10):3134–3139PubMedGoogle Scholar
  96. 96.
    Tegelberg R, Julkunen-Tiitto R, Aphalo PJ (2004) Red: far-red light ratio and UV-B radiation: their effects on leaf phenolics and growth of silver birch seedlings. Plant Cell Environ 27(8):1005–1013Google Scholar
  97. 97.
    Tanase C, Coșarcă S, Muntean DL (2019) A critical review of phenolic compounds extracted from the bark of woody vascular plants and their potential biological activity. Molecules 24(6):1182PubMedCentralGoogle Scholar
  98. 98.
    Tenhaken R (2015) Cell wall remodeling under abiotic stress. Front Plant Sci 5:771PubMedPubMedCentralGoogle Scholar
  99. 99.
    Trejo-Tapia G, Jimenez-Aparicio A, Rodriguez-Monroy M, De Jesus-Sanchez A, Gutierrez-Lopez G (2001) Influence of cobalt and other microelements on the production of betalains and the growth of suspension cultures of Beta vulgaris. Plant Cell Tissue Organ Cult 67(1):19–23Google Scholar
  100. 100.
    Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47(3):346–354PubMedGoogle Scholar
  101. 101.
    Verslues PE, Juenger TE (2011) Drought, metabolites, and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments. Curr Opin Plant Biol 14(3):240–245PubMedGoogle Scholar
  102. 102.
    Visser EJ, Voesenek LA (2005) Acclimation to soil flooding—sensing and signal-transduction. Root physiology: from gene to function. Springer, Dordrecht, pp 197–214Google Scholar
  103. 103.
    Wagner D, Przybyla D, op den Camp R, Kim C, Landgraf F, Lee KP et al (2004) The genetic basis of singlet oxygen–induced stress responses of Arabidopsis thaliana. Science 306(5699):1183–1185PubMedGoogle Scholar
  104. 104.
    Weinstein LH, Kaur-Sawhney R, Rajam MV, Wettlaufer SH, Galston AW (1986) Cadmium-induced accumulation of putrescine in oat and bean leaves. Plant Physiol 82(3):641–645PubMedPubMedCentralGoogle Scholar
  105. 105.
    Witt S, Galicia L, Lisec J, Cairns J, Tiessen A, Araus JL et al (2012) Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Mol Plant 5(2):401–417PubMedGoogle Scholar
  106. 106.
    Yadav BS, Lahav T, Reuveni E, Chamovitz DA, Freilich S (2016) Multidimensional patterns of metabolic response in abiotic stress-induced growth of Arabidopsis thaliana. Plant Mol Biol 92(6):689–699PubMedGoogle Scholar
  107. 107.
    Yadav BS, Singh AK, Kushwaha SK (2017) Systems-based approach to the analyses of plant functions: conceptual understanding, implementation, and analysis. Plant Bioinform. Springer, Cham, pp 107–133Google Scholar
  108. 108.
    Yang L, Wen KS, Ruan X, Zhao YX, Wei F, Wang Q (2018) Response of plant secondary metabolites to environmental factors. Molecules 23(4):762PubMedCentralGoogle Scholar
  109. 109.
    Ye Y, Ding Y, Jiang Q, Wang F, Sun J, Zhu C (2017) The role of receptor-like protein kinases (RLKs) in abiotic stress response in plants. Plant Cell Rep 36(2):235–242PubMedGoogle Scholar
  110. 110.
    Yu J, Li R, Fan N, Yang Z, Huang B (2017) Metabolic pathways involved in carbon dioxide enhanced heat tolerance in Bermudagrass. Front Plant Sci 8:1506PubMedPubMedCentralGoogle Scholar
  111. 111.
    Yuan F, Yang H, Xue Y, Kong D, Ye R, Li C et al (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514(7522):367PubMedGoogle Scholar
  112. 112.
    Yuan P, Yang T, Poovaiah BW (2018) Calcium signaling-mediated plant response to cold stress. Int J Mol Sci 19(12):3896PubMedCentralGoogle Scholar
  113. 113.
    Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124(3):941–948PubMedPubMedCentralGoogle Scholar
  114. 114.
    Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53(1):247–273PubMedPubMedCentralGoogle Scholar
  115. 115.
    Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324PubMedPubMedCentralGoogle Scholar
  116. 116.
    Zhu J, Lee BH, Dellinger M, Cui X, Zhang C, Wu S et al (2010) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J 63(1):128–140PubMedPubMedCentralGoogle Scholar
  117. 117.
    Zhou H, Lin H, Chen S, Becker K, Yang Y, Zhao J, Guo Y (2014) Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell 26:1166–1182PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Molecular Biology and Ecology of PlantsTel Aviv UniversityTel AvivIsrael
  2. 2.Department of BioengineeringUniversity of Information Science and Technology (UIST) St. Paul the ApostleOhridRepublic of North Macedonia

Personalised recommendations