Please wait a minute...
Journal of Integrative Agriculture  2018, Vol. 17 Issue (04): 826-836    DOI: 10.1016/S2095-3119(17)61717-9
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Enzymatic activity and chlorophyll fluorescence imaging of maize seedlings (Zea mays L.) after exposure to low doses of chlorsulfuron and cadmium
ZHAO Li-juan1, 2, XIE Jing-fang1, ZHANG Hong3, WANG Zhen-tao1, JIANG Hong-jin1, GAO Shao-long1
1 College of Environment and Resource, Shanxi University, Taiyuan 030006, P.R.China
2 Department of Biology, Xinzhou Teachers University, Xinzhou 034000. P.R.China
3 Shanxi Academy of Analytical Science, Taiyuan 030006, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  The aim of this research was to study the influence of chlorsulfuron residue and cadmium on the enzymatic activity and photosynthetic apparatus of maize (Zea mays L.) plants.  Chlorsulfuron and cadmium at 0.001 and 5.0 mg kg–1, respectively, were mixed and applied to soil prior to planting.  The levels of chlorsulfuron- and cadmium-induced stress to plants were estimated by growth, chlorophyll content, lipid peroxide content, enzyme activities, and major fluorescence parameters of chlorophyll (revealed by the fluorescence imaging system FluorCam).  Chlorsulfuron negatively affected the chlorophyll content, photochemical efficiency of photosystem II in the dark-adapted state, the maximum efficiency of photosystem II, photochemical quenching coefficient, and steady-state fluorescence decline ratio in the leaves of maize seedlings.  However, cadmium did not produce noticeable changes.  Plants that were exposed to both chlorsulfuron and cadmium showed an obvious increase in the steady-state fluorescence decline ratio.  These results implied that the seedlings possessed more resistance to cadmium than to chlorsulfuron and their resistance to chlorsulfuron toxicity was enhanced by the presence of cadmium.  The results also suggested that chlorophyll fluorescence imaging reveals overall alterations within the leaves but may not reflect small-scale effects on tissues, as numeric values of specific parameters are averages of the data collected from the whole leaf.
Keywords:  major parameters of Chl fluorescence imaging        germination        growth        metals        sulfonylurea herbicides  
Received: 30 March 2017   Accepted:
Fund: 

This research was supported by grants from the National Natural Science Foundation of China (30740037), the Special Fund for Agro-scientific Research in the Public Interest, China (201103024), and the Foundation for Graduate Innovation, Shanxi University, China (011452901009).

Corresponding Authors:  Correspondence XIE Jing-fang, Tel/Fax: +86-351-7018807, E-mail: xiejf@sxu.edu.cn   
About author:  ZHAO Li-juan, E-mail: zhaolijuan6286145@tom.com;

Cite this article: 

ZHAO Li-juan, XIE Jing-fang, ZHANG Hong, WANG Zhen-tao, JIANG Hong-jin, GAO Shao-long . 2018. Enzymatic activity and chlorophyll fluorescence imaging of maize seedlings (Zea mays L.) after exposure to low doses of chlorsulfuron and cadmium. Journal of Integrative Agriculture, 17(04): 826-836.

Ahmad I, Naeem M, Khan N A, Samiullah. 2009. Effects of cadmium stress upon activities of antioxidative enzymes, photosynthetic rate, and production of phytochelatins in leaves and chloroplasts of wheat cultivars differing in yield potential. Photosynthetica, 47, 146–151.

AL-Quraan N A, Ghunaim A I, Alkhatib R Q. 2015, The influence of chlorsulfuron herbicide on GABA metabolism and oxidative damage in lentil (Lens culinaris Medik) and wheat (Triticum aestivum L.) seedlings. Acta Physiologiae Plantarum, 37, 227.

Antonkiewicz J, Jasiewicz C, Lošak T. 2006. Using Virginia fanpetals for extraction of heavy metals from soil. Acta Scientiarum Polonorum, 5, 63–73. (in Polish)

Baczek-Kwinta R, Bartoszek A, Kusznierewicz B, Antonkiewicz J. 2011a. Physiological response of plants and cadmium accumulation in heads of two cultivars of white cabbage. Journal of Elementology, 16, 355–364.

Baczek-kwinta R, Koziel A, Seidler-Lozykowska K. 2011b. Are the fluorescence parameters of German chamomile leaves the first indicators of the anthodia field in drought conditions? Photosynthetica, 49, 87–97.

Barbagallo R P, Oxborough K, Pallett K E, Baker N R. 2003. Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiology, 132, 485–493.

