Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (24): 4884-4893.doi: 10.3864/j.issn.0578-1752.2024.24.005

• PLANT PROTECTION • Previous Articles     Next Articles

Differentially Expressed Proteins Analysis of Locusta migratoria Infected by Paranosema locustae Based on TMT Proteomics Technique

ZHANG HuiHui1,2(), KANG HanYe1,2, LIU Hui1,2, ZHANG JinRui1,2, HUO Fan1,2, GUO WeiQi1,2, YE XiaoFang1,2, JI Rong1,2, HU HongXia1,2()   

  1. 1 College of Life Sciences, Xinjiang Normal University/International Research Center of Cross-Border Pest Management in Central Asia, China/Xinjiang Key Laboratory of Special Species Conservation and Regulatory Biology, Urumqi 830017
    2 Tacheng, Research Field (Migratory Biology), Observation and Research Station of Xinjiang, Tacheng 834700, Xinjiang
  • Received:2024-07-28 Accepted:2024-08-30 Online:2024-12-16 Published:2024-12-23
  • Contact: HU HongXia

Abstract:

【Objective】The objective of this study is to determine differentially expressed proteins in Locusta migratoria before and after Paranosema locustae infection by using tandem mass tag (TMT) quantitative proteomics techniques, screen differentially expressed immune and metabolic related proteins, and to explore the pathogenic mechanism of P. locustae, so as to provide a scientific basis for better use of P. locustae to control locusts in the future. 【Method】The healthy nymphs obtained by laboratory incubation were inoculated with 5 µL of 1×106 spores/mL P. locustae. The uninfected nymphs were used as the control group and fed under the same conditions as the infected group. The hemolymph of L. migratoria was taken as a sample. TMT technique was used to analyze the quantitative proteomics of the L. migratoria hemolymph in the infected group and the control group, and the differential proteins were identified. The biological process, molecular function and cellular component of differential proteins were analyzed by the Gene Ontology (GO) method. The differential proteins metabolic pathways were annotated by the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway website. 【Result】A total of 128 proteins were significantly different in abundance between the infected group and the control group, of which 66 proteins were up-regulated and 62 proteins were down-regulated in the infected group. GO analysis showed that the differential proteins were mainly involved in metabolic processes and were mainly distributed in cells. KEGG analysis showed that 16 proteins were significantly enriched in five pathways. Immune-related proteins, including six glutathione S-transferases (GSTs), one superoxide dismutase (SOD), four heat shock proteins (HSPs) and two peroxide dismutases (PODs), were significantly changed. Besides, metabolism-related proteins, including six glycometabolism-related proteins, two amino acids and one lipid metabolism-related proteins, were significantly changed. 【Conclusion】There were significant differences in the protein levels of L. migratoria before and after infection with P. locustae. Several differentially expressed proteins with different functions were screened, which were mainly distributed in cells. Immune-related proteins such as GST, HSP, SOD and POD were significantly up-regulated, indicating that immune and stimulus response-related proteins play an important role in the immune defense of locust hosts. The significant increase in metabolism-related proteins suggests that P. locustae infection promotes L. migratoria metabolism and provides energy for its proliferation.

Key words: Paranosema locustae, Locusta migratoria, hemolymph, proteomics, immune-related protein, metabolism-related protein

Fig. 1

SDS-PAGE analysis of total proteins of L. migratoria before and after infection with P. locustae"

Fig. 2

GO enrichment function analysis of differentially expressed proteins"

Table 1

KEGG signal pathway annotation of differentially expressed proteins"

通路
Pathway
P
P value
通路号
Pathway ID
过氧化物酶体Peroxisome 0.015 ko04146
糖酵解Glycolysis 0.035 ko00010
核苷酸糖的生物合成
Biosynthesis of nucleotide sugars
0.048 ko01250
HIF-1信号通路
HIF-1 signaling pathway
0.048 ko04066
内吞作用Endocytosis 0.048 ko04144

Fig. 3

Network interaction analysis of differential proteins Up-regulated proteins are labeled red, down-regulated proteins are labeled blue, and the size of the circle indicates the connectivity of the protein"

Table 2

Change of immune-related protein contents against infection"

蛋白类型
Protein type
登录号
Accession number
蛋白名称
Protein name
上调/下调表达倍数
Ratio of up/down expression
谷胱甘肽S-转移酶
Glutathione S-transferase
E7BTM5 GST-1 1.67↑
A0A6G7K2Y6 GST-2 1.78↑
V9Q4G7 GST-3 1.46↑
V9Q315 GST-4 1.42↑
F4YUJ0 GST-5 1.41↑
A0A140DD58 GST-6 1.36↑
超氧化物歧化酶Superoxide dismutase G9C5D1 SOD-1 1.78↑
热休克蛋白
Heat shock protein
G9C5E1 HSP-1 1.78↑
Q0ZLZ4 HSP-2 1.43↑
Q6SXP5 HSP-3 1.31↑
Q6WAW3 HSP-4 1.20↑
过氧化物酶
Peroxide dismutase
A0A1B3PEJ4 POD-1 1.32↑
A0A7U0QRH0 POD-2 1.51↑

Table 3

Change of energy-related protein contents against infection"

