Uptake of Cd2+ by ectomycorrhizal fungus Paxillus involutus and the modulation of H2O2 in Cd2+ influx

Zhu Zhimei; Zhang Yuhong; Sa Gang; Liu Jian; Ma Xujun; Deng Chen; Zhao Rui; Chen Shaoliang

doi:10.13332/j.1000-1522.20170418

Journal of Beijing Forestry University > 2018 > 40(4): 24-32. > DOI: 10.13332/j.1000-1522.20170418

Zhu Zhimei, Zhang Yuhong, Sa Gang, Liu Jian, Ma Xujun, Deng Chen, Zhao Rui, Chen Shaoliang. Uptake of Cd²⁺ by ectomycorrhizal fungus Paxillus involutus and the modulation of H₂O₂ in Cd²⁺ influx[J]. Journal of Beijing Forestry University, 2018, 40(4): 24-32. DOI: 10.13332/j.1000-1522.20170418

Citation:

PDF (6234 KB)

Uptake of Cd²⁺ by ectomycorrhizal fungus Paxillus involutus and the modulation of H₂O₂ in Cd²⁺ influx

College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China

More Information

Received Date: November 26, 2017
Revised Date: January 30, 2018
Published Date: March 31, 2018

Graphical Abstract

Abstract

Abstract

ObjectiveThe uptake of Cd²⁺ by ectomycorrhizal fungus Paxillus involutus and the modulation of H₂O₂ in Cd²⁺ influx were investigated in this study.
Method Two Paxillus involutus strains, MAJ and NAU, were subjected to 50 μmol/L CdCl₂ for 24 hours, and then fluxes of Ca²⁺ and Cd²⁺ were examined by non-invasive micro-test technique.
Result The results showed that Cd²⁺ treatment caused the Cd²⁺ influx, and the Ca²⁺ influx was also significantly enhanced by Cd²⁺ in MAJ and NAU hyphae. However, the Cd²⁺-elicited influxes of Cd²⁺ and Ca²⁺ were both restricted by Ca²⁺ channel inhibitors including Verapamil, GdCl₃, TEA (Tetraethylammonium), indicating that Cd²⁺ and Ca²⁺ simultaneously entered the hyphal cell through plasma membrane (PM) Ca²⁺-permeable channels (CaPCs). The promotion of Ca²⁺ by Cd²⁺ implied that Cd²⁺ activated CaPCs, thus leading to an increased entry of Ca²⁺, in addition to Cd²⁺. Moreover competitive inhibition experiments were also conducted to verify whether Cd²⁺ and Ca²⁺ entered into the mycelium through CaPCs in the PM. The influx of Cd²⁺ in MAJ and NAU was lowered by increased concentration of Ca²⁺, and vice versa. Therefore, Cd²⁺ and Ca²⁺ competitively permeated the plasma membrane through Ca²⁺-permeable channels. Additionally, the influxes of Ca²⁺ and Cd²⁺ in mycelium were enhanced by 1 mmol/L H₂O₂ while suppressed by the ROS scavenger, DMTU (N, N′-Dimethylthiourea). This indicated that H₂O₂ could mediate the entry of Cd²⁺ through PM Ca²⁺-permeable channels in fungal hyphae.
Conclusion In conclusion, the ectomycorrhizal fungus Paxillus involutus has the ability of Cd²⁺ enrichment and the influx of Cd²⁺ can be facilitated through CaPCs activated by H₂O₂.
- Paxillus involutus,
- MAJ,
- NAU,
- cadmium stress,
- CaPCs,
- non-invasive micro-test technique,
- ion flux

FullText(HTML)

References (33)

