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Effects of hematin and carbon monoxide on the salinity stress responses of Cassia obtusifolia L. seeds and seedlings

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Abstract

Aims

The purpose of the present study was to investigate the mechanism of carbon monoxide (CO) and hematin in alleviating the inhibition of Cassia obtusifolia seeds and seedlings. NaCl (100 mM) was used to mimic salinity stress in a series of experiments.

Methods

Varying combinations of CO in a saturated aqueous solution and hematin (1.0 μM) were added to seeds and seedlings under salinity stress. Seed germination indices and seedling parameters were investigated.

Results

Seed germination and seedling growth were significantly inhibited under salinity stress. NaCl-induced inhibitory effects on seed germination and seedling growth were ameliorated by hematin or the CO aqueous solution. Addition of 1.0 μM hematin or 5 % CO-saturated aqueous solution to seeds and seedlings significantly alleviated damage to the plant cells under salinity stress. Hematin and the CO aqueous solution enhanced chlorophyll concentration, total soluble sugars, free proline, and soluble protein, and improved photosystem II (PSII) photochemical efficiency levels, PSII actual photochemical efficiency, and the photochemical quench coefficient. In contrast, the non-photochemical quenching coefficient decreased. Hematin and the CO aqueous solution also enhanced the activities of superoxide dismutase, peroxidase, catalase, ascorbate peroxidase, and glutathione reductase, thus alleviating oxidative damage, as indicated by decreases in hiobarbituric acid reactive substances, hydrogen peroxide concentration, relative conductivity, and lipoxygenase activity. Heme oxygenase (HO) activity was increased by hematin treatment. Hematin may contribute to endogenous HO-derived CO, since the addition of zinc protoporphyrin IX or hemoglobin reversed the protective effects conferred by hematin specified above.

Conclusions

Based on the experimental results, we conclude that hematin and CO induce advantageous effects on the attenuation of salt-stress inhibition of C. obtusifolia seeds and seedlings and alleviate oxidative damage by conferring beneficial cytoprotection and activating anti-oxidant enzymes.

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Abbreviations

CO:

carbon monoxide

H:

hematin

HO:

heme oxygenase

Hb:

hemoglobin

ZnPPIX:

zinc protoporphyrin IX

BV-IXα:

biliverdin-IXα

Gi:

germination index

Gr:

germination rate

Gv:

germination vigor

Vi:

vigor index

Chl:

Chlorophyll

F v/F m :

photochemical efficiency of photosystem II

\( F_v^{\prime }/F_m^{\prime } \) :

photochemical efficiency

ΦPSII:

PSII actual photochemical efficiency

qP :

photochemical quench coefficient

NPQ:

no-photochemical quenching coefficient

ROS:

reactive oxygen species

TBARS:

thiobarbituric acid reactive substances

H2O2 :

hydrogen peroxide

LOX:

lipoxygenase

NBT:

nitroblue tetrazolium

SOD:

superoxide dismutase

POD:

peroxidase

CAT:

catalase

APX:

ascorbate peroxidase

GR:

glutathione reductase.

References

  • Ahmad S, Wahid A, Rasul E, Wahid A (2005) Comparative morphological and physiological responses of green gram genotypes to salinity applied at different growth stages. Bot Bull Acad Sin 46:135–142

    Google Scholar 

  • Anu SJ, Rao JM (2001) Oxanthrone esters from the aerial parts of Cassia kleinii. Phytochemistry 57:583–585

    Article  PubMed  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Asada K (1999) The water-cycle in chloroplasts: scavenging the active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639

    Article  CAS  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Application of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  PubMed  CAS  Google Scholar 

  • Barber J, Andersson B (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17:61–66

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldran RP, Teare ID (1973) Raipid determination of free proline for water studies. Plant Soil 39:205–208

