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Different tolerance of photosynthetic apparatus to Cd stress in two rice cultivars with the same leaf Cd accumulation

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Abstract

In plants, cadmium (Cd) is regarded as one of the most toxic metals and affects many physiological and biochemical processes. To investigate the effects of Cd on photosynthesis and antioxidant system of japonica and indica rice cultivars, Wuyu 21 (WY21) and IIyou 808 (IIY808) seedlings were exposed to different concentrations of Cd for 7 days. Our results indicated that Cd treatments resulted in the significant decrease in photosynthetic capacity and the obvious oxidative damage in WY21 and IIY808. Although Cd contents in the leaves and stem had no obvious difference between WY21 and IIY808 under Cd stress, japonica cultivar WY21 showed higher Cd contents of roots and photosynthetic efficiency compared with indica cultivar IIY808 under Cd stress. In contrast, the lower generation of reactive oxygen species (ROS) and cell death were observed in WY21 relative to IIY808. However, almost all antioxidant enzymes activities and the concentrations of four antioxidants showed no significant differences between WY21 and IIY808. Furthermore, the severe oxidative damage in IIY808 was accompanied by the marked decline in the levels of two photosystem II (PSII) proteins (D2 and D1) under high concentration of Cd. In conclusion, we concluded that high Cd resistance in japonica cultivar WY21 is probably attributed to the high photosynthesis under Cd stress.

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References

  • Agami RA, Mohamed GF (2013) Exogenous treatment with indole-3-acetic acid and salicylic acid alleviates cadmium toxicity in wheat seedlings. Ecotoxicol Environ Saf 94:164–171

    CAS  PubMed  Google Scholar 

  • Aina R, Labra M, Fumagalli P, Vannini C, Marsoni M, Cucchi U, Bracale M, Sgorbati S, Citterio S (2007) Thiol-peptide level and proteomic changes in response to cadmium toxicity in Oryza sativa L. roots. Environ Exp Bot 59:381–392

    CAS  Google Scholar 

  • Arthur Thomas T (1977) An automated procedure for the determination of soluble carbohydrates in herbage. J Sci Food Agric 28(7):639–642

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bao T, Sun T, Sun L (2011) Effect of cadmium hyperaccumulation on antioxidative defense and proline accumulation of Solanum nigrum L. Afr J Biotechnol 10(37):7198–7206

    CAS  Google Scholar 

  • Basa B, Lattanzio G, Soltia Á, Tóthc B, Abadía J, Fodor F, Sárvária É (2014) Changes induced by cadmium stress and iron deficiency in the composition and organization of thylakoid complexes in sugar beet (Beta vulgaris L.). Environ Exp Bot 101:1–11

    CAS  Google Scholar 

  • Bashir S, Zhu J, Fu Q, Hu H (2018) Cadmium mobility, uptake and anti-Oxidative response of water spinach (Ipomoea aquatic) under rice straw biochar, zeolite and rock phosphate as amendments. Chemosphere 194:579–587

    CAS  PubMed  Google Scholar 

  • Brien JAO, Benkova E (2013) Cytokinin cross-talking during biotic and abiotic stress responses. Front Plant Sci 4:451

    Google Scholar 

  • Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98(4):1222–1227

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YE, Liu WJ, Su YQ, Cui JM, Zhang ZW, Yuan M, Zhang HY, Yuan S (2016a) Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. Physiol Plant 158(2):225–235

    CAS  PubMed  Google Scholar 

  • Chen YE, Yuan S, Schröder WP (2016b) Comparison of methods for extracting thylakoid membranes of Arabidopsis plants. Physiol Plant 156(1):3–12

    CAS  PubMed  Google Scholar 

  • Chen YE, Cui JM, Su YQ, Zhang CM, Yuan S (2017a) Comparison of phosphorylation and assembly of photosystem complexes and redox homeostasis in two wheat cultivars with different drought resistance. Sci Rep 7(1):12718

    PubMed  PubMed Central  Google Scholar 

  • Chen YE, Zhang CM, Su YQ, Ma J, Zhang ZW, Yuan M, Zhang HY, Yuan S (2017b) Responses of photosystem II and antioxidative systems to high light and high temperature co-stress in wheat. Environ Exp Bot 135:45–55

    CAS  Google Scholar 

  • Chen YE, Mao JJ, Sun LQ, Huang B, Ding CB, Gu Y, Liao JQ, Hu C, Zhang ZW, Yuan S, Yuan M (2018) Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. Physiol Plant 164(3):349–363

    CAS  PubMed  Google Scholar 

  • Chen YE, Yuan S, Lezhneva L, Meurer J, Schwenkert S, Mamedov F, Schröder WP (2019) The low molecular mass photosystem II protein PsbTn is important for light acclimation. Plant Physiol 179:1739–1753