蛋白类型
Protein type
登录号
Accession number
蛋白名称
Protein name
上调/下调表达倍数
Ratio of up/down expression
糖代谢
Glycometabolism
C0KJJ7 己糖激酶Hexokinase 1.35↑
C0KJJ8 磷酸葡萄糖变位酶Phosphoglucomutase 1.37↑
G9C5D5 果糖二磷酸醛缩酶,I类Fructose-bisphosphate aldolase, class I 2.03↑
O96558 甘油醛-3-磷酸脱氢酶(磷酸化)
Glyceraldehyde-3-phosphate dehydrogenase (phosphorylating)
1.55↑
H8YU84 甘油醛-3-磷酸脱氢酶Glyceraldehyde-3-phosphate dehydrogenase 1.46↑
A8D372 海藻糖-6-磷酸合酶Trehalose-6-phosphate synthase 1.42↑
氨基酸代谢
Amino acid metabolism
G9C5D9 谷氨酰胺合成酶Glutamine synthetase 1.53↑
A0A290WIX5 苯丙氨酸羟化酶Phenylalanine hydroxylase 1.41↑
脂代谢 Lipid metabolism P10762 脂载蛋白Apolipophorin-3b 2.31↑
[1]
LANGE C E. The host and geographical range of the grasshopper pathogen Paranosema (Nosema) locustae revisited. Journal of Orthoptera Research, 2005, 14(2): 137-141.
[2]
赵紫华, 涂雄兵, 张泽华, 李志红. 警惕沙漠蝗种群持续增加和入侵我国边境地区的风险. 植物保护学报, 2021, 48(1): 5-12.
ZHAO Z H, TU X B, ZHANG Z H, LI Z H. The alert of population expansion of the desert locust Schistocerca gregaria and its risk to enter China. Journal of Plant Protection, 2021, 48(1): 5-12. (in Chinese)
[3]
张龙. 蝗虫微孢子虫及其在蝗害治理中的作用. 生物学通报, 1999, 34(2): 11-12.
ZHANG L. The role of Nosema locust in pest control. Bulletin of Biology, 1999, 34(2): 11-12. (in Chinese)
[4]
HOU C Y, GUO D Q, YU X, WANG S Y, LIU T H. TMT-based proteomics analysis of the anti-hepatocellular carcinoma effect of combined dihydroartemisinin and sorafenib. Biomedicine & Pharmacotherapy, 2020, 126: 109862.
[5]
FU M Z, YAN Y C, SU H, WANG J J, SHI X J, ZHOU H C, ZHANG Q, XU X G. Spleen proteome profiling of dairy goats infected with C. pseudotuberculosis by TMT-based quantitative proteomics approach. Journal of Proteomics, 2021, 248: 104352.
[6]
严毓骅, 张龙. 我国蝗虫微孢子虫治蝗的进展. 植保技术与推广, 1994(1): 43.
YAN Y H, ZHANG L. Progress of controlling locust with Nosema locustae in China. Plant Protection Technology and Promotion, 1994(1): 43. (in Chinese)
[7]
张龙, 游银伟. 中国特色蝗灾治理技术体系及应用成效. 植物保护学报, 2022, 49(1): 118-124.
ZHANG L, YOU Y W. Technical systems for locust and grasshopper management with Chinese features and their success in application. Journal of Plant Protection, 2022, 49(1): 118-124. (in Chinese)
[8]
陈龙欣. 蝗虫微孢子虫寄生飞蝗的分子基础[D]. 北京: 中国农业大学, 2017.
CHEN L X. Molecular basis of Antonospora locustae parasite in locust[D]. Beijing: China Agricultural University, 2017. (in Chinese)
[9]
CHEN L X, GAO X K, LI R T, ZHANG L M, HUANG R, WANG L Q, SONG Y, XING Z Z, LIU T, NIE X N, et al. Complete genome of a unicellular parasite (Antonospora locustae) and transcriptional interactions with its host locust. Microbial Genomics, 2020, 6(9): mgen000421.
[10]
姜义仁, 宋佳, 秦玉璘, 王勇, 臧敏, 钟亮, 杨瑞生, 石生林, 段玉玺, 秦利. 柞蚕感染微孢子虫后血淋巴免疫应答蛋白质的分离与鉴定. 昆虫学报, 2012, 55(10): 1119-1131.
JIANG Y R, SONG J, QIN Y L, WANG Y, ZANG M, ZHONG L, YANG R S, SHI S L, DUAN Y X, QIN L. Separation and identification of haemolymph proteins involved in immune response to Nosema pernyi infection in Antheraea pernyi (Lepidoptera: Saturniidae) larvae. Acta Entomologica Sinica, 2012, 55(10): 1119-1131. (in Chinese)
[11]
LIU H, WEI X J, YE X F, ZHANG H H, YANG K, SHI W P, ZHANG J R, JASHENKO R, JI R, HU H X. The immune response of Locusta migratoria manilensis at different times of infection with Paranosema locustae. Archives of Insect Biochemistry and Physiology, 2023, 114(4): e22055.
[12]
ZHANG H H, YANG K, WANG H, LIU H, SHI W P, KABAK I, JI R, HU H X. Molecular and biochemical changes in Locusta migratoria (Orthoptera: Acrididae) infected with Paranosema locustae. Journal of Insect Science, 2023, 23(5): 1.
[13]
MOURA H, OSPINA M, WOOLFITT A R, BARR J R, VISVESVARA G S. Analysis of four human microsporidian isolates by MALDI-TOF mass spectrometry. Journal of Eukaryotic Microbiology, 2003, 50(3): 156-163.

pmid: 12836871
[14]
HAN B, POLONAIS V, SUGI T, YAKUBU R, TAKVORIAN P M, CALI A, MAIER K, LONG