    Article  CAS  Google Scholar 

  • Battacharjee S, Mukherjee AK (1996) Ethylene evolution and membrane lipid peroxidation as indicators of salt injury in leaf tissues of Amaranthus seedlings. Indian J Exp Biol 34:279–281

    Google Scholar 

  • Bor M, Özdemir F, Türkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Sci 164:77–84

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Bio chem 72:248–254

    CAS  Google Scholar 

  • Cao ZY, Huang BK, Wang QY, Xuan W, Ling TF, Zhang B (2007) Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway. Chin Sci Bull 52:2365–2373

    Article  CAS  Google Scholar 

  • Carrasco RM, Rodriguez JS, Perez P (2002) Changes in chlorophyll fluorescence during the course of photoperiod and in response to drought in Casuarina equisetifolia Forst. and Forst. Photosynthetica 40:363–368

    Article  Google Scholar 

  • Davis SJ, Kurepa J, Vierstra RD (1999) The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc Natl Acad Sci 96:6541–6546

    Article  PubMed  CAS  Google Scholar 

  • Davis SJ, Hee-Bhoo S, Durski AM, Walker JM, Vierstra RD (2001) The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 126:656–669

    Article  PubMed  CAS  Google Scholar 

  • Dekker J, Hargrove M (2002) Weedy adaptation in Setaria spp. V. effects of gaseous environment on giant foxtail (Setaria faberii) (Poaceae) seed germination. Am J Bot 89:410–416

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Adams WWIII, Barker DH (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci Limerick 135:1–9

    Article  CAS  Google Scholar 

  • Dulak J, Józkowicz A (2003) Carbon monoxide-a “new” gaseous modulator of gene expression. Acta Biochim Pol 50:31–47

    PubMed  CAS  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplast: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  Google Scholar 

  • Gadallah MAA (1999) Effect of proline and glycine betaine on Vicia faba responses to salt stress. Biol Plant 42:247–249

    Article  Google Scholar 

  • García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem Biophys Acta 99:87–92

    Google Scholar 

  • Giannoplitis CN, Ries SK (1977) Superoxide dismutase purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59:315–318

    Article  Google Scholar 

  • Goel A, Sheoran IS (2003) Lipid peroxidation and peroxide-scavenging enzyme in cotton seeds under natural ageing. Biol Plant 46:429–434

    Article  CAS  Google Scholar 

  • Guo K, Xia K, Yang ZM (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452

    Article  PubMed  CAS  Google Scholar 

  • Guo K, Kong WW, Yang ZM (2009) Carbon monoxide promotes root hair development in tomato. Plant Cell Environ 32:1033–1045

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Strasser RJ, Greppin H (1991) Atheoretical and experimental analysis of the qP and qN coefficients of chlorophyll fluorescence quenching and their relation to photochemical land non photochemical event. Photosynth Res 27:41–55

    Article  CAS  Google Scholar 

  • Heath RL, Packer I (1968) Photoperoxidation in isolated chloroplst I, kinetics and stochiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  PubMed  CAS  Google Scholar 

  • Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Anal Biochem 55:554–562

    Article  PubMed  CAS  Google Scholar 

  • Hormann H, Neubauer C, Schreiber U (1994) On the relationship between chlorophyll fluorescence quenching and the quantum yield of electron transport in isolated thylakoids. Photosynth Res 40:93–106

    Article  CAS  Google Scholar 

  • Jahnke LS, White AL (2003) Long-termhyposaline and hypersaline stresses produce distinct antioxidant responses in the marine alga Dunaliella tertiolecta. J Plant Physiol 160:1193–1202

    Article  PubMed  CAS  Google Scholar 

  • Joshi H, Kapoor VP (2003) Cassia grandis Linn. f. seed galactomannan: structural and crystallographical studies. Carbohydrate Res 338:1907–1912

    Article  CAS  Google Scholar 

  • Koca H, Bor M, Özdemir F, Türkan I (2007) The effect of salt stress on lipid peroxidation, antioxidative enzymes and proline content of sesame cultivars. Environ Exp Bot 60:344–351

