pp 1–17 | Cite as

Methylobacterium oryzae CBMB20 influences photosynthetic traits, volatile emission and ethylene metabolism in Oryza sativa genotypes grown in salt stress conditions

  • Poulami Chatterjee
  • Arooran Kanagendran
  • Sandipan Samaddar
  • Leila Pazouki
  • Tong-Min SaEmail author
  • Ülo NiinemetsEmail author
Original Article


Main conclusion

Inoculation of endophytic Methylobacterium oryzae CBMB20 in salt-stressed rice plants improves photosynthesis and reduces stress volatile emissions due to mellowing of ethylene-dependent responses and activating vacuolar H+-ATPase.


The objective of this study was to analyze the impact of ACC (1-aminocyclopropane-1-carboxylate) deaminase-producing Methylobacterium oryzae CBMB20 in acclimation of plant to salt stress by controlling photosynthetic characteristics and volatile emission in salt-sensitive (IR29) and moderately salt-resistant (FL478) rice (Oryza sativa L.) cultivars. Saline levels of 50 mM and 100 mM NaCl with and without bacteria inoculation were applied, and the temporal changes in stress response and salinity resistance were assessed by monitoring photosynthetic characteristics, ACC accumulation, ACC oxidase activity (ACO), vacuolar H+ ATPase activity, and volatile organic compound (VOC) emissions. Salt stress considerably reduced photosynthetic rate, stomatal conductance, PSII efficiency and vacuolar H+ ATPase activity, but it increased ACC accumulation, ACO activity, green leaf volatiles, mono- and sesquiterpenes, and other stress volatiles. These responses were enhanced with increasing salt stress and time. However, rice cultivars treated with CBMB20 showed improved plant vacuolar H+ ATPase activity, photosynthetic characteristics and decreased ACC accumulation, ACO activity and VOC emission. The bacteria-dependent changes were greater in the IR29 cultivar. These results indicate that decreasing photosynthesis and vacuolar H+ ATPase activity rates and increasing VOC emission rates in response to high-salinity stress were effectively mitigated by M. oryzae CBMB20 inoculation.


ACC deaminase ACC oxidase Fv/Fm Salt stress Vacuolar H+ ATPase VOC 



Green leaf volatiles


Volatile organic compounds


ACC (1-aminocyclopropane-1-carboxylate) oxidase


Geranyl-geranyl diphosphate pathway


Oxygenated volatile organic compounds



This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (2015R1A2A1A05001885) and Grants from the European Commission through the European Research Council (advanced grant 322603, SIP-VOL+), and the European Regional Development Fund (Centre of Excellence EcolChange) and the Estonian Ministry of Science and Education (institutional grant IUT-8-3).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

425_2019_3139_MOESM1_ESM.docx (60 kb)
Supplementary material 1 (DOCX 60 kb)


