Please wait a minute...
Journal of Integrative Agriculture  2017, Vol. 16 Issue (07): 1624-1633    DOI: 10.1016/S2095-3119(16)61456-9
Agro-Ecosystem & Environment Advanced Online Publication | Current Issue | Archive | Adv Search |
Effects of soil salinity on rhizosphere soil microbes in transgenic Bt cotton fields
LUO Jun-yu1, 2*, ZHANG Shuai1*, ZHU Xiang-zhen1, LU Li-min1, WANG Chun-yi1, LI Chun-hua1, CUI Jin-jie1, ZHOU Zhi-guo2
1 State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, P.R.China
2 College of Agriculture, Nanjing Agricultural University/Key Laboratory of Crop Physiology & Ecology in Southern China, Ministry of Agriculture, Nanjing 210095, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract      With increased cultivation of transgenic Bacillus thuringiensis (Bt) cotton in the saline alkaline soil of China, assessments of transgenic crop biosafety have focused on the effects of soil salinity on rhizosphere microbes and Bt protein residues. In 2013 and 2014, investigations were conducted on the rhizosphere microbial biomass, soil enzyme activities and Bt protein contents of the soil under transgenic Bt cotton (variety GK19) and its parental non-transgenic cotton (Simian 3) cultivated at various salinity levels (1.15, 6.00 and 11.46 dS m−1). Under soil salinity stress, trace amounts of Bt proteins were observed in the Bt cotton GK19 rhizosphere soil, although the protein content increased with cotton growth and increased soil salinity levels. The populations of slight halophilic bacteria, phosphate solubilizing bacteria, ammonifying bacteria, nitrifying bacteria and denitrifying bacteria decreased with increased soil salinity in the Bt and non-Bt cotton rhizosphere soil, and the microbial biomass carbon, microbial respiration and soil catalase, urease and alkaline phosphatase activity also decreased. Correlation analyses showed that the increased Bt protein content in the Bt cotton rhizosphere soil may have been caused by the slower decomposition of soil microorganisms, which suggests that salinity was the main factor influencing the relevant activities of the soil microorganisms and indicates that Bt proteins had no clear adverse effects on the soil microorganisms. The results of this study may provide a theoretical basis for risk assessments of genetically modified cotton in saline alkaline soil.
Keywords:  soil salinity        Bt cotton        soil microorganisms        microbial biomass carbon        microbial respiration        soil enzyme activity        Bt protein  
Received: 02 June 2016   Accepted:

This work was supported by the National Natural Science Foundation of China (31501253) and the Project for the Development of Genetically Modified Crops, Ministry of Agriculture, China (2016ZX08011-002).

Corresponding Authors:  Correspondence CUI Jin-jie, E-mail:; ZHOU Zhi-guo, E-mail:   
About author:  LUO Jun-yu, E-mail:;

Cite this article: 

LUO Jun-yu, ZHANG Shuai, ZHU Xiang-zhen, LU Li-min, WANG Chun-yi, LI Chun-hua, CUI Jin-jie, ZHOU Zhi-guo . 2017. Effects of soil salinity on rhizosphere soil microbes in transgenic Bt cotton fields. Journal of Integrative Agriculture, 16(07): 1624-1633.

Barrett-Lennard E G. 2003. The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant and Soil, 253, 35–54.

Beck T, Joergensen R G, Kandeler E, Makeschin F, Nuss E, Oberholzer H R, Scheu S. 1997. An inter-laboratory comparison of ten different ways of measuring soil microbial biomass C. Soil Biology & Biochemistry, 29, 1023–1032.

Bekku Y, Koizumi H, Oikawa T, Iwaki H. 1997. Examination of four methods for measuring soil respiration. Applied Soil Ecology, 5, 247–254.

Belimov A A, Kojemiakov A P, Chuvarliyeva C V. 1995. Interaction between barley and mixed cultures of nitrogen fixing and phosphate-solubilizing bacteria. Plant and Soil, 173, 29–37.