    Article  CAS  Google Scholar 

  • Kong WW, Zhang LP, Guo K, Lui ZP, Yang ZM (2010) Carbon monoxide improves adaptation of Arabidopsis to iron deficiency. Plant Biotech J 8:88–99

    Article  CAS  Google Scholar 

  • Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017

    Article  CAS  Google Scholar 

  • Korkmaz A (2005) Inclusion of acetyl salicylic acid and methyl jasmonate into the priming solution improves low temperature germination and emergence of sweet pepper seeds. HortSci 40:197–200

    CAS  Google Scholar 

  • Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187

    Article  CAS  Google Scholar 

  • Lee GY, Jang DS, Lee YM, Kim JM, Kim JS (2006) Naphthopyrone glucosides from the seeds of Cassia tora with inhibitory activity on advanced glycation end products (AGEs) formation. Arch Pharm Res 29:587–590

    Article  PubMed  CAS  Google Scholar 

  • Liau YJ, Wen L, Shaw JF, Lin CT (2007) A highly stable cambialistic-superoxide dismutase from Antrodia camphorata: Expression in yeast and enzyme properties. J Biotechnol 131:84–91

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomemranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu KL, Xu S, Xuan W, Ling TF, Cao ZY, Huang BK, Sun YG, Fang L, Liu ZY, Zhao N, Shen WB (2007) Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa. Plant Sci 172:544–555

    Article  CAS  Google Scholar 

  • Maines MD, Trakshel GM, Kutty RK (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 261:411–419

    PubMed  CAS  Google Scholar 

  • Malash NM, Flowers TJ, Ragab R (2007) Effect of irrigation methods, management and salinity of irrigation water on tomato yield, soil moisture and salinity distribution. Plant Soil 26:313–323

    Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • McCoubrey WK, Huang TJ, Maines MD (1997) Isolation and characterization of a cDNA from rat brain that encodes hemoprotein heme oxygenase-3. Eur J Biochem 247:725–732

    Article  PubMed  CAS  Google Scholar 

  • McDonald MB (1999) Seed deterioration: physiology, repair and assessment. Seed Sci Technol 27:177–237

    Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2002) Salt stress induces upregulation of an efficient chloroplast antioxidant system in the salt-tolerant wild tomato species Lycopersicon pennellii but not in the cultivated species. Physiol Plant 115:393–400

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Muramoto T, Kohchi T, Yokota A, Hwang I, Goodman HM (1999) The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 11:335–348

    PubMed  CAS  Google Scholar 

  • Muramoto T, Tsurui N, Terry MJ, Yokota A, Kohchi T (2002) Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis. Plant Physiol 130:1958–1966

    Article  PubMed  CAS  Google Scholar 

  • Murkherje SP, Choudhuri MA (1983) Implication of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogenperoxide in Vigna seedlings. Physiol Plant 58:166–170

    Article  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbatespecific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  PubMed  CAS  Google Scholar 

  • Noriega GO, Balestrasse KB, Batlle A, Tomaro ML (2004) Heme oxygenase exerts a protective role against oxidative stress in soybean leaves. Biochem Biophys Res Commun 323:1003–1008

    Article  PubMed  CAS  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  PubMed  CAS  Google Scholar 

  • Roychoudhury A, Roy C, Sengupta DN (2007) Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep 26:1839–1859

    Article  PubMed  CAS  Google Scholar 

  • Rozema J, Flowers T (2008) Crops for a Salinized World. Science 322:1478–1480

    Article  PubMed  CAS  Google Scholar 

  • Sairam RK (1994) Effect of moisture stress on physiological activities of two contrasting wheat genotypes. Indian J Exp Biol 32:584–593

    Google Scholar 

  • Sairam RK, Desmukh PS, Saxena C (1998) Role of antioxidant systems in wheat genotypes tolerant to water stress. Biol Plant 41:387–394

