Skip to main content
Log in

Physiological and proteomic analysis in two wild tomato lines under waterlogging and high temperature stress

  • Original Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Tomato yields are reduced under waterlogging and high temperature stress condition. Ascorbic acid (ASA) was shown to be involved in tolerance to waterlogging and heat stresses in tomato. Among 44 wild tomato lines treated with waterlogging at 38 °C, L6138 (Solanum peruvianum) showed highest ASA, shoot growth, chlorophyll content and chlorophyll fluorescence in comparison to other tomato lines. Further leaf proteins in L6138 and L0994 under waterlogging at 38 °C for 72 h were analyzed by two-dimensional protein fractionation system. Different protein peaks were analyzed by comparative proteomic analysis and database searching. Fifty protein peaks expressed in response to stress treatment were identified, among which 27 proteins from L0994 and 17 proteins from L6138 were successfully sequenced. Differentially proteins expressed have major functions in protein structure maintenance, metabolism, secretion, translation, biosynthesis, signal transduction, degradation, and photosynthesis under stress. ASA might be played a role in tolerance to waterlogging and heat stress by maintaining RNA transcription, protein structure, and metabolism. In this study, we utilized a physiological and proteomic approach to discover the changes in protein expression profiles of tomatoes in response to heat and flood stresses.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ASA:

Ascorbic acid

PF2D:

Two dimensions liquid phase fractionation

References

  • Camejo D, Rodriguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcon JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol 162:281–289

    Article  PubMed  CAS  Google Scholar 

  • Camejo D, Jimenez A, Alarcon JJ, Torres W, Gomez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Funct Plant Biol 33:177–187

    Article  CAS  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang S-C, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. Proc Natl Acad Sci U S A 100:3525–3530

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cramer GR, Van Sluyter SC, Hopper DW, Pascovici D, Keighley T, Haynes PA (2013) Proteomic analysis indicates massive changes in metabolism prior to the inhibition of growth and photosynthesis of grapevine (Vitis vinifera L.) in response to water deficit. BMC Plant Biol 13:49–71

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia–is survival a balancing act? Trends Plant Sci 9:449–456

    Article  PubMed  CAS  Google Scholar 

  • Gautier H, Massot C, Stevens R, Serino S, Genard M (2009) Regulation of tomato fruit ascorbate content is more highly dependent on fruit irradiance than leaf irradiance. Ann Bot 103:495–504

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hemavathi UCP, Akula N, Young KE, Chun SC, Kim DH, Park SW (2010) Enhanced ascorbic acid accumulation in transgenic potato confers tolerance to various abiotic stresses. Biotechnol Lett 32:321–330

    Article  PubMed  CAS  Google Scholar 

  • Irar S, Brini F, Goday A, Masmoudi K, Pagès M (2010) Proteomic analysis of wheat embryos with 2-DE and liquid-phase chromatography (ProteomeLab PF-2D) - A wider perspective of the proteome. J Proteomics 73:1707–1721

    Article  PubMed  CAS  Google Scholar 

  • Komatsu S, Konishi H, Shen S, Yang G (2003) Rice proteomics: a step toward functional analysis of the rice genome. Mol Cell Proteomics 2:2–10

    Article  PubMed  CAS  Google Scholar 

  • Komatsu S, Kuji R, Nanjo Y, Hiraga S, Furukawa K (2012) Comprehensive analysis of endoplasmic reticulum-enriched fraction in root tips of soybean under flooding stress using proteomics techniques. J Proteomics 77:531–560

    Article  PubMed  CAS  Google Scholar 

  • Kurepa J, Wang S, Li Y, Smalle J (2009) Proteasome regulation, plant growth and stress tolerance. Plant Signal Behav 4:924–927

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kwon SY, Choi SM, Ahn YO, Lee HS, Lee HB, Park YM, Kwak SS (2003) Enhanced stress-tolerance of transgenic tobacco plants expressing a human dehydroascorbate reductase gene. J Plant Physiol 160:347–353

    Article  PubMed  CAS  Google Scholar 

  • Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159:75–85

    Article  PubMed  CAS  Google Scholar 

  • Lee HJ, Kang MJ, Lee EY, Cho SY, Kim H, Paik YK (2008) Application of apeptide-based PF2D plateform for quantitative proteomics in disease biomarker discovery. Proteomics 8:2371–3381

