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Physiological response to heat stress of tomato ‘Micro-Tom’ plants expressing high and low levels of mitochondrial sHSP23.6 protein

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Abstract

Tomato Micro-Tom’ plants were transformed for high or low expression of the mitochondrial small “heat shock” protein (HSP) (MT-sHSP23.6) to evaluate their response to high temperature. The plants were raised for 59 days under a controlled temperature, photoperiod and photon flow density and then subjected to heat stress for 24 h at 37 °C, followed by a recovery period under normal conditions (21 ± 2 °C). The cycle was repeated. The chlorophyll a fluorescence intensity was measured, and the parameters of the JIP-test were calculated. The gas exchange was also evaluated. The JIP-test showed significantly different responses of the genotypes to heat stress. The parameters of photosystem I activity and the net assimilation of CO2 increased during the first stress cycle in genotypes with a high expression of MT-sHSP23.6 and in non-transformed plants; however, the net assimilation of CO2 decreased in genotypes with a low expression of MT-sHSP23.6. The data suggest that MT-sHSP23.6 participates in the heat tolerance mechanism, considering that the suppression of this protein resulted in greater physiological damage during heat stress.

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Abbreviations

ABS/RC:

Absorption flux (of antenna Chls) per RC

AS:

Plants transformed in the anti-sense orientation

DI0/RC:

Dissipation flux per RC

ET0/RC:

Electron transport flux (further than QA) per RC

MT-sHSP:

Mitochondrial small HSP

N:

Turnover number as reduction, oxidation, re-reduction of QA in time span from light until reaching FM

OEC:

Oxygen evolution complex

PIABS :

Performance index (potential) for energy conservation from exciton to the reduction of intersystem electron acceptors

PItotal :

Performance index (potential) for energy conservation from exciton to the reduction of PSI end acceptors

PSII:

Photosystem II

PSI:

Photosystem I

RC:

Reaction centre

RE0/RC:

Electron flux reducing end electron acceptors at the PSI acceptor side, per RC

sHSPs:

Small HSPs

S:

Plants transformed in the sense orientation

Sm :

Total complementary area normalised above the transient OJIP

Ss :

Total complementary area normalised above the curve of only transient OJ

TR0/RC:

Trapped energy flux (leading to QA reduction) per RC

WT:

Non-transformed plants

φPo :

Maximum quantum yield for primary photochemistry

φEo :

Quantum yield for electron transport (ET)

φRo :

Quantum yield for reduction of end electron acceptors at the PSI acceptor side (RE)

φDo :

Quantum yield for dissipation (DI)

Ψ0 :

Probability (at time 0) that a trapped exciton moves an electron into the electron transport chain beyond QA

δ0 :

Probability with which an electron from the intersystem electron carriers moves to reduce end electron acceptors at the PSI acceptor side

References

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev PlantBiol 59:89–113

    CAS  Google Scholar 

  • Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, Koskull-Doring PV (2004) Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29:471–487

    PubMed  CAS  Google Scholar 

  • Barsan C, Sanchez-Bel P, Rombaldi C, Egea I, Rossignol M, Kuntz M, Zouine M, Latché A, Bouzayen M, Pech JC (2010) Characteristics of the tomato chromoplast revealed by proteomic analysis. J Exp Bot 61:2413–2431

    PubMed  CAS  Google Scholar 

  • Béthune J, Wieland F, Moelleken J (2006) COPI-mediated transport. J Membr Biol 211:65–69

    PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–251

    PubMed  CAS  Google Scholar 

  • Bukhov NG, Sabat SC, Mohanty P (1990) Analysis of chlorophyll a fluorescence changes in weak light in heat treated Amaranthus chloroplasts. Photosynth Res 23:81–87

    CAS  Google Scholar 

  • Bukhov NG, Wiese C, Neimanis SE, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–83

    CAS  Google Scholar 

  • Bukhov NG, Govindachary S, Egorova EA, Joly D, Carpentier R (2003) N, N, N′, N′ -tetramethyl-p-phenylenediamine initiates the appearance of a well-resolved I peak in the kinetics of chlorophyll fluorescence rise in isolated thylakoids. Biochim Biophys Acta 1607:91–96

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143:251–262

    PubMed  CAS  Google Scholar 

  • Chou M, Chen Y, Lin C (1989) Thermotolerance of isolated mitochondria associated with heat shock proteins. Plant Physiol 89:617–621