Blackwood C B, Buyer J S. 2004. Soil microbial communities associated with Bt and non-Bt corn in three soils. Journal of Environmental Quality, 33, 832–836.

Burns R G, De Forest J L, Marxsen J, Sinsabaugh R L, Stromberger M E, Wallenstein M D, Weintraub M, Zoppini A. 2013. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biology & Biochemistry, 58, 216–234.

Carvalhais L C, Dennis P G, Dmitri F, Mohammad-Reza H, Rainer B, Nicolaus V W. 2011. Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. Journal of Plant Nutrition & Soil Science, 174, 3–11.

Chen Z H, Chen L J, Wu Z J. 2012. Relationships among persistence of Bacillus thuringiensis and cowpea trypsin inhibitor proteins, microbial properties and enzymatic activities in rhizosphere soil after repeated cultivation with transgenic cotton. Applied Soil Ecology, 53, 23–30.

Daffonchio D, Hirt H, Berg G. 2015. Plant-microbe interactions and water management in arid and saline soils//principles of plant-microbe interactions. In: Principles of Plant-Microbe Interactions.  Springer International Publishing, Switzerland.pp. 265–276.

Dick W A, Cheng L, Wang P. 2000. Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biology and  Biochemistry, 32, 1915–1919.

Dong H Z, Li W J. 2007. Variability of endotoxin expression in Bt transgenic cotton. Journal of Agronomy and Crop Science, 193, 21–29.

García M T, Mellado E, Ostos J C, Ventosa A. 2004. Halomonas organivorans sp. nov., a moderate halophile able to degrade aromatic compounds. International Journal of Systematic & Evolutionary Microbiology, 54, 1723–1728.

Griffiths B S, Caul S, Thompson J, Birch A N, Cortet J, Andersen M N, Krogh P H. 2007. Microbial and microfaunal community structure in cropping systems with genetically modified plants. Pedobiologia, 51, 195–206.

Gupta V V, Roberts G N, Neate S M, McClure S G, Crisp P, Watson S K. 2002. Impact of Bt-cotton on biological processes in Australian soils. In: Akhurst R J, Beard C E, Hughes P A, eds., Proceedings of the Fourth Pacific Rim Conference on the Biotechnology of Bacillus thuringiensis and its Environmental Impacts.  Commonwealth Scientific and Industrial Research Organization (CSIRO), Australia. pp. 191–194.

Gupta V V S R, Watson S. 2004. Ecological Impacts of GM Cotton on Soil Biodiversity: Below-round Production of Bt by GM Cotton and Bt Cotton Impacts on Soil Biological Processes. Australian Government Department of the Environment and Heritage, CSIRO Land and Water. pp. 1–72.

Head G, Surber J B, Watson J A, Martin J W, Duan J J. 2002. No detection of Cry1Ac protein in soil after multiple years of transgenic Bt cotton (Bollgard) use. Environmental Entomology, 31, 30–36.

Helassa N, Quiquampoix H, Noinville S, Szponarski W, Staunton S. 2009. Adsorption and desorption of monomeric Bt (Bacillus thuringiensis) Cry1Aa toxin on montmorillonite and kaolinlte. Soil Biology & Biochemistry, 41, 498–504.

Henry H A L. 2013. Reprint of soil extracellular enzyme dynamics in a changing climate. Soil Biology and Biochemistry, 56, 53–59.

Hopkins D W, Gregorich E G. 2003. Detection and decay of the Bt endotoxin in soil from a field trial with genetically modified maize. European Journal of Soil Science, 54, 793–800.

Jesse L C, Obrycki J J. 2000. Field deposition of Bt transgenic corn pollen: Lethal effects on the monarch butterfly. Oecologia, 125, 241–248.

Joergensen R G, Emmerling C. 2006. Methods for evaluating human impact on soil microorganisms based on their activity, biomass, and diversity in agricultural soils. Journal of Plant Nutrition & Soil Science, 169, 295–309.

