Abstract
Sweet sorghum is an important energy crop. This study aimed to investigate the effects of salt pretreatment on the interaction between photosystem II (PSII) and photosystem I (PSI) upon salt stress. In this study, sweet sorghum was pretreated with 150 mM NaCl for 10 days, and subsequently, the pretreated plants were subjected to severe salt stress at 300 mM NaCl. PSII and PSI photoinhibition occurred in non-pretreated plants after 4 days of salt stress, as the maximum quantum yield of PSII (Fv/Fm) and the maximal photochemical capacity of PSI (△MR/MR0) significantly decreased, and their normal coordination was destroyed. The significant positive correlation between Fv/Fm and △MR/MR0 under salt stress indicated that PSII photoinhibition was in relation to PSI photoinhibition, and PSI photoinhibition might lead to PSII photoinhibition through inhibiting electron transport at the acceptor side of PSII. Salt stress did not induce PSII photoinhibition in salt-pretreated plants, and thus, salt pretreatment protected PSI against photoinhibition not by aggravating PSII photoinhibition. Salt pretreatment mitigated the decrease in CO2 assimilation, reduced the feedback inhibition on photosynthetic electron transport and then contributed to suppressing PSI and PSII photoinhibition in sweet sorghum under salt stress. Therefore, the normal coordination between PSII and PSI was maintained in salt-pretreated plants. In conclusion, salt pretreatment ensured normal PSII and PSI coordination by preventing photoinhibition in sweet sorghum under salt stress.
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Abbreviations
- Ci:
-
Intercellular CO2 concentration
- ETo/ABS:
-
Quantum yield for electron transport
- ETo/TRo:
-
Probability that an electron moves further than primary acceptor of PSII
- Fv/Fm:
-
The maximal quantum yield of PSII
- gs :
-
Stomatal conductance
- MDA:
-
Malondialdehyde
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- ROS:
-
Reactive oxygen species
- △MR/MR0 :
-
The maximal photochemical capacity of PSI
- ΦPSII:
-
Actual photochemical efficiency of PSII
- 1−qP:
-
Excitation pressure of PSII
References
Almodares A, Hadi MR, Ahmadpour H (2008) Sorghum stem yield and soluble carbohydrates under different salinity levels. Afr J Biotechnol 7:4051–4055
Amzallag GN, Lerner HR, Poljakoff-Mayber A (1990) Induction of increased salt tolerance in sorghum bicolor by NaCl pretreatment. J Exp Bot 41:29–34
Arnon DI (1950) Dennis Robert Hoagland: 1884–1949. Science 112(2921):739–742
Azzabi G, Pinnola A, Betterle N, Bassi R, Alboresi A (2012) Enhancement of non-photochemical quenching in the bryophyte Physcomitrella patens during acclimation to salt and osmotic stress. Plant Cell Physiol 53(10):1815–1825
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
Djanaguiraman M, Sheeba JA, Shanker AK, Devi DD, Bangarusamy U (2006) Rice can acclimate to lethal level of salinity by pretreatment with sublethal level of salinity through osmotic adjustment. Plant Soil 284:363–373
Feng LL, Han YJ, Liu G, An BG, Yang J, Yang GH, Li YS, Zhu YG (2007) Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants. Funct Plant Biol 34:822–834
Guerrero RY, González LM, Dell’Amico J, Núñez M, Pieters AJ (2014) Reversion of deleterious effects of salt stress by activation of ROS detoxifying enzymes via foliar application of 24-epibrassinolide in rice seedlings. Theor Exp Plant Physiol 27:31–40
Kalaji HM, Pietkiewicz S (1993) Salinity effects on plant growth and other physiological processes. Acta Physiol Plant 15:89–124
Kalaji HM, Govindjee Bosa K, Koscielniak J, Zuk-Golaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72
Kalaji HM, Goltsev V, Bosa K, Allakhverdiev SI, Strasser RJ, Govindjee (2012) Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker. Photosynth Res 114:69–96
Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, Samborska IA, Cetner MD, Allakhverdiev SI, Goltsev V (2014a) Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol Biochem 81:16–25
Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dabrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli DB, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serodio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014b) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res 122:121–158
Kiani-Pouya A (2015) Changes in activities of antioxidant enzymes and photosynthetic attributes in triticale (×Triticosecale Wittmack) genotypes in response to long-term salt stress at two distinct growth stages. Acta Physiol Plant 37:72
Koyro HW, Hussain T, Huchzermeyer B, Khan MA (2013) Photosynthetic and growth responses of a perennial halophytic grass Panicum turgidum to increasing NaCl concentrations. Environ Exp Bot 91:22–29
Kudoh H, Sonoike K (2002) Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215:541–548
Lea PJ, Parry MAJ, Medrano H (2004) Improving resistance to drought and salinity in plants. Ann Appl Biol 144:249–250
Li XG, Wang XM, Meng QW, Zou Q (2004) Factors limiting photosynthetic recovery in sweet pepper leaves after short-term chilling stress under low irradiance. Photosynthetica 42:257–262
Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ 26:595–601
Lu KX, Yang Y, He Y, Jiang DA (2008) Induction of cyclic electron flow around photosystem 1 and state transition are correlated with salt tolerance in soybean. Photosynthetica 46:10–16
Lu KX, Cao BH, Feng XP, He Y, Jiang DA (2009) Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthetica 47:381–387
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421
Nishiyamaa Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46