Basi S, Noga G, Hunsche M. 2013. Relevance of the deposit structure for the uptake and bioefficacy of diquat, as monitored by the spatially resolved chlorophyll fluorescence. Pesticide Biochemistry and Physiology, 107, 218–225.

Borek M, B?czek-Kwinta R, Rapacz M. 2013. Chlorophyll fluorescence imaging of cadmium-treated white cabbage plants. In: Proceedings of the16th International Conference on Heavy Metals in the Environment. Rome, Italy. pp. 1–4.

Brown H M, Kearney P C. 1991. Plant biochemistry, environmental properties, and global impact of sulfonylurea herbicides. American Chemical Society Symposium Series, 22, 32–49.

Chen D W, Shao S N, Chen R D, Yang C H.  1994. Chlorsulfuron residue dynamics in wheat field. Agricultural Environmental Protection, 13, 140–141.

Chen X, Wang J, Shi Y, Zhao M Q, Chi G Y. 2011. Effects of cadmium on growth and photosynthetic activities in pakchoi and mustard. Botanical Studies, 52, 41–46.

Cui J, Zhang R, Wu G L, Zhu H M, Yang H. 2010. Salicylic acid reduces napropamide toxicity by preventing its accumulation in rapeseed (Brassica napus L.). Archives of Environmental Contamination and Toxicology, 59, 100–108.

Day T A, Howells B W, Ruhl C T. 1996. Changes in growth and pigment concentrations with leaf age in pea under modulated UV-B radiation field treatments. Plant Cell and Environment, 19, 101–108.

Demmig-Adams B, Adams III W W, Logan B A, Verhoeven A S. 1995. Xanthophyll-cycle-dependent energy dissipation and flexible photosystem II efficiency in plants acclimated to light stress. Australian Journal of Plant Physiology, 22, 249–260.

Dezhban A, Shirvany A, Attarod P, Delshad M, Matinizadeh M, Khoshnevis M. 2015. Cadmium and lead effects on chlorophyll fluorescence, chlorophyll pigments and proline of Robinia pseudoacacia. Journal of  Forestry Research, 26, 323–329.

Edwards R, Dixon D P, Walbot V. 2000. Plant glutathione-S-transferases: Enzymes with multiple functions in sickness and in health. Trends in Plant Science, 5, 193–198.

Haouari C C, Nasraoui A H, Bouthour D, Houda M D, Daieb C B, Mnai J, Gouia H. 2012. Response of tomato (Solanum lycopersicon) to cadmium toxicity: Growth, element uptake, chlorophyll content and photosynthetic rate. African Journal of Plant Science, 6, 1–7.

Fayeaz K A, Kristen U. 1996. The influence of herbicides on the growths and proline content of primary roots and on the ultra structure of root caps. Environmental and Experimental Botany, 36, 71–81.

Frahry G, Schopfer P. 2001. NADH-stimulated, cyanide-resistant superoxide production in maize coleoptiles analyzed with a tetrazolium-based assay. Planta, 212, 175–183.

Frankart C, Eullaffroy P, Vernet G. 2003. Comparative effects of four herbicides on non-photochemical fluorescence quenching in Lemna minor. Environmental & Experimental Botany, 49, 159–168.

Guisandecollazo A, González L, Souzaalonso P. 2016. Impact of an invasive nitrogen-fixing tree on arbuscular mycorrhizal fungi and the development of native species. AoB Plants, 8, 1–11.

Hegedus A, Erdei S, Horvath G. 2001. Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress. Plant Science, 160, 1085–1093.

Hollaway K L, Kookana R S, Noy D M, Smith J G ,Wilhelm N. 2006. Persistence and leaching of sulfonylurea herbicides over a 4-year period in the highly alkaline soils of south-eastern Australia. Australian Journal of Experimental Agriculture, 46, 1069–1076.

Horton P, Hague A. 1984. Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. IV. Resolution of non-photochemical quenching. Biochimical et Biophysica Acta-Bioenergetics, 849, 1–6.

Hussain M I, Reigosa M J. 2015. Characterization of xanthophyll pigments, photosynthetic performance, photon energy dissipation, reactive oxygen species generation and carbon Isotope discrimination during artemisinin-induced stress in Arabidopsis thaliana. PLoS ONE, 10, e0114826.

ISO Soil Quality. 2013. Determination of the effects of pollutants on soil flora-Part 2: Effects of contaminated soil on the emergence and early growth of higher plants. BS EN ISO 11269–2:2013, International Organization for Standardization.