    CAS  PubMed  Google Scholar 

  • Clemens S, Aarts MG, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18(2):92–99

    CAS  PubMed  Google Scholar 

  • Daud MK, He Q, Mei L, Ali B, Zhu SJ (2015) Ultrastructural, metabolic and proteomic changes in leaves of upland cotton in response to cadmium stress. Chemosphere 120:309–320

    CAS  PubMed  Google Scholar 

  • Duan YP, Yuan S, Tu SH, Feng WQ, Xu F, Zhang ZW, Chen YE, Wang X, Shang J, Lin HH (2010) Effects of cadmium stress on alternative oxidase and photosystem II in three wheat cultivars. Z Naturforsch C 65(1–2):87–94

    CAS  PubMed  Google Scholar 

  • Duan G, Shao G, Tang Z, Chen H, Wang B, Tang Z, Yang Y, Liu Y, Zhao FJ (2017) Genotypic and environmental variations in grain cadmium and arsenic concentrations among a panel of high yielding rice cultivars. Rice 10:9

    PubMed  PubMed Central  Google Scholar 

  • Ekmekci Y, Tanyolac D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165(6):600–611

    CAS  PubMed  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212

    CAS  PubMed  Google Scholar 

  • Ha S, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Phan Tran LS (2012) Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci 17:172–179

    CAS  PubMed  Google Scholar 

  • Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54(393):2601–2613

    CAS  PubMed  Google Scholar 

  • Harel E, Klein S (1972) Light dependent formation of δ-aminolevulinic acid in etiolated leaves of higher plants. Biochem Biophys Res Commun 49(2):364–370

    CAS  PubMed  Google Scholar 

  • Hayat Q, Hayat S, Irfan M, Ahmad A (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ Exp Bot 68(1):14–25

    CAS  Google Scholar 

  • He S, Yang X, He Z, Baligar VC (2017) Morphological and physiological responses of plants to cadmium toxicity: a review. Pedosphere 27(3):421–438

    Google Scholar 

  • Hodgins RR, Van Huystee RB (1986) Rapid simultaneous estimation of protoporphyrin and Mg-porphyrins in higher plants. J Plant Physiol 125(3–4):311–323

    CAS  Google Scholar 

  • Hu X, Tanaka A, Tanaka R (2013) Simple extraction methods that prevent the artifactual conversion of chlorophyll to chlorophyllide during pigment isolation from leaf samples. Plant Methods 9:19

    PubMed  PubMed Central  Google Scholar 

  • Huang D, Gong X, Liu Y, Zeng G, Lai C, Bashir H, Zhou L, Wang D, Xu P, Cheng M, Wan J (2017) Effects of calcium at toxic concentrations of cadmium in plants. Planta 245(5):863–873

    CAS  PubMed  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Lukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192(2):261–268

    CAS  Google Scholar 

  • Krantev A, Yordanova R, Janda T, Szalai G, Popova L (2008) Treatment with salicylic acid decreases the effect of cadmium on photosynthesis in maize plants. J Plant Physiol 165(9):920–931

    CAS  PubMed  Google Scholar 

  • Lee KS, Choi WY, Ko JC, Kim TS, Gregorio GB (2003) Salinity tolerance of japonica and indica Rice (Oryza Sativa L.) at the seedling stage. Planta 216(6):1043–1046

    CAS  PubMed  Google Scholar 

  • Li S, Yu J, Zhu M, Zhao F, Luan S (2012) Cadmium impairs ion homeostasis by altering K+ and Ca2+ channel activities in rice root hair cells. Plant Cell Environ 35:1998–2013

    CAS  PubMed  Google Scholar 

  • Li H, Luo N, Li YW, Cai QY, Li HY, Mo CH, Wong MH (2017) Cadmium in rice: transport mechanisms, influencing factors, and minimizing measures. Environ Pollut 224:622–630

    CAS  PubMed  Google Scholar 

  • Liu JG, Qu P, Zhang W, Dong Y, Li L, Wang MX (2014) Variations among rice cultivars in subcellular distribution of Cd: the relationship between translocation and grain accumulation. Environ Exp Bot 107:25–31

    CAS  Google Scholar 

  • Liu H, Zhang C, Wang J, Zhou C, Feng H, Mahajan MD, Han X (2017) Influence and interaction of iron and cadmium on photosynthesis and antioxidative enzymes in two rice cultivars. Chemosphere 171:240–247