Oukarroum A, Bussotti F, Goltsev V, Kalaji HM (2014) Correlation between reactive oxygen species production and photochemistry of photosystems I and II in Lemna gibba L. plants under salt stress. Environ Exp Bot 109:80–88
Rozema J, Flowers T (2008) Ecology crops for a salinized world. Science 322:1478–1480
Saha P, Kunda P, Biswas AK (2012) Influence of sodium chloride on the regulation of Krebs cycle intermediates and enzymes of respiratory chain in mungbean (Vigna radiata L. Wilczek) seedlings. Plant Physiol Biochem 60:214–222
Schansker G, Srivastava A, Govindjee Strasser RJ (2003) Characterization of the 820 nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30:785–796
Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Horie T, Kochian LV, Munns R, Nishizawa NK, Tsay YF, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66
Sivritepe HO, Sivritepe N, Eris A, Turhan E (2005) The effects of NaCl pre-treatments on salt tolerance of melons grown under long-term salinity. Sci Hortic 106:568–581
Song J, Shi GW, Gao B, Fan H, Wang BS (2011) Waterlogging and salinity effects on two Suaeda salsa populations. Physiol Plant 141:343–351
Sonoike K (1996) Degradation of psaB gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: possible involvement of active oxygen species. Plant Sci 115:157–164
Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64
Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll-alpha fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42
Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor & Francis, Bristol, pp 445–483
Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820 nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta 1797:1313–1326
Tajdoost S, Farboodnia T, Heidari R (2007) Salt pretreatment enhance salt tolerance in Zea mays L. seedlings. Pak J Biol Sci 10:2086–2090
Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182
Umezawa T, Shimizu K, Kato M, Ueda T (2000) Enhancement of salt tolerance in soybean with NaCl pretreatment. Physiol Plant 110:59–63
Vasilakoglou I, Dhima K, Karagiannidis N, Gatsis T (2011) Sweet sorghum productivity for biofuels under increased soil salinity and reduced irrigation. Field Crop Res 120:38–46
Wani AS, Ahmad A, Hayat S, Fariduddin Q (2013) Salt-induced modulation in growth, photosynthesis and antioxidant system in two varieties of Brassica juncea. Saudi J Biol Sci 20:183–193
Yan K, Chen W, He XY, Zhang GY, Xu S, Wang LL (2010) Responses of photosynthesis, lipid peroxidation and antioxidant system in leaves of Quercus mongolica to elevated O3. Environ Exp Bot 69:198–204
Yan K, Chen P, Shao H, Zhao S, Zhang L, Zhang L, Xu G, Sun J (2012) Responses of photosynthesis and photosystem II to higher temperature and salt stress in sorghum. J Agron Crop Sci 198:218–226
Yan K, Chen P, Shao HB, Shao CY, Zhao SJ, Brestic M (2013a) Dissection of photosynthetic electron transport process in sweet sorghum under heat stress. PLoS One 8:e62100
Yan K, Chen P, Shao HB, Zhao SJ (2013b) Characterization of photosynthetic electron transport chain in bioenergy crop Jerusalem artichoke (Helianthus tuberosus L.) under heat stress for sustainable cultivation. Ind Crop Prod 50:809–815
Yan K, Shao HB, Shao CY, Chen P, Zhao SJ, Brestic M, Chen XB (2013c) Physiological adaptive mechanisms of plants grown in saline soil and implications for sustainable saline agriculture in coastal zone. Acta Physiol Plant 35:2867–2878
Yan K, Wu CW, Zhang LH, Chen XB (2015) Contrasting photosynthesis and photoinhibition in tetraploid and its autodiploid honeysuckle (Lonicera japonica Thunb.) under salt stress. Front Plant Sci 6:227
Yang XH, Liang Z, Wen XG, Lu CM (2008) Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 66:73–86
Yang C, Zhang ZS, Gao HY, Fan XL, Liu MJ, Li XD (2014) The mechanism by which NaCl treatment alleviates PSI photoinhibition under chilling-light treatment. J Photochem Photobiol B 140:286–291
Yazici I, Tuerkan I, Sekmen AH, Demiral T (2007) Salinity tolerance of purslane (Portulaca oleracea L.) is achieved by enhanced antioxidative system, lower level of lipid peroxidation and proline accumulation. Environ Exp Bot 61:49–57
Zhang SP, Scheller HV (2004) Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45:1595–1602
Zhang ZS, Jia YJ, Gao HY, Zhang LT, Li HD, Meng QW (2011) Characterization of PSI recovery after chilling-induced photoinhibition in cucumber (Cucumis sativus L.) leaves. Planta 234:883–889
Zhang LT, Zhang ZS, Gao HY, Xue ZC, Yang C, Meng XL, Meng QW (2012) Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiol Plant 143:396–407
Zhang ZS, Yang C, Gao HY, Zhang LT, Fan XL, Liu MJ (2014) The higher sensitivity of PSI to ROS results in lower chilling-light tolerance of photosystems in young leaves of cucumber. J Photochem Photobiol B 137:127–134
Zivcak M, Brestic M, Balatova Z, Drevenakova P, Olsovska K, Kalaji HM, Yang XH, Allakhverdiev SI (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546
Zivcak M, Brestic M, Kalaji MH, Govindjee (2014) Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynth Res 119:339–354
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This work was jointly supported by the National Natural Science Foundation of China (41201292) and the Special Project of Commonweal Vocation (Ocean, 201105020).
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Yan, K., Zhao, S., Liu, Z. et al. Salt pretreatment alleviated salt-induced photoinhibition in sweet sorghum. Theor. Exp. Plant Physiol. 27, 119–129 (2015). https://doi.org/10.1007/s40626-015-0038-2
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DOI: https://doi.org/10.1007/s40626-015-0038-2