Jiang L, Ma L, Sui Y, Han S Q, Wu Z Y, Feng Y X. 2010. Effect of manure compost on the herbicide prometryne bioavailability to wheat plants. Journal of Hazardous Materials, 184, 337–344.

Juneau P, Qiu B, Deblois C P. 2007. Use of chlorophyll fluorescence as a tool for determination of herbicide toxic effect: Review. Toxicological and Environmental Chemistry, 89, 609–625.

Krause G H, Vernotte C, Briantais J M. 1982. Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Biochimical et Biophysica Acta-Bioenergetics, 679, 116–124.

Li H S. 2001. Principles and Techniques of Plant Physiology and Biochemistry Experiment. Higher Education Press, China. pp. 160–170. (in Chinese)

Li J Z, Chen Y P, Teng K Q. 2015. Rice leaf heterogeneity in chlorophyll fluorescence parameters under short-term osmotic stress. Biologia Plantarum, 59, 187–192.

Lichtenehaler H K, Babani F, Langsdorf G, Buschmann C. 2000. Measurement of differences in red chlorophyll fluorescence and photosynthetic activity between sun and shade leaves by fluorescence imaging. Photosynthetica, 38, 521–529.

Lichtenehaler H K, Mieh? J A 1997. Fluorescence imaging as a diagnostic tool for plant stress. Trends in Plant Science, 2, 316–320.

Luo H Y, Gao H B, Xia Q P. 2011. Effects of exogenous GABA on reactive oxygen species metabolism and chlorophyll fluorescence parameters in tomato seedlings under NaCl stress. Journal of Agricultural University of Hebei, 34, 37–40. (in Chinese)

Ma S C, Zhang H B, Ma S T. 2015. Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties, heavy metal uptake and grain yield in winter wheat. Ecotoxicology and Environmental Safety, 113, 483–490.

Martínez-Peñalver A, Reigosa M J, Sánchez-Moreiras A M. 2011. Imaging chlorophyll a fluorescence reveals specific spatial distributions under different stress conditions. Flora, 206, 836–844.

Maxwell K, Johnson G N 2000. Chlorophyll fluorescence - A practical guide. Journal of Experimental Botany, 51, 659–668.

Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 405–410.

Moustaka J, Moustakas M. 2014, Photoprotective mechanism of the non-target organism Arabidopsis thaliana to paraquat exposure. Pesticide Biochemistry and Physiology, 111, 1–6.

Moustaka J, Tanou G, Adamakis I D, Eleftheriou E P, Moustakas M. 2015. Leaf age-dependent photoprotective and antioxidative mechanisms to paraquat-induced oxidative stress in Arabidopsis thaliana. International Journal of Molecular Sciences, 16, 13989–14006.

Muniz C R, Freire F C O, Viana F M P. 2014. Monitoring cashew seedlings during interactions with the fungus Lasiodiplodia theobromae using chlorophyll fluorescence imaging. Photosynthetica, 52, 529–537.

Murzaeva S V. 2004. Effect of heavy metals on wheat seedlings: Activation of antioxidant enzymes. Applied Biochemistry and Microbiology, 40, 98–113.

Müller P, Li X P, Niyog K K. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology, 125, 1558–1566.

Nestler H, Groh K J, Schönenberger R, Behra R, Schirmer K, Eggen R I L, Suter M J F. 2012. Multiple-endpoint assay provides a detailed mechanistic view of responses to herbicide exposure in Chlamydomonas reinhardtii. Aquatic Toxicology, 110–111, 214–224.

Pagliano C, Raviolo M, Vecchia F D, Gabbrielli R, Gonnelli C, Rascio N, Barbato R, Rocca N L. 2006. Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.). Journal of Photochemistry and Photobiology (B: Biology), 84, 70–78.

Papageorgiou G C, Govindjee (eds.). 2004. Chlorophyll a Fluorescence: A Signatureof Photosynthesis. Springer, Dordrecht.

Peng M, Wang H X, Wu Y S. 1991. Changes in cell ultrastructure of Zea mays L. seedlings induced by cadmium and lead. China Environmental Science, 11, 426–431.

Porra R J, Thompson R A, Kriedemann P E. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvent verifications of the concentration of chlorophyll standards by atomic absorption spectroscopy.  Biochimical et Biophysica Acta-Bioenergetics, 975, 384–394.

Ralph P J, Burchett M D. 1998. Photosynthetic response of Halophila ovalis to heavy metal stress. Environmental Pollution, 103, 91–101.