  1. Abogadallah GM (2010) Insights into the significance of antioxidative defense under salt stress. Plant Signal Behav 5:369–374. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15:664–674. CrossRefPubMedGoogle Scholar
  3. Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J Plant Physiol 164:685–694. CrossRefPubMedGoogle Scholar
  4. Arimura GI, Ozawa R, Nishioka T, Boland W, Koch T, Kühnemann F, Takabayashi J (2002) Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J 29:87–98. CrossRefPubMedGoogle Scholar
  5. Arimura GI, Garms S, Maffei M, Bossi S, Schulze B, Leitner M, Mithöfer A, Boland W (2008) Herbivore-induced terpenoid emission in Medicago truncatula: concerted action of jasmonate, ethylene and calcium signaling. Planta 227:453–464. CrossRefPubMedGoogle Scholar
  6. Arisz SA, Munnik T (2011) The salt stress-induced LPA response in Chlamydomonas is produced via PLA2 hydrolysis of DGK-generated phosphatidic acid. J Lipid Res 52:2012–2020. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ashraf MPJC, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16. CrossRefGoogle Scholar
  8. Bongi G, Loreto F (1989) Gas-exchange properties of salt-stressed olive (Olea europea L.) leaves. Plant Physiol 90:1408–1416. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Borghesi E, González-Miret ML, Escudero-Gilete ML, Malorgio F, Heredia FJ, Meléndez-Martínez AJ (2011) Effects of salinity stress on carotenoids, anthocyanins, and color of diverse tomato genotypes. J Agric Food Chem 59:11676–11682. CrossRefPubMedGoogle Scholar
  10. Bracho-Nunez A, Welter S, Staudt M, Kesselmeier J (2011) Plant-specific volatile organic compound emission rates from young and mature leaves of Mediterranean vegetation. J Geophys Res: Atmos 116(D16)Google Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. CrossRefPubMedGoogle Scholar
  12. Carystinos GD, MacDonald HR, Monroy AF, Dhindsa RS, Poole RJ (1995) Vacuolar H+-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol 108:641–649. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cellini A, Buriani G, Rocchi L, Rondelli E, Savioli S, Rodriguez Estrada MT, Cristescu SM, Costa G, Spinelli F (2018) Biological relevance of volatile organic compounds emitted during the pathogenic interactions between apple plants and Erwinia amylovora. Mol Plant Pathol 19:158–168. CrossRefPubMedGoogle Scholar
  14. Chatterjee P, Samaddar S, Anandham R, Kang Y, Kim K, Selvakumar G, Sa T (2017) Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front Plant Sci 8:705. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chatterjee P, Samaddar S, Niinemets Ü, Sa T (2018) Brevibacterium linens RS16 confers salt tolerance to Oryza sativa genotypes by regulating antioxidant defense and H+ ATPase activity. Microbiol Res 215:89–101. CrossRefPubMedGoogle Scholar
  16. Chen YH, Lu CW, Shyu YT, Lin SS (2017) Revealing the saline adaptation strategies of the halophilic bacterium Halomonas beimenensis through high-throughput omics and transposon mutagenesis approaches. Sci Rep 7:13037. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Copolovici L, Niinemets Ü (2010) Flooding induced emissions of volatile signalling compounds in three tree species with differing waterlogging tolerance. Plant Cell Environ 33:1582–1594. PubMedGoogle Scholar
  18. Copolovici L, Kännaste A, Remmel T, Vislap V, Niinemets Ü (2011) Volatile emissions from Alnus glutionosa induced by herbivory are quantitatively related to the extent of damage. J Chem Ecol 37:18–28. CrossRefPubMedGoogle Scholar
  19. Dabbous A, Saad RB, Brini F, Farhat-Khemekhem A, Zorrig W, Abdely C, Hamed KB (2017) Over-expression of a subunit E1 of a vacuolar H+-ATPase gene (Lm VHA-E1) cloned from the halophyte Lobularia maritima improves the tolerance of Arabidopsis thaliana to salt and osmotic stresses. Environ Exp Bot 137:128–141. CrossRefGoogle Scholar