    Article  Google Scholar 

  • Li HY, Chang CS, Lu LS, Liu CA, Chan MT, Charng YY (2005) Over-expression of Arabidopsis thaliana heat shock factor gene (AtHsfA1b) enhances chilling tolerance in transgenic tomato. Bot Bull Acad Sinica 46:91

    Google Scholar 

  • Lin KH, Weng CC, Lo HF, Chen JT (2004) Study of the root antioxidative system of tomatoes and eggplants under waterlogged conditions. Plant Sci 167:355–365

    Article  CAS  Google Scholar 

  • Lin KH, Tsou CC, Hwang SY, Chen LF, Lo HF (2006) Paclobutrazol pre-treatment enhanced flooding tolerance of sweet potato. J Plant Physiol 163:750–760

    Article  PubMed  CAS  Google Scholar 

  • Lin KH, Kuo WS, Chiang CM, Hsiung TC, Chiang MC, Lo HF (2013) Study of sponge gourd ascorbate peroxidase and winter squash superoxide dismutase under respective flooding and chilling stresses. Sci Hortic 162:333–340

    Article  CAS  Google Scholar 

  • Ling Q, Huang W, Jarvis P (2011) Use of a SPAD-502 meter to measure leaf chlorophyll concentration in Arabidopsis thaliana. Photosynth Res 107:209–214

    Article  PubMed  CAS  Google Scholar 

  • Markus V, Lurie S, Bravdo B, Stevens MA, Rudich J (1981) High temperature effects on RuBP earboxylase and carbonic anhydrase activity in two tomato cultivars. Physiol Plant 53:407–412

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  PubMed  CAS  Google Scholar 

  • Netto AT, Campostrini E, Oliveira JG, Bressan-Smith RE (2005) Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves. Sci Hortic 104:199–209

    Article  Google Scholar 

  • Ono K, Hibino T, Kohinata T, Suzuki S, Tanaka Y, Nakamura T, Takabe T, Takabe T (2001) Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances the high-temperatue tolerance of tobacco during germination and early growth. Plant Sci 160:455–461

    Article  PubMed  CAS  Google Scholar 

  • Opeña R, Chen J, Kuo C, Chen H (1992) Genetic and physiological aspects of tropical adaptation in tomato. Asian Vegetable Research and Development Center, Shanhua, pp 321–334

    Google Scholar 

  • Pirondini A, Visioli G, Malcevschi A, Marmiroli N (2006) A 2-D liquid-phase chromatography for proteomic analysis in plant tissues. J Chromatogr B Analyt Technol Biomed Life Sci 833:91–100

    Article  PubMed  CAS  Google Scholar 

  • Porcar-Castell A, Pfundel E, Korhonen JF, Juurola E (2008) A new monitoring PAM fluorometer (MONI-PAM) to study the short- and long-term acclimation of photosystem II in field conditions. Photosynth Res 96:173–179

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Rodríguez E, Moreno DA, Ferreres F, Rubio-Wilhelmi Mdel M, Ruiz JM (2011) Differential responses of five cherry tomato varieties to water stress: changes on phenolic metabolites and related enzymes. Phytochemistry 72:723–729

    Article  PubMed  Google Scholar 

  • Sato S, Peet MM, Thomas JF (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant Cell Environ 23:719–726

    Article  Google Scholar 

  • Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483–486

    Article  PubMed  CAS  Google Scholar 

  • Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52:2207–2211

    PubMed  CAS  Google Scholar 

  • She XP, Song XG (2012) Ethylene inhibits abscisic acid-induced stomatal closure in Vicia faba via reducing nitric oxide levels in guard cells. N Z J Bot 50:203–216

    Article  Google Scholar 

  • Soldi M, Sarto C, Valsecchi C, Magni F, Proserpio V, Ticozzi D, Mocarelli P (2005) Proteome profile of human urine with two-dimensional liquid phase fractionation. Proteomics 5:2641–2647

    Article  PubMed  CAS  Google Scholar 

  • Sultana S, Khew CY, Morshed MM, Namasivayam P, Napis S, Ho CL (2012) Overexpression of monodehydroascorbate reductase from a mangrove plant (AeMDHAR) confers salt tolerance on rice. J Plant Physiol 169:311–318

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Thompson BE (1985) Seedling morphological evaluation: what you can tell by looking. In: Duryea ML (ed) Evaluating seedling quality: principles, procedures, and predictive abilities of major tests. Forest Research Laboratory of the Oregon State University, Oregon, pp 59–71