Ralph P J, Smith R A, Macinnis-Ng C M O, Seery C R. 2007. Use of fluorescence-based ecotoxicological bioassays inmonitoring toxicants and pollution in aquatic systems: Review. Environmental Toxicology and Chemistry, 89, 589–607.

Rey-Caballero J, Menendez J, Osuna M D, Marisa S, Joel T. 2017. Target-site and non-target-site resistance mechanisms to ALS inhibiting herbicides in Papaver rhoeas. Pesticide Biochemistry and Physiology, 138, 57–65.

Rohá?ek K, Soukupová J, Barták M. 2008. Chlorophyll fluorescence: A wonderful tool to study plant physiology and plant stress. Plant Cell Compartments - Selected Topics. Research Signpost, Kerala, India. pp. 41–51.

Sarmah A K, Kookana R S, Alston A M. 1998. Fate and behaviour of triasulfuron, metsulfuron-methyl, and chlorsulfuron in the Australian soil environment: A review. Australian Journal of Agricultural Research, 49, 775–790.

Scandalio J G. 2005. Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian Journal of Medical and Biological Research, 38, 995–1014.

Schreiber U, Klughammer C. 2008. Non-photochemical fluorescence quenching and quantum yields in PS I and PS II: Analysis of heat-induced limitations using Maxi-Imaging PAM and Dual-PAM-100. PAM Application Notes, 1, 15–18.

Shafi T M, Agnihotri R K. 2010. Chlorophyll and proline content of gram (Cicer arietinum L.) under cadmium and mercury treatments. Research Journal of Agricultural Sciences, 1, 119–122.

Shan Z J, Cai D J. 1998. Study on the residues of chlorsulfuron in wheat and soil. Pesticides, 36, 27–29.

Sofo A, Dichio B, Montanaro G, Xiloyannis C. 2009. Photosynthetic performance and light response of two olive cultivars under different water and light regimes. Photosynthetica, 47, 602–608.

Stork P R. 1995. Field leaching and degradation of soil applied herbicides in a gradationally textured alkaline soil: Chlorsulfuron and triasulfuron. Australian Journal of Agricultural Research, 46, 1445–1458.

Su J W, Wang X P. 2004. Effect of cadmiumions on photosynthetic structure and its functions of tea leaves. Tea Science, 24, 65–69. (in Chinese)

Sun Y Y, Xu L L, Feng X D, Guan P. 2015. Biomass, cadmium accumulation and chlorophyll fluorescence parameters response of Ageratum conyzoides to different concentrations of cadmium stress. Guihaia, 35, 679–684.

Wilson P C, Whitwell T, Klaine S J. 2000. Phytotoxicity, uptake, and distribution of C-14-simazine in Acorus gramenius and Pontederia cordata. Weed Science, 48, 701–709.

Wu G L, Cui J, Tao L,Yang H. 2010. Fluroxypyr triggers oxidative damage by producing superoxide and hydrogen peroxide in rice (Oryza sativa). Ecotoxicology, 19, 124–132.

Yan L L, Lu L. 2013. Joint ecotoxicology of cadmium and metsulfuron-methyl in wheat (Triticum aestivum). Environmental Monitoring and Assessment, 185, 2939–2950.

Yin X L, Jiang L, Song N H, Yang H. 2008. Toxic reactivity of wheat (Triticum aestivum) plants to herbicide isoproturon. Journal of Agricultural and Food Chemistry, 56, 4825–4831.

Zhao L J, Xie J F, Zhang H, Wang Z T, Fan R J, Lü J L, Zhang M. 2016. Changes in metabolites in maize seedlings under chlorsulfuron and cadmium stress. The Journal of Agricultural Science, 154, 890–913.

Zhou Z S, Guo K, Elbaz A A, Yang Z M. 2009. Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environmental and Experimental Botany, 65, 27–34.

Zhou Z S, Huang S J, Yang Z M. 2008. Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere, 70, 1500–1509.
[1] WANG Li-xin, WANG Lin-xia, ZHANG Meng-ling, QU Ying-yue, YUAN Ye, Ehsan SADEGHNEZHAD, GAO Meng-jiao, ZHAO Ruo-yu, QI Chao-feng, GUO Xiao-xue, ZHU Wen-hui, LI Rui-mei, DAI Li, LIU Meng-jun, LIU Zhi-guo. A cyclic effect of cAMP and calcium signaling contributes to jujube growth and development[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2094-2110.
[2] XIE Jiao, CAO Qi, WANG Wen-jun, ZHANG Hong-yan, DENG Bing. Understanding changes in volatile compounds and fatty acids of Jincheng orange peel oil at different growth stages using GC–MS[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2282-2294.
[3] REN Chuan-ying, LU Shu-wen, GUAN Li-jun, HONG Bin, ZHANG Ying-lei, HUANG Wen-gong, LI Bo, LIU Wei, LU Wei-hong.