References

[1]	卢红玲, 肖光辉, 刘青山, 等.土壤污染现状及其治理措施研究进展[J].南方农业学报, 2014, 45(11): 1986-1993. http://d.old.wanfangdata.com.cn/Periodical/gxnykx201411015 Lu H L, Xiao G H, Liu Q S, et al. Advances in soil Cd pollution and solution measures[J]. Journal of Southern Agriculture, 2014, 45(11):1986-1993. http://d.old.wanfangdata.com.cn/Periodical/gxnykx201411015
[2]	Ott T, Fritz E, Polle A, et al. Characterisation of antioxidative systems in the ectomycorrhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium[J]. Fems Microbiology Ecology, 2002, 42(3):359-366. doi: 10.1111/fem.2002.42.issue-3
[3]	Verbruggen N, Hermans C, Schat H. Mechanisms to cope with arsenic or cadmium excess in plants[J]. Current Opinion in Plant Biology, 2009, 12(3):364-372. doi: 10.1016/j.pbi.2009.05.001
[4]	Krämer U. Metal hyperaccumulation in plants[J]. Annual Review of Plant Biology, 2010, 61(2):517. http://d.old.wanfangdata.com.cn/OAPaper/oai_pubmedcentral.nih.gov_527178
[5]	Prozialeck W C, Edwards J R, Woods J M. The vascular endothelium as a target of cadmium toxicit[J]. Life Sciences, 2006, 79(16) : 1493-1506. doi: 10.1016/j.lfs.2006.05.007
[6]	张强, 刘斌, 刘巍, 等.污染土壤的生物修复治理技术研究进展[J].生物技术通报, 2014(10):56-63. http://d.old.wanfangdata.com.cn/Periodical/swjstb201410008 Zhang Q, Liu B, Liu W, et al. The biological remediation technology for the contaminated soil[J]. Biotechnology Bulletin, 2014(10):56-63. http://d.old.wanfangdata.com.cn/Periodical/swjstb201410008
[7]	陈保冬, 孙玉青, 张莘, 等.菌根真菌重金属耐性机制研究进展[J].环境科学, 2015, 36(3):1123-1132. http://d.old.wanfangdata.com.cn/Periodical/hjkx201503054 Chen B D, Sun Y Q, Zhang X, et al. Underlying mechanisms of the heavy metal tolerance of mycorrhizal fungi[J]. Environmental Science, 2015, 36(3): 1123-1132. http://d.old.wanfangdata.com.cn/Periodical/hjkx201503054
[8]	Colpaert J V, Assche J A V. The effects of cadmium on ectomycorrhizal Pinus sylvestris L.[J]. New Phytologist, 1993, 123: 325-333. doi: 10.1111/nph.1993.123.issue-2
[9]	Miransari M. Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals[J]. Biotechnology Advances, 2011, 29: 645-653. doi: 10.1016/j.biotechadv.2011.04.006
[10]	Khullar S, Reddy M S. Ectomycorrhizal fungi and its role in metal homeostasis through metallothionein and glutathione mechanisms[J]. Current Biotechnology, 2016, 5(3):1-11.
[11]	马永禄.外生菌根真菌Paxillus involutus提高灰杨(Populus×canescens)对重金属Cd的吸收和耐受能力[D].陕西杨凌: 西北农林科技大学, 2013. Ma Y L. Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populous×canesccens[D]. Shaanxi Yangling: North West Agriculture and Forestry University, 2013.
[12]	Blaudez D, Botton B, Chalot M. Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus[J]. Microbiology, 2000, 146: 1109-1117. doi: 10.1099/00221287-146-5-1109
[13]	González-guerrero M, Melville L H, Ferrol N, et al. Ultrastructural localization of heavy metals in the extraradical mycelium and spores of the arbuscular mycorrhizal fungus Glomus intraradices[J]. Canadian Journal of Microbiology, 2008, 54: 103-110. doi: 10.1139/W07-119
[14]	Ovečka M, Takáč T. Managing heavy metal toxicity stress in plants: biological and biotechnological tools[J]. Biotechnology Advances, 2014, 32: 73-86. doi: 10.1016/j.biotechadv.2013.11.011
[15]	Luo Z B, He J L, Polle A, et al. Heavy metal accumulation and signal transduction in herbaceous and woody plants: paving the way for enhancing phytoremediation efficiency[J]. Biotechnology Advances, 2016, 34: 1131-1148. doi: 10.1016/j.biotechadv.2016.07.003
[16]	Liu X F, Supek F, Nelson N, et al. Negative control of heavy metal uptake by the Saccharomyces cerevisiae BSD2 gene[J]. Journal of Biological Chemistry, 1997, 272: 11763-11769. doi: 10.1074/jbc.272.18.11763
[17]	Clemens S, Antosiewicz D M, Ward J M, et al. The plant cDNA LCT1 mediates the uptake of calcium and cadmium in yeast[J]. Proceedings of the National Academy of Sciences, 1998, 95: 12043-12048. doi: 10.1073/pnas.95.20.12043