    PubMed  CAS  Google Scholar 

  • Clarke AK, Critchley C (1990) Synthesis of early heat shock proteins in young leaves of barley and sorgum. Plant Physiol 94:567–576

    PubMed  CAS  Google Scholar 

  • Dubeau SF, Pan F, Tremblay GC, Bradley TM (1998) Thermal shock of salmon in vivo induces the heat shock protein hsp 70 and confers protection against osmotic shock. Aquaculture 168:311–323

    CAS  Google Scholar 

  • Ducruet MH, Lemoine Y (1985) Increased heat sensitivity of the photosynthetic apparatus in triazine-resistant bio types from different plant species. Plant Cell Physiol 26:419–429

    CAS  Google Scholar 

  • Gandia-Herrero F, Lorenz A, Larson T, Graham IA, Bowles DJ, Rylott EL, Bruce NC (2008) Detoxification of the explosive 2,4,6-trinitrotoluene in Arabidopsis- discovery of bifunctional O- and C-glucosyltransferases. Plant J 56:963–974

    PubMed  CAS  Google Scholar 

  • Hájek T, Honys D, Witters E, Čapková V (2005) Identification of stress-induced mitochondrial proteins in cultured tobacco cells. Physiol Plantarum 124:12–24

    Google Scholar 

  • Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444

    PubMed  CAS  Google Scholar 

  • Hoagland D, Arnon DI (1950) The water culture method for growing plants without soil. California agriculture experimental station circular. University of California at Berkeley, Berkeley, p 32

    Google Scholar 

  • Kouřil R, Ilíka P, Tomeka P, Nauša JAN, Poulíčkováb A (2001) Chlorophyll fluorescence temperature curve on Klebsormidiumflaccidum cultivated at different temperature regimes. J Plant Physiol 158:1131–1136

    Google Scholar 

  • Lazár D (2006) The Polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Funct Plant Biol 33:9–30

    Google Scholar 

  • Lee BH, Won SH, Lee HS, Miyao M, Chung WI, Kim IJ, Jo J (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245:283–290

    PubMed  CAS  Google Scholar 

  • Lin CY, Roberts JK, Key JL (1984) Acquisition of thermotolerance in soybean seedling, synthesis and accumulation of heat shock proteins and their cellular localization. Plant Physiol 74:152–160

    PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408

    PubMed  CAS  Google Scholar 

  • Millar AH, Sweetlove LJ, Giege P, Leaver CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127:1711–1727

    PubMed  CAS  Google Scholar 

  • Millar AH, Trend AE, Heazlewood JL (2004) Changes in the mitochondrial proteome during the anoxia to air transition in rice focus around cytochrome-containing respiratory complexes. J Biol Chem 279:39471–39478

    PubMed  CAS  Google Scholar 

  • Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM (2005) The plant mitochondrial proteome. Trends Plant Sci 10:36–43

    PubMed  CAS  Google Scholar 

  • Millar AH, Small ID, Day DA, Whelan J (2008) Mitochondrial biogenesis and function in Arabidopsis. Arabidopsis Book 6:e0111. doi:10.1199/tab.0111

    PubMed  Google Scholar 

  • Misra AN, Srivastava A, Strasser RJ (2001) Utilization of fast chlorophyll a fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings. J Plant Physiol 158:1173–1181

    CAS  Google Scholar 

  • Mohanty P, Kreslavski VD, Klimov VV, Los DA, Mimuro M, Carpentier R, Allakhverdiev SI (2012) Heat stress: susceptibility, recovery and regulation. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advance in photosynthesis and respiration. v.34. Springer, Dordrecht, pp 251–274

    Google Scholar 

  • Murakami T, Matsuba S, Funatsuki H, Kawaguchi K, Saruyama H, Tanida M, Sato Y (2004) Overexpression of a small heat shock protein, sHSP17.7, confers both heat tolerance and UV-B resistance to rice plants. Mol Breeding 13:165–175

    CAS  Google Scholar 

  • Nautiyal PC, Shono M (2010) Analysis of the role of mitochondrial and endoplasmic reticulum localized small heat shock proteins in tomato. Biol Plant 54:715–719

    CAS  Google Scholar 

  • Nautiyal PC, Shono M, Egawa Y (2005) Enhanced thermotolerance of the vegetative part of MT-sHSP transgenic tomato line. Sci Hortic 105:393–409