    Google Scholar 

  • Tóth SZ, Nagy V, Puthur JT, Kovács L, Garab G (2011) The physiological role of ascorbate as photosystem II electron donor: Protection against photoinactivation in heat-stressed leaves. Plant Physiol 156:382–392

    Article  PubMed  PubMed Central  Google Scholar 

  • Tyler PD, Crawford RMM (1970) The role of shikimic acid in waterlogged roots and rhizomes of Iris pseudacorus L. J Exp Bot 21:677–682

    Article  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: An overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151

    PubMed  CAS  PubMed Central  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Xiao Y, Chen W, Tang K, Zhang L (2010) Increased vitamin C content accompanied by an enhanced recycling pathway confers oxidative stress tolerance in Arabidopsis. J Integr Plant Biol 52:400–409

    Article  PubMed  CAS  Google Scholar 

  • Yan X, Chen CS, Ji DH, Hang N, Xie CT (2013) Proteomic profile analysis of Pyropia haitanensis in response to high-temperature stress. J Appl Phycol 26:607–618

    Google Scholar 

  • 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 176:575–582

    Article  PubMed  CAS  Google Scholar 

Download references

Conflict of Interest

The authors declare that they have no competing interests.

Author Contributions Statement

H.H.L and K.H.L carried out the conception and wrote the manuscript. J.Y.S and S.Y.T performed the experiment. H.F.L supervised the whole research. All authors read and approved the revised manuscript. This research was supported by grants from National Council of Science, Taiwan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hsiao-Feng Lo.

Additional information

Hsin-Hung Lin and Kuan-Hung Lin contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. S1

Effects of stress treatments on relative chlorophyll content (SPAD values) in L0994 and L6138. Plants were treated with 22 °C (C), flooding at 22 °C (F), 38 °C (H), and flooding at 38 °C (HF) for 24 h. Values represent the means of five independent SPAD meter readings on five independent plants. Means with the same letters are not significantly different within a row, based on a least significant different (LSD) test at p ≤ 0.05. Error bars represent the standard error. (DOCX 131 kb)

Supplementary Fig. S2

Effects of stress treatments (F, H, and HF) on Fv/Fm in L0994 (circles) and L6138 (triangles). Plants were treated with flooding at 22 °C (a), 38 °C (b), and flooding at 38 °C (c) for 96 h. Values represent the means of five independent plants. Means with the same small letters are not significantly different among times within the same row, based on LSD at p ≤ 0.05 under ANOVA. Means with the same capital letters are not significantly different between two rows within the same time point, based on LSD at p ≤ 0.05 under ANOVA. (DOCX 220 kb)

Supplementary Fig. S3

Representatives of second-column separation in L0994 fractions. Leaf proteins from L0994 plants treated with 22 °C (C; red lines), flooding at 22 °C (F), 38 °C (H), and flooding at 38 °C (HF) for 72 h were separated with a two-dimensional protein fractionation (PF2D) system. The Y-axis represents the optical densitometry pattern (OD at 214 nm). The X-axis represents retention time in minutes according to the concentration of acetonitrile in the mobile phase. Red lines indicate the absorbance after treatment C. Green lines indicate the absorbance from treatment F (a to f), treatment H (g to k), and treatment HF (l to o). (DOCX 414 kb)

Supplementary Fig. S4

Representatives of the second column separation of L6138 fractions. Leaf proteins from L6138 plants treated with 22 °C (C; red lines), flooding at 22 °C (F), 38 °C (H), and flooding at 38 °C (HF) for 72 h were separated with PF2D. The Y-axis represents optical densitometry pattern (OD at 214 nm). The X-axis represents retention time in minutes according to the concentration of acetonitrile in the mobile phase. Red lines indicate the absorbance from treatment C. Green lines indicate the absorbance from treatment F (a and b), treatment H (c to f), and treatment HF (g to j). (DOCX 314 kb)

Supplementary Table S1

Highly differentially expressed protein pattern and function in stressed L0994. (DOCX 23 kb)

Supplementary Table S2

Highly differentially expressed protein pattern and function in stressed L6138. (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, HH., Lin, KH., Syu, JY. et al. Physiological and proteomic analysis in two wild tomato lines under waterlogging and high temperature stress. J. Plant Biochem. Biotechnol. 25, 87–96 (2016). https://doi.org/10.1007/s13562-015-0314-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-015-0314-x

Keywords

Navigation