[18]	Hirschi K D, Korenkov V D, Wilganowski N L, et al. Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance[J]. Plant Physiology, 2000, 124: 125-134. doi: 10.1104/pp.124.1.125
[19]	Zhao F J, Hamon R E, Lombi E, et al. Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens[J]. Journal of Experimental Botany, 2002, 53: 535-543. doi: 10.1093/jexbot/53.368.535
[20]	Sun J, Wang R G, Zhang X, et al. Hydrogen sulfide alleviates cadmium toxicity through regulations of cadmium transport across the plasma and vacuolar membranes in Populus euphratica cells[J]. Plant Physiology and Biochemistry, 2013, 65: 67-74. doi: 10.1016/j.plaphy.2013.01.003
[21]	He J L, Li H, Ma C F, et al. Overexpression of bacterial γ-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar[J]. New Phytologist, 2015, 205: 240-254. doi: 10.1111/nph.13013
[22]	Perfus-barbeoch L, Leonhardt N, Vavasseur A, et al. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status[J]. The Plant Journal, 2002, 32: 539-548. doi: 10.1046/j.1365-313X.2002.01442.x
[23]	Gallego S M, Pena L B, Barcia R A, et al. Unravelling cadmium toxicity and tolerance in plants: insight into regulatory mechanisms[J]. Environmental and Experimental Botany, 2012, 83: 33-46. doi: 10.1016/j.envexpbot.2012.04.006
[24]	Li L Z, Liu X L, You L P, et al. Uptake pathways and subcellular fractionation of Cd in the polychaete Nereis diversicolor[J]. Ecotoxicology, 2012, 21(1): 104-110. doi: 10.1007/s10646-011-0770-6
[25]	向敏, 孙会敏, 王少杰, 等. NaCl对泌盐红树和非泌盐红树Cd吸收和积累的影响[J].北京林业大学学报, 2016, 38(8): 10-17. doi: 10.13332/j.1000-1522.20160079 Xiang M, Sun H M, Wang S J, et al. Effects of NaCl on cadmium uptake, accumulate in secretor and non-secretor mangrove species[J]. Journal of Beijing Forestry University, 2016, 38(8): 10-17. doi: 10.13332/j.1000-1522.20160079
[26]	Li L Z, Liu X L, Peijnenburg W J G M, et al. Pathways of cadmium fluxes in the root of the halophyte Suaedasalsa[J]. Ecotoxicology and Environmental Safety, 2012, 75: 1-7. doi: 10.1016/j.ecoenv.2011.09.007
[27]	Han Y S, Wang S J, Zhao N, et al. Exogenous abscisic acid alleviates cadmium toxicity by restricting Cd²⁺ influx in Populus euphratica cells[J]. Journal of Plant Growth Regulation, 2016, 35(3):812-837. http://www.wanfangdata.com.cn/details/detail.do?_type=perio&id=a032cb8de06b4737a489d90784acac07
[28]	Sun J, Wang M J, Ding M Q, et al. H₂O₂ and cytosolic Ca²⁺ signals triggered by the PM H⁺-coupled transport system mediate K⁺/Na⁺ homeostasis in NaCl-stressed Populus euphratica cells[J]. Plant, Cell & Environment, 2010, 33: 943-958.
[29]	Ma Y L, He J L, MA C F, et al. Ectomycorrhizas with Paxillus involutus enhance cadmium uptake and tolerance in Populus×canescens[J]. Plant, Cell & Environment, 2014, 37: 627-642.
[30]	Zhang Y H, Sa G, Zhang Y N, et al. Paxillus involutus-facilitated Cd²⁺ influx through plasma membrane Ca²⁺-permeable channels is stimulated by H₂O₂ and H⁺-ATPase in ectomycorrhizal Populus×canescens under cadmium stress[J]. Frontiers in Plant Science, 2017, 7:1975[2017-10-18]. https://doi.org/10.3389/fpls.2016.01975.
[31]	Gafur A, Schützendübel A, Langenfeld-heyser R, et al. Compatible and incompetent Paxillus involutus isolates for ectomycorrhiza formation in vitro with poplar (Populus×canescens) differ in H₂O₂ production[J]. Plant Biology, 2004, 7: 91-99.
[32]	Li J, Bao S Q, Zhang Y H, et al. Paxillus involutus strains MAJ and NAU mediate K⁺/Na⁺ homeostasis in ectomycorrhizal Populus×canescens under NaCl stress[J]. Plant Physiology, 2012, 159:1771-1786. doi: 10.1104/pp.112.195370
[33]	Pei Z M, Murata Y, Benning G, et al. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells[J]. Nature, 2000, 406: 731-734. doi: 10.1038/35021067