  20. Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dettmer J, Hong-Hermesdorf A, Stierhof YD, Schumacher K (2006) Vacuolar H+-ATPase activity is required for endocytic and secretory trafficking in Arabidopsis. Plant Cell 18:715–730. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Eida AA, Alzubaidy HS, de Zélicourt A, Synek L, Alsharif W, Lafi FF, Hirt H, Saad MM (2019) Phylogenetically diverse endophytic bacteria from desert plants induce transcriptional changes of tissue-specific ion transporters and salinity stress in Arabidopsis thaliana. Plant Sci 280:228–240CrossRefPubMedGoogle Scholar
  23. Esitken A, Yildiz HE, Ercisli S, Donmez MF, Turan M, Gunes A (2010) Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci Hortic 124:62–66. CrossRefGoogle Scholar
  24. Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297. CrossRefPubMedGoogle Scholar
  25. Gholizadeh A (2012) Molecular evidence for the contribution of methylobacteria to the pink-pigmentation process in pink-colored plants. J Plant Interact 7:316–321. CrossRefGoogle Scholar
  26. Ghosh S, Bagchi S, Majumder AL (2001) Chloroplast fructose-1, 6-bisphosphatase from Oryza differs in salt tolerance property from the Porteresia enzyme and is protected by osmolytes. Plant Sci 160:1171–1181. CrossRefPubMedGoogle Scholar
  27. Gronwald JW, Suhayda CG, Tal M, Shannon MC (1990) Reduction in plasma membrane ATPase activity of tomato roots by salt stress. Plant Sci 66:145–153. CrossRefGoogle Scholar
  28. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics. PubMedPubMedCentralGoogle Scholar
  29. Hinge VR, Patil HB, Nadaf AB (2016) Aroma volatile analyses and 2AP characterization at various developmental stages in basmati and non-basmati scented rice (Oryza sativa L.) cultivars. Rice 9:38. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hu ZH, Shen YB, Su XH (2009) Saturated aldehydes C6–C10 emitted from ashleaf maple (Acer negundo L.) leaves at different levels of light intensity, O2, and CO2. J Plant Biol 52:289–297. CrossRefGoogle Scholar
  31. Ivushkin K, Bartholomeus H, Bregt AK, Pulatov A, Bui EN, Wilford J (2018) Soil salinity assessment through satellite thermography for different irrigated and rainfed crops. Int J Appl Earth Obs Geoinf 68:230–237. CrossRefGoogle Scholar
  32. Jiang Y, Ye J, Li S, Niinemets Ü (2017) Methyl jasmonate-induced emission of biogenic volatiles is biphasic in cucumber: a high-resolution analysis of dose dependence. J Exp Bot 68:4679–4694. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Kalaji HM, Bosa K, Kościelniak J, Żuk-Gołaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exper Bot 73:64–72. CrossRefGoogle Scholar
  34. Kanagendran A, Pazouki L, Li S, Liu B, Kännaste A, Niinemets Ü (2017) Ozone-triggered surface uptake and stress volatile emissions in Nicotiana tabacum ‘Wisconsin’. J Exp Bot 69:681–697. CrossRefPubMedCentralGoogle Scholar
  35. Kanagendran A, Pazouki L, Niinemets Ü (2018) Differential regulation of volatile emission from Eucalyptus globulus leaves upon single and combined ozone and wounding treatments through recovery and relationships with ozone uptake. Environ Exp Bot 145:21–38. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kännaste A, Copolovici L, Niinemets Ü (2014) Gas chromatography mass spectrometry method for determination of biogenic volatile organic compounds emitted by plants. In: Rodríguez-Concepción M (ed) Plant isoprenoids: methods and protocols, methods in molecular biology. Humana Press, New York, pp 161–169. CrossRefGoogle Scholar
  37. Karl T, Guenther A, Spirig C, Hansel A, Fall R (2003) Seasonal variation of biogenic VOC emissions above a mixed hardwood forest in northern Michigan. Geophys Res Lett 30(23)Google Scholar