The metabolomics variations among rice, brown rice, wet germinated brown rice, and processed wet germinated brown rice [J]. >Journal of Integrative Agriculture, 2022, 21(9): 2767-2776.

[4] LI Si-ping, ZENG Lu-sheng, SU Zhong-liang. Wheat growth, photosynthesis and physiological characteristics under different soil Zn levels[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1927-1940.
[5] ZHOU Nian-bing, ZHANG jun, FANG Shu-liang, WEI Hai-yan, ZHANG Hong-cheng. Effects of temperature and solar radiation on yield of good eating-quality rice in the lower reaches of the Huai River Basin, China[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1762-1774.
[6] WU Fan-lin, QU De-hui, TIAN Wei, WANG Meng-yun, CHEN Fei-yan, LI Ke-ke, SUN Ya-dong, SU Ying-hua, YANG Li-na, SU Hong-yan, WANG Lei. Transcriptome analysis for understanding the mechanism of dark septate endophyte S16 in promoting the growth and nitrate uptake of sweet cherry[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1819-1831.
[7] ZHANG Zhe, CHEN Zi-tao, DIAO Shu-qi, YE Shao-pan, WANG Jia-ying, GAO Ning, YUAN Xiao-long, CHEN Zan-mou, ZHANG Hao, LI Jia-qi. Identifying the complex genetic architecture of growth and fatness traits in a Duroc pig population[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1607-1614.
[8] GONG Xiao-dong, LIU Yu-wei, BI Huan-huan, YANG Xiao-rong, HAN Jian-min, DONG Jin-gao, GU Shou-qin. StKU80, a component in the NHEJ repair pathway, is involved in mycelial morphogenesis, conidiation, appressorium development, and oxidative stress reactions in Exserohilum turcicum[J]. >Journal of Integrative Agriculture, 2021, 20(1): 147-158.
[9] WANG Chuan-long, XING Guan-zhong, WANG Li-sai, LI Su-fen, ZHANG Li-yang, LU Lin, LUO Xu-gang, LIAO Xiu-dong . Effects of selenium source and level on growth performance, antioxidative ability and meat quality of broilers[J]. >Journal of Integrative Agriculture, 2021, 20(1): 227-235.
[10] ZHANG Yong-sheng, LU Dan, LIU Yu-wen, YI Guo-qiang, TANG Zhong-lin . The untold story between enhancers and skeletal muscle development[J]. >Journal of Integrative Agriculture, 2020, 19(9): 2137-2149.
[11] LI Yu-xiang, LIU Yang, WANG Yu-hui, DING Yan-feng, WANG Shao-hua, LIU Zheng-hui, LI Gang-hua. Effects of seedling age on the growth stage and yield formation of hydroponically grown long-mat rice seedlings[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1755-1767.
[12] ZHU Shi-ping, HUANG Tao-jiang, YU Xin, HONG Qi-bin, XIANG Jin-song, ZENG An-zhong, GONG Gui-zhi, ZHAO Xiao-chun. The effects of rootstocks on performances of three late-ripening navel orange varieties[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1802-1812.
[13] LIU Guo-qing, SUN Guang-ming, LIAO Xiu-dong, HUANG Jian-zhong, GUO Mei-jin, ZHANG Li-yang, GUO Yan-li, LU Lin, LUO Xu-gang. Effect of dietary supplementation of pyrroloquinoline quinone disodium on growth performance, meat quality and antioxidative ability of broilers[J]. >Journal of Integrative Agriculture, 2020, 19(7): 1850-1856.
[14] ZHANG Zhen, LIU Qiang, WANG Cong, GUO Gang, HUO Wen-jie, ZHANG Yan-li, PEI Cai-xia, ZHANG Shuan-lin. Effects of palm fat powder and coated folic acid on growth performance, ruminal fermentation, nutrient digestibility and hepatic fat accumulation of Holstein dairy bulls[J]. >Journal of Integrative Agriculture, 2020, 19(4): 1074-1084.
[15] BAI Tie-cheng, WANG Tao, ZHANG Nan-nan, CHEN You-qi, Benoit MERCATORIS. Growth simulation and yield prediction for perennial jujube fruit tree by integrating age into the WOFOST model[J]. >Journal of Integrative Agriculture, 2020, 19(3): 721-734.
No Suggested Reading articles found!