Kahlown M A, Azam M. 2002. Individual and combined effect of waterlogging and salinity on crop yields in the Indus basin. Irrigation and Drainage, 51, 329–338.

Kapur M, Bhatia R, Pandey G, Pandey J, Paul D, Jain R K. 2010. A case study for assessment of microbial community dynamics in genetically modified Bt cotton crop fields. Current Microbiology, 61, 118–124.

Kirk J L, Beaudette L A, Hart M, Moutoglis P, Klironomos J N, Lee H, Trevors J T. 2004. Methods of studying soil microbial diversity. Journal of Microbiological Methods, 58, 169–188.

Knox O G G, Gupta V V S R, Lardner R. 2014. Field evaluation of the effects of cotton variety and GM status on rhizosphere microbial diversity and function in Australian soils. Soil Research, 52, 203–215.

Mavi M S, Marschner P, Chittleborough D J, Cox J W, Sanderman J. 2012. Salinity and sodicity affect soil respiration and dissolved organic matter dynamics differentially in soils varying in texture. Soil Biology and Biochemistry, 45, 8–13.

May P B, Douglas L A. 1976. Assay for soil urease activity. Plant and Soil, 45, 301–305.

Mina U, Chaudhary A, Kamra A. 2011. Effect of Bt cotton on enzymes activity and microorganisms in rhizosphere. Journal of Agricultural Science, 3, 96–104.

Pathak H, Rao D L N. 1998. Carbon and nitrogen mineralization from added organic matter in saline and alkali soils. Soil Biology and Biochemistry, 30, 695–702.

Rahman M, Zaman M, Shaheen T,Irem S, Zafar Y. 2015. Safe use of Cry genes in genetically modified crops. Environmental Chemistry Letters, 13, 1–11.

Rengasamy P. 2006. World salinization with emphasis on Australia. Journal of Experimental Botany, 57, 1017–1023.

Rietz D N, Haynes R J. 2003. Effects of irrigation-induced salinity and sodicity on soil microbial activity. Soil Biology and Biochemistry, 35, 845–854.

Rui Y K, Yi G X, Zhao J, Wang B M, Li Z H, Zhai Z X, He Z P, Li Q X. 2005. Changes of Bt toxin in the rhizosphere of transgenic Bt cotton and its influence on soil functional bacteria. World Journal of Microbiology and Biotechnology, 21, 1279–1284.

Salinity K R. 2000. Handbook of Soil Science. CRC Press, Boca Raton. pp. 3–25.

Sardinha M, Müller T, Schmeisky H, Joergensen R G. 2003. Microbial performance in soils along a salinity gradient under acidic conditions. Applied Soil Ecology, 23, 237–244.

Sarkar B, Patra A K, Purakayastha T J, Megharaj M. 2009. Assessment of biological and biochemical indicators in soil under transgenic Bt and non-Bt cotton crop in a sub-tropical environment. Environmental Monitoring Assessment, 156, 595–604.

Shen R F, Cai H, Gong W H. 2006. Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil. Plant and Soil, 285, 149–159.

Steinweg J M, Dukes J S, Wallenstein M D. 2012. Modeling the effects of temperature and moisture on soil enzyme activity: Linking laboratory assays to continuous field data. Soil Biology and Biochemistry, 55, 85–92.

Stepniewska Z, Wolińska A, Ziomek J. 2009. Response of soil catalase activity to chromium contamination. Journal of Environmental Sciences, 21, 1142–1147.

Sun C X, Chen L J, Wu Z J, Zhou L K, Shimizu H. 2007. Soil persistence of Bacillus thuringiensis (Bt) toxin from transgenic Bt cotton tissues and its effect on soil enzyme activities. Biology and Fertility of Soils, 43, 617–620.