    CAS  PubMed  Google Scholar 

  • Lutz C, Navakoudis E, Seidlitz H, Kotzabasis K (2005) Simulated solar irradiation with enhanced UV-B adjust plastid- and thylakoid-associated polyamine changes for UV-B protection. Biochim Biophys Acta 1710:24–33

    CAS  PubMed  Google Scholar 

  • Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55(1):64–69

    CAS  PubMed  Google Scholar 

  • Mao HT, Chen MY, Su YQ, Wu N, Yuan M, Yuan S, Brestic M, Zivcak M, Zhang HY, Chen YE (2018) Comparison on photosynthesis and antioxidant defense systems in wheat with different ploidy levels and octoploid Triticale. Int J Mol Sci 19(10):3006

    PubMed Central  Google Scholar 

  • Marsh HV, Evans HJ, Matrone G (1963) Investigations of the role of iron in chlorophyll metabolism II. Effect of iron deficiency on chlorophyll synthesis. Plant Physiol 38(6):638–642

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng F, Chae SR, Drews A, Kraume M, Shin HS, Yang F (2009) Recent advances in membrane bioreactors (MBRs): membrane fouling and membrane material. Water Res 43(6):1489–1512

    CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161(1):5–19

    PubMed  Google Scholar 

  • Nath K, Jajoo A, Poudyal RS, Timilsina R, Park YS, Aro EM, Nam HG, Lee CH (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Lett 587(21):3372–3381

    CAS  PubMed  Google Scholar 

  • Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5(5):388–395

    CAS  PubMed  Google Scholar 

  • Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, Jahns P (2010) Identification of slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta 1797(4):466–475

    CAS  PubMed  Google Scholar 

  • Norton GJ, Shafaei M, Travis AJ, Claire MD, John D, Pond D, Cochrane N, Lockhart K, Salt D, Zhang H, Dodd IC, Hossain M, Islam MR, Price AH (2017) Impact of alternate wetting and drying on rice physiology, grain production, and grain quality. Field Crop Res 205:1–13

    Google Scholar 

  • Oomen RJFJ, Wu J, Leliѐvre F, Blanchet S, Richaud P, Barbier-Brygoo H, Aarts MGM, Thomine S (2008) Functional characterization of NRAMP3 and NRAMP4 from the metal hyperaccumulator Thlaspi caerulescens. New Phytol 181:637–650

    PubMed  Google Scholar 

  • Pagliano C, Raviolo M, Dalla Vecchia F, Gabbrielli R, Gonnelli C, Rascio N, Barbato R, La Rocca N (2006) Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). J Photochem Photobiol B 84(1):70–78

    CAS  PubMed  Google Scholar 

  • Pál M, Horváth E, Janda T, Páldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci 169:239–246

    Google Scholar 

  • Paunov M, Koleva L, Vassilev A, Vangronsveld J, Goltsev V (2018) Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. Int J Mol Sci 19(3):787

    PubMed Central  Google Scholar 

  • Perfus-Barbeoch L, Leonhardt N, Vavasseur A, Forestier C (2002) Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. Plant J 32(4):539–548

    CAS  PubMed  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975(3):384–394

    CAS  Google Scholar 

  • Rizwan M, Ali S, Adrees M, Rizvi H, Zia-Ur-Rehman M, Hannan F, Qayyum MF, Hafeez F, Ok YS (2016) Cadmium stress in rice: toxic effects, tolerance mechanisms, and management: a critical review. Environ Sci Pollut Res Int 23(18):17859–17879

    CAS  PubMed  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, Del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29(8):1532–1544

    PubMed  Google Scholar 

  • Schreiber U, Klughammer C, Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse modulation system. Z Naturforsch C 43:686–698

    CAS  Google Scholar 

  • Sebastian A, Prasad MNV (2014) Cadmium minimization in rice. A review. Agron Sustain Dev 34:155–173

    CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:1–26

    Google Scholar 

  • Shirasu K, Lahaye T, Tan MW, Zhou F, Azevedo C, Schulze-Lefert P (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99(4):355–366

    CAS  PubMed  Google Scholar 

  • Song WY, Mendoza-Cózatl DG, Lee Y, Schroeder JI, Ahn SN, Lee HS, Wicker T, Martinoia E (2014a) Phytochelatin-metal(loid) transport into vacuoles shows different substrate preferences in barley and Arabidopsis. Plant Cell Environ 37(5):1192–1201

    CAS  PubMed  Google Scholar 

  • Song WY, Yang HC, Shao HB, Zheng AZ, Marian B (2014b) The alleviative effects of salicylic acid on the activities of catalase and superoxide dismutase in malting barley (Hordeum uhulgare L.) seedling leaves stressed by heavy metals. Clean Soil Air Water 42(1):88–97