    Google Scholar 

  • Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547

    PubMed  CAS  Google Scholar 

  • Ogweno J, Song X, Hu W, Shi K, Zhou Y, Yu J (2009) Detached leaves of tomato differ in their photosynthetic physiological response to moderate high and low temperature stress. Sci Hortic 123:17–22

    CAS  Google Scholar 

  • Oukarroum A, Strasser RJ, Schansker G (2012) Heat stress and the photosynthetic electron transport chain of the lichen Parmelinatiliacea (Hoffm.) Ach. in the dry and the wet state: differences and similarities with the heat stress response of higher plants. Photosynth Res 111:303–314

    PubMed  CAS  Google Scholar 

  • Panda D, Rao DN, Sharma SG, Strasser RJ, Sarkar RK (2006) Submergence effects on rice genotypes during seedling stage: probing of submergence driven changes of photosystem 2 by chlorophyll a fluorescence induction O-J-I-P transients. Photosynthetica 44:69–75

    CAS  Google Scholar 

  • Pegoraro C, Mertz LM, Maia LC, Rombaldi CV, Oliveira AC (2011) Importance of heat shock proteins in maize. J Crop Sci Biotech 14:85–95

    Google Scholar 

  • Preczewski PJ, Heckathorn SA, Downs CA, Coleman JS (2000) Photosynthetic thermo-tolerance is quantitatively and positively correlated with production of specific heat-shock proteins among nine genotypes of Lycopersicon (tomato). Photosynthetica 38:127–134

    CAS  Google Scholar 

  • Radloff M, Delling M, Gercken G (1998) Protein phosphorylation in alveolar macrophages after stimulation with heavy metal-coated silica particles. Toxicol Lett 96–97:69–75

    PubMed  Google Scholar 

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    PubMed  CAS  Google Scholar 

  • Sanmiya K, Suzuki K, Egawa Y, Shono M (2004) Mitochondrial small heat-shock protein enhances thermotolerance in tobacco plants. FEBS Lett 557:265–268

    PubMed  CAS  Google Scholar 

  • Schansker G, Tóth SZ, Kovács L, Holzwarth AR, Garab G (2011) Evidence for a fluorescence yield change driven by a light-induced conformational change within photosystem II during the fast chlorophyll a fluorescence rise. Biochim Biophys Acta 1807:1032–1043

    PubMed  CAS  Google Scholar 

  • Srivastava A, Strasser RJ, Govindjee (1999) Greening of peas: parallel measurements of 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37:365–392

    CAS  Google Scholar 

  • Strasser BJ (1997) Donor side capacity of Photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–155

    CAS  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transient to address environmental questions: the JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer, Dordrecht, pp 977–980

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis. Advance in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 321–362

    Google Scholar 

  • Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A (ed) Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics. Springer, Dordrecht, pp 679–703

    Google Scholar 

  • Van Aken O, Zhang B, Carrie C, Uggalla V, Paynter E, Giraud E, Whelan J (2009) Defining the mitochondrial stress response in Arabidopsis thaliana. Mol Plant 2:1310–1324

    PubMed  Google Scholar 

  • Vierling E (1991) The role of heat shock proteins in plants. Annu Rev Plant Phys 42:579–620

    CAS  Google Scholar 

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

    Google Scholar 

  • Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. Environ Exp Bot 47:325–338

    CAS  Google Scholar 

  • Yusuf MA, Kumar D, Rajwanshi R, Strasser RJ, Tsimilli-Michael M, Govindjee, Sarin NB (2010) Overexpression of y-totopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochim Biophys Acta 1797:1428–1438

    PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge the financial support of the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), Ministério de Ciência e Tecnologia, FINEP, CAPES (Coordenação de Aperfeiçoamento de pessoal de Nível Superior), and FAPERGS (Fundação de Amparo à Pesquisa do Estudo do Rio Grande do Sul).

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Correspondence to Marcos Antonio Bacarin.

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Huther, C.M., Ramm, A., Rombaldi, C.V. et al. Physiological response to heat stress of tomato ‘Micro-Tom’ plants expressing high and low levels of mitochondrial sHSP23.6 protein. Plant Growth Regul 70, 175–185 (2013). https://doi.org/10.1007/s10725-013-9790-y

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