Velmourougane K, Sahu A. 2013. Impact of transgenic cottons expressing Cry1Ac on soil biological attributes. Plant Soil and Environment, 59, 108–114.

Vieira F C, Nahas E. 2005. Comparison of microbial numbers in soils by using various culture media and temperatures. Microbiological Research, 160, 197–202.

De Vries F T, Jørgensen B H, Hedlund K, Bardgett R D. 2015. Disentangling plant and soil microbial controls on carbon and nitrogen loss in grassland mesocosms. Journal of  Ecology, 103, 629–640.

Wallenstein M, Allison S D, Ernakovich J, Steinweg J M, Sinsabaugh R. 2010. Controls on the temperature sensitivity of soil enzymes: A key driver of in situ enzyme activity rates. In: Soil Enzymology. Springer Verlag, Berlin. pp. 245–258.

Yuan B, Li Z, Liu H, Gao M, Zhang Y. 2007. Microbial biomass and activity in salt affected soils under arid conditions. Applied Soil Ecology, 35, 319–328.

Zak D R, Holmes W E, White D C, Peacock A D, Tilman D. 2003. Plant diversity, soil microbial communities, and ecosystem function: Are there any links? Ecology, 84, 2054–2050.

Zaman M, Mirza M S, Irem S, Zafar Y, Mehboob-ur-Rahman. 2015. A temporal expression of Cry1Ac protein in cotton plant and its impact on soil health. International Journal of Agriculture and Biology, 17, 28–288.
[1] YANG Ya-jun, XU Hong-xing, WU Zhi-hong, LU Zhong-xian. Effects of inhibitors on the protease profiles and degradation of activated Cry toxins in larval midgut juices of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae)[J]. >Journal of Integrative Agriculture, 2021, 20(8): 2195-2203.
[2] CHEN Yuan, LIU Zhen-yu, HENG Li, Leila I. M. TAMBEL, CHEN De-hua. High plant density increases seed Bt endotoxin content in Bt transgenic cotton[J]. >Journal of Integrative Agriculture, 2021, 20(7): 1796-1806.
[3] GUO Yan, ZHOU Yin, ZHOU Lian-qing, LIU Ting, WANG Lai-gang, CHENG Yong-zheng, HE Jia, ZHENG Guo-qing. Using proximal sensor data for soil salinity management and mapping[J]. >Journal of Integrative Agriculture, 2019, 18(2): 340-349.
[4] QIAO Fang-bin, HUANG Ji-kun, WANG Shu-kun, LI Qiang. The impact of Bt cotton adoption on the stability of pesticide use[J]. >Journal of Integrative Agriculture, 2017, 16(10): 2346-2356.
[5] LIU Xiu-wei, Til Feike, CHEN Su-ying, SHAO Li-wei, SUN Hong-yong, ZHANG Xi-ying. Effects of saline irrigation on soil salt accumulation and grain yield in the winter wheat-summer maize double cropping system in the low plain of North China[J]. >Journal of Integrative Agriculture, 2016, 15(12): 2886-2898.
[6] CHU Lin-lin, KANG Yao-hu, WAN Shu-qin. Effects of water application intensity of microsprinkler irrigation on water and salt environment and crop growth in coastal saline soils[J]. >Journal of Integrative Agriculture, 2015, 14(10): 2077-2089.
[7] GUAN Hong-jie, LI Jiu-sheng, , LI Yan-feng. Effects of Drip System Uniformity and Irrigation Amount on Water and Salt Distributions in Soil Under Arid Conditions[J]. >Journal of Integrative Agriculture, 2013, 12(5): 924-939.
[8] LI Xiao-ming, YANG Jing-song, LIU Mei-xian, LIU Guang-ming, YU Mei. Spatio-Temporal Changes of Soil Salinity in Arid Areas of South Xinjiang Using Electromagnetic Induction[J]. >Journal of Integrative Agriculture, 2012, 12(8): 1365-1376.
No Suggested Reading articles found!