  38. Kask K, Kännaste A, Talt E, Copolovici L, Niinemets Ü (2016) How specialized volatiles respond to chronic and short-term physiological and shock heat stress in Brassica nigra. Plant Cell Environ 39:2027–2042. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kim K, Yim W, Trivedi P, Madhaiyan M, Boruah HPD, Islam MR, Lee G, Sa T (2010) Synergistic effects of inoculating arbuscular mycorrhizal fungi and Methylobacterium oryzae strains on growth and nutrient uptake of red pepper (Capsicum annuum L.). Plant Soil 327:429–440. CrossRefGoogle Scholar
  40. Kim HS, Ji CY, Lee CJ, Kim SE, Park SC, Kwak SS (2018) Orange: a target gene for regulating carotenoid homeostasis and increasing plant tolerance to environmental stress in marginal lands. J Exp Bot 69:3393–3400. CrossRefPubMedGoogle Scholar
  41. Kwak MJ, Jeong H, Madhaiyan M, Lee Y, Sa TM, Oh TK, Kim JF (2014) Genome information of Methylobacterium oryzae, a plant-probiotic methylotroph in the phyllosphere. PLoS One 9:p.e106704. CrossRefGoogle Scholar
  42. Lee HS, Madhaiyan M, Kim CW, Choi SJ, Chung KY, Sa T (2006) Physiological enhancement of early growth of rice seedlings (Oryza sativa L.) by production of phytohormone of N2-fixing methylotrophic isolates. Biol Fertil Soils 42:402–408. CrossRefGoogle Scholar
  43. Lee M, Chauhan PS, Yim W, Lee G, Kim YS, Park K, Sa T (2011) Foliar colonization and growth promotion of red pepper (Capsicum annuum L.) by Methylobacterium oryzae CBMB20. J Appl Biol Chem 54:120–125. CrossRefGoogle Scholar
  44. Lizada MCC, Yang SF (1979) A simple and sensitive assay for 1-aminocyclopropane-l-carboxylic acid. Anal Biochem 100:140–145CrossRefPubMedGoogle Scholar
  45. Loreto F, Förster A, Dürr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant, Cell Environ 21:101–107. CrossRefGoogle Scholar
  46. Low R, Rockel B, Kirsch M, Ratajczak R, Hortensteiner S, Martinoia E, Luttge U, Rausch T (1996) Early salt stress effects on the differential expression of vacuolar H+-ATPase genes in roots and leaves of Mesembryanthemum crystallinum. Plant Physiol 110:259–265. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lu Y, Wang X, Lou Y, Cheng J (2006) Role of ethylene signaling in the production of rice volatiles induced by the rice brown planthopper Nilaparvata lugens. Chin Sci Bull 51:2457–2465. CrossRefGoogle Scholar
  48. Madhaiyan M, Reddy BS, Anandham R, Senthilkumar M, Poonguzhali S, Sundaram SP, Sa T (2006a) Plant growth-promoting Methylobacterium induces defense responses in groundnut (Arachis hypogaea L.) compared with rot pathogens. Curr Microbiol 53:270–276. CrossRefPubMedGoogle Scholar
  49. Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006b) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278CrossRefPubMedGoogle Scholar
  50. Madhaiyan M, Kim BY, Poonguzhali S, Kwon SW, Song MH, Ryu JH, Go SJ, Koo BS, Sa T (2007a) Methylobacterium oryzae sp. nov., an aerobic, pink-pigmented, facultatively methylotrophic, 1-aminocyclopropane-1-carboxylate deaminase-producing bacterium isolated from rice. Int J Syst Evol Microbiol 57:326–331. CrossRefPubMedGoogle Scholar
  51. Madhaiyan M, Poonguzhali S, Sa T (2007b) Characterization of 1-aminocyclopropane-1-carboxylate (ACC) deaminase containing Methylobacterium oryzae and interactions with auxins and ACC regulation of ethylene in canola (Brassica campestris). Planta 226:867–876. CrossRefPubMedGoogle Scholar
  52. Madhaiyan M, Poonguzhali S, Kang BG, Lee YJ, Chung JB, Sa T (2010) Effect of co-inoculation of methylotrophic Methylobacterium oryzae with Azospirillum brasilense and Burkholderia pyrrocinia on the growth and nutrient uptake of tomato, red pepper and rice. Plant Soil 328:71–82. CrossRefGoogle Scholar