Cited By

Cited by

Periodical cited type(10)

1.	邹玉珍，曾庆伟，武红敢，郑仁高. 变色立木卫星影像样本特征分析及应用. 中国森林病虫. 2023(03): 1-8 .
2.	焦全军，郑焰锋，黄文江，张兵，张鹤译，史宜梦，吴发云，付安民. 陆地生态系统碳监测卫星松材线虫病变色木识别指数研究. 林业资源管理. 2023(04): 123-131 .
3.	曾庆伟，武红敢，张静，杨雅菲. 碳卫星在变色立木遥感监测中的应用潜力分析. 卫星应用. 2023(11): 20-25 .
4.	李炜浩，张硕，刘梓航，苏旻，高浩然，刘善军. 基于光谱指数法的本溪市域红叶提取方法研究. 测绘与空间地理信息. 2022(04): 47-50 .
5.	戴丽，周席华，罗治建，武红敢，陈亮. 湖北松材线虫病卫星遥感监管技术初探. 湖北林业科技. 2022(04): 60-64 .
6.	孙红，曾庆伟. “高分七号”数据在松材线虫病松树样木监测中的应用. 林业科技通讯. 2022(09): 27-29 .
7.	陶欢，李存军，程成，蒋丽雅，胡海棠. 松材线虫病变色松树遥感监测研究进展. 林业科学研究. 2020(03): 172-183 .
8.	陶欢，李存军，谢春春，周静平，淮贺举，蒋丽雅，李凤涛. 基于HSV阈值法的无人机影像变色松树识别. 南京林业大学学报(自然科学版). 2019(03): 99-106 .
9.	武红敢，牟晓伟，杨清钰，王成波. 无人机遥感技术在重庆市沙坪坝区松材线虫病监测中的应用. 林业资源管理. 2019(02): 109-115 .
10.	武红敢，王成波，常原飞. 变色立木的无人机遥感监测技术. 中国森林病虫. 2019(04): 29-32+37 .

Other cited types(4)

Get Citation

PDF

XML

Article views (1964) PDF downloads (66) Cited by(14)

Turn off MathJax

Article Contents

Abstract

References

Uptake of Cd2+ by ectomycorrhizal fungus Paxillus involutus and the modulation of H2O2 in Cd2+ influx

Abstract

References

Cited by

Periodical cited type(10)

Other cited types(4)

Catalog

Export File

Citation

Format

Content

Uptake of Cd²⁺ by ectomycorrhizal fungus Paxillus involutus and the modulation of H₂O₂ in Cd²⁺ influx