    CAS  Google Scholar 

  • Song WE, Chen SB, Liu JF, Li CH, Song NN, Ning LI, Bin LI (2015) Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution. J Integr Agric 14:1845–1854

    CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    CAS  PubMed  Google Scholar 

  • Sytar O, Kumari P, Yadav S, Brestic M, Rastogi A (2019) Phytohormone priming: regulator for heavy metal stress in plants. J Plant Growth Regul 38(2):739–752

    CAS  Google Scholar 

  • Taiz L, Zeiger E (2010) Photosynthesis: the light reaction. In: Plant physiology. Sinauer Associates Inc, Sunderland, pp 163–198

  • Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62(14):4843–4850

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tambussi EA, Nogués S, Araus JL (2005) Ear of durum wheat under water stress: water relations and photosynthetic metabolism. Planta 221(3):446–458

    CAS  PubMed  Google Scholar 

  • Tóth T, Zsiros O, Kis M, Garab G, Kovács L (2012) Cadmium exerts its toxic effects on photosynthesis via a cascade mechanism in the cyanobacterium, Synechocystis PCC 6803. Plant, Cell Environ 35(12):2075–2086

    Google Scholar 

  • Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107(38):16500–16505

    CAS  PubMed  Google Scholar 

  • Ueno D, Millner MJ, Yamaji N, Yokosho K, Koyama E, Zambrono MC, Kaskie M, Ebbs S, Kochian LV, Ma JF (2011) Elevated expression of TcHMA3 plays a key role in the extreme Cd tolerance in a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Plant J 66:852–862

    CAS  PubMed  Google Scholar 

  • Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162(6):669–677

    CAS  PubMed  Google Scholar 

  • Wang SL, Xu XR, Sun YX, Liu JL, Li HB (2013) Heavy metal pollution in coastal areas of South China: a review. Mar Pollut Bull 76(1–2):7–15

    CAS  PubMed  Google Scholar 

  • Wang CH, Zheng XM, Xu Q, Yuan XP, Huang L, Zhou HF, Wei XH, Ge S (2014a) Genetic diversity and classification of Oryza sativa with emphasis on Chinese rice germplasm. Heredity 112:489–496

    CAS  PubMed  Google Scholar 

  • Wang Y, Jiang X, Li K, Wu M, Zhang R, Zhang L, Chen G (2014b) Photosynthetic responses of Oryza sativa L. seedlings to cadmium stress: physiological, biochemical and ultrastructural analyses. Biometals 27:389–401

    CAS  PubMed  Google Scholar 

  • Wang F, Wang M, Liu Z, Shi Y, Han T, Ye Y, Gong N, Sun J, Zhu C (2015) Different responses of low grain-Cd-accumulating and high grain-Cd-accumulating rice cultivars to Cd stress. Plant Physiol Biochem 96:261–269

    CAS  PubMed  Google Scholar 

  • Wei W, Chai T, Zhang Y, Han L, Xu J, Guan Z (2009) The Thlaspi caerulescens NRAMP homologue TcNRAMP3 is capable of divalent cation transport. Mol Biotechnol 41:15–21

    CAS  PubMed  Google Scholar 

  • Xu C, Huang B (2010) Diferential proteomic responses to water stress induced by PEG in two creeping bentgrass cultivars difering in stress tolerance. J Plant Physiol 167:1477–1485

    CAS  PubMed  Google Scholar 

  • Yamori W, Noguchi K, Hanba YT, Terashima I (2006) Effects of internal conductance on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Physiol 47(8):1069–1080

    CAS  PubMed  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119(1–2):101–117

    CAS  PubMed  Google Scholar 

  • Yu HY, Liu C, Zhu J, Li F, Deng DM, Wang Q, Liu C (2016) Cadmium availability in rice paddy fields from a mining area: the effects of soil properties highlighting iron fractions and pH value. Environ Pollut 209:38–45

    CAS  PubMed  Google Scholar 

  • Zeng L (2005) Exploration of relationships between physiological parameters and growth performance of rice (Oryza sativa L.) seedlings under salinity stress using multivariate analysis. Plant Soil 268(1):51–59

    CAS  Google Scholar 

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Acknowledgements

This research was obtained to support by Xichang Municipal Science and Technology Program (18JSYJ09), Sichuan Province Academic and Technical Leaders Fund, and Sichuan Science and Technology Program (2018HH0129).

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Chen, YE., Mao, HT., Wu, N. et al. Different tolerance of photosynthetic apparatus to Cd stress in two rice cultivars with the same leaf Cd accumulation. Acta Physiol Plant 41, 191 (2019). https://doi.org/10.1007/s11738-019-2981-z

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