  53. Mano JI, Miyatake F, Hiraoka E, Tamoi M (2009) Evaluation of the toxicity of stress-related aldehydes to photosynthesis in chloroplasts. Planta 230:639–648. CrossRefPubMedGoogle Scholar
  54. Matsui K, Kurishita S, Hisamitsu A, Kajiwara T (2000) A lipid-hydrolysing activity involved in hexenal formation. Biochem Soc Trans 28: 857–860.
  55. Matsuoka H, Ohwaki Y, Terakado-Tonooka J, Tanaka F (2016) Changes in volatiles in carrots inoculated with ACC deaminase-producing bacteria isolated from organic crops. Plant Soil 407:173–186. CrossRefGoogle Scholar
  56. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572. CrossRefPubMedGoogle Scholar
  57. Mostofa MG, Hossain MA, Fujita M (2015) Trehalose pretreatment induces salt tolerance in rice (Oryza sativa L.) seedlings: oxidative damage and co-induction of antioxidant defense and glyoxalase systems. Protoplasma 252:461–475. CrossRefPubMedGoogle Scholar
  58. Niinemets Ü (2010) Mild versus severe stress and BVOCs: thresholds, priming and consequences. Trends Plant Sci 15:145–153. CrossRefPubMedGoogle Scholar
  59. Niinemets Ü, Hauff K, Bertin N, Tenhunen JD, Steinbrecher R, Seufert G (2002) Monoterpene emissions in relation to foliar photosynthetic and structural variables in Mediterranean evergreen Quercus species. New Phytol 153:243–256. CrossRefGoogle Scholar
  60. Niinemets Ü, Kuhn U, Harley PC, Staudt M, Arneth A, Cescatti A, Ciccioli P, Copolovici L, Geron C, Guenther A et al (2011) Estimations of isoprenoid emission capacity from enclosure studies: measurements, data processing, quality and standardized measurement protocols. Biogeosciences 8:2209–2246CrossRefGoogle Scholar
  61. Pazouki L, Niinemets Ü (2016) Multi-substrate terpene synthases: their occurrence and physiological significance. Front Plant Sci 7:1019. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Pazouki L, Kanagendran A, Li S, Kännaste A, Rajabi Memari H, Bichele R, Niinemets Ü (2016) Mono- and sesquiterpene release from tomato (Solanum lycopersicum) leaves upon mild and severe heat stress and through recovery: from gene expression to emission responses. Environ Exp Bot 132:1–15. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pichersky E, Noel JP, Dudareva N (2006) Biosynthesis of plant volatiles: nature’s diversity and ingenuity. Science 311:808–811. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Portillo-Estrada M, Kazantsev T, Talts E, Tosens T, Niinemets Ü (2015) Emission timetable and quantitative patterns of wound-induced volatiles across different leaf damage treatments in aspen (Populus tremula). J Chem Ecol 41:1105–1117. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Ranjbarfordoei A, Samson R, Van Damme P (2006) Chlorophyll fluorescence performance of sweet almond [Prunus dulcis (Miller) D. Webb] in response to salinity stress induced by NaCl. Photosynthetica 44:513–522CrossRefGoogle Scholar
  66. Ruther J, Kleier S (2005) Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222. CrossRefPubMedGoogle Scholar
  67. Samaddar S, Chatterjee P, Choudhury AR, Ahmed S, Sa T (2019) Interactions between Pseudomonas spp. and their role in improving the red pepper plant growth under salinity stress. Microbiol Res 219:66–73. CrossRefPubMedGoogle Scholar
  68. Schuurink RC, Haring MA, Clark DG (2006) Regulation of volatile benzenoid biosynthesis in petunia flowers. Trends Plant Sci 11:20–25. CrossRefPubMedGoogle Scholar
  69. Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. Plant J 54:712–732. CrossRefPubMedGoogle Scholar
  70. Seck PA, Diagne A, Mohanty S, Wopereis MCS (2012) Crops that feed the world 7: rice. Food Secur 4:7–24. CrossRefGoogle Scholar
  71. Seemann JR, Christa C (1985) Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164(2):151–162CrossRefPubMedGoogle Scholar