    Article  CAS  Google Scholar 

  • Salin ML (1988) Toxic oxygen species and protective systems of the chloroplast. Physiol Plant 72:681–689

    Article  CAS  Google Scholar 

  • Sayed OH (2003) Chlorophyll fluorescence as a tool in cereal research. Photosynthetica 41:321–330

    Article  CAS  Google Scholar 

  • Smirnoff N, Cumbes QT (1989) Hydroxyl radicals scavenging activity of compatible isolates. Phytochemisiry 28:1057–1060

    Article  CAS  Google Scholar 

  • Song XG, She XP, Zhang B (2008) Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis. Physiol Plant 132:514–525

    Article  PubMed  CAS  Google Scholar 

  • Storey R, Wyn-Jones RG (1975) Betaine and choline levels in plnats and their relationship to NaCl stress. Plant Sci Lett 4:161–168

    Article  CAS  Google Scholar 

  • Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natil Acad Sci USA 61:748–755

    Article  CAS  Google Scholar 

  • Van-Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosyn Res 25:147–150

    Article  Google Scholar 

  • Wahid A, Parveen M, Gelani S, Basra SMA (2007) Pretreatment of seeds with H2O2 improves salt tolerance of wheat seedling by alleviation of oxidative damage and expression of stress proteins. J Plant Physiol 164:283–294

    Article  PubMed  CAS  Google Scholar 

  • Xu CC, Zhang JH (1999) Effect of drought on chlorophyll fluorescence and xanthophyll cycle components in winter wheat leaves with different ages. Acta Phytophysiologica Sinica 25:29–37

    Google Scholar 

  • Xu S, Sa ZS, Cao ZY, Xuan W, Huang BK, Ling TF, Hu QY, Shen WB (2006) Carbon monoxide alleviates wheat seed germination inhibition and counteracts lipid peroxidation mediated by salinity. J Integr Plant Biol 48:1168–1176

    Article  CAS  Google Scholar 

  • Xu PL, Guo YK, Bai JG, Shang L, Wang XJ (2008) Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. Physiol Plant 132:467–478

    Article  PubMed  CAS  Google Scholar 

  • Xuan W, Zhu FY, Xu S, Huang BK, Ling TF, Qi JY (2008) The heme oxygenase/carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process. Plant Physiol 148:881–893

    Article  PubMed  CAS  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    PubMed  CAS  Google Scholar 

  • Yoshida T, Kikuchi G (1974) Partial purification and reconstitution of the heme oxygenase system from pig spleen microsomes. Biochem J 75:1187–1191

    CAS  Google Scholar 

  • Zhang SR (1999) A discussion on chlorophyll fluorescence kinetics parameters and their significance. Chinese Bulletin of Botany 16:444–448

    Google Scholar 

  • Zhang H, Shen WB, Xu LL (2003) Effects of nitric oxide on the germination of wheat seeds and its reactive oxygen species metabolism under osmotic stress. Acta Bot Sin 45:901–905

    CAS  Google Scholar 

  • Zhang C, Li GL, Xiao YQ, Li L, Pang Z (2009) Two new glycosides from the seeds of Cassia obtusifolia. Chin Chemical Lett 20:1097–1099

    Article  CAS  Google Scholar 

  • Zheng CF, Jiang D, Liu FL, Dai TB, Liu WC, Jing Q, Cao WX (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67:222–227

    Article  CAS  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge the National Natural Science Foundation of China for their financial support (Grant Nos. 30560025 and 31060069).

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Correspondence to Ping He.

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Zhang, C., Li, Y., Yuan, F. et al. Effects of hematin and carbon monoxide on the salinity stress responses of Cassia obtusifolia L. seeds and seedlings. Plant Soil 359, 85–105 (2012). https://doi.org/10.1007/s11104-012-1194-7

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