  72. Sheng M, Tang M, Chen H, Yang B, Zhang F, Huang Y (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18:287–296CrossRefPubMedGoogle Scholar
  73. Siddikee MA, Glick BR, Chauhan PS, Yim WJ, Sa T (2011) Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol Biochem 49:427–434. CrossRefPubMedGoogle Scholar
  74. Soontharapirakkul K, Incharoensakdi A (2010) Na+-stimulated ATPase of alkaliphilic halotolerant cyanobacterium Aphanothece halophytica translocates Na+ into proteoliposomes via Na+ uniport mechanism. BMC Boichem 11:30. CrossRefGoogle Scholar
  75. Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486. CrossRefGoogle Scholar
  76. Sultana N, Ikeda T, Kashem MA (2001) Effect of foliar spray of nutrient solutions on photosynthesis, dry matter accumulation and yield in seawater-stressed rice. Environ Exp Bot 46:129–140. CrossRefGoogle Scholar
  77. Timmusk S, El-Daim IAA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets Ü (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PloS One 9:p.e96086. CrossRefGoogle Scholar
  78. Tomescu D, Şumălan R, Copolovici L, Copolovici D (2017) The influence of soil salinity on volatile organic compounds emission and photosynthetic parameters of Solanum lycopersicum L. varieties. Open Life Sci 12:135–142. Google Scholar
  79. von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387. CrossRefGoogle Scholar
  80. Wang W, Scali M, Vignani R, Spadafora A, Sensi E, Mazzuca S, Cresti M (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24:2369–2375. CrossRefPubMedGoogle Scholar
  81. Wang Q, Dodd IC, Belimov AA, Jiang F (2016) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Func Plant Biol 43:161–172CrossRefGoogle Scholar
  82. Wei T, Simko V (2013) corrplot: Visualization of a correlation matrix. R package version 0.73. 230:11Google Scholar
  83. Wildt J, Kobel K, Schuh-Thomas G, Heiden AC (2003) Emissions of oxygenated volatile organic compounds from plants Part II: emissions of saturated aldehydes. J Atmos Chem 45:173. CrossRefGoogle Scholar
  84. Yeo AR, Flowers SA, Rao G, Welfare K, Senanayake N, Flowers TJ (1999) Silicon reduces sodium uptake in rice (Oryza sativa L.) in saline conditions and this is accounted for by a reduction in the transpirational bypass flow. Plant Cell Environ 22:559–565. CrossRefGoogle Scholar
  85. Yim W, Seshadri S, Kim K, Lee G, Sa T (2013) Ethylene emission and PR protein synthesis in ACC deaminase producing Methylobacterium spp. inoculated tomato plants (Lycopersicon esculentum Mill.) challenged with Ralstonia solanacearum under greenhouse conditions. Plant Physiol Biochem 67:95–104. CrossRefPubMedGoogle Scholar
  86. Zapata PJ, Serrano M, Pretel MT, Amoros A, Botella MA (2003) Changes in ethylene evolution and polyamine profiles of seedlings of nine cultivars of Lactuca sativa L. in response to salt stress during germination. Plant Sci 164:557–563. CrossRefGoogle Scholar
  87. Zhao N, Guan J, Ferrer JL, Engle N, Chern M, Ronald P, Tschaplinski TJ, Chen F (2010) Biosynthesis and emission of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol Biochem 48:279–287. CrossRefPubMedGoogle Scholar
  88. Zheng C, Jiang D, Liu F, Dai T, Jing Q, Cao W (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582CrossRefPubMedGoogle Scholar
  89. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445. CrossRefPubMedGoogle Scholar
  90. Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Environmental and Biological ChemistryChungbuk National UniversityCheongjuRepublic of Korea
  2. 2.Institute of Agricultural and Environmental Sciences, Estonian University of Life SciencesTartuEstonia
  3. 3.Department of BiologyUniversity of LouisvilleLouisvilleUSA
  4. 4.Estonian Academy of SciencesTallinnEstonia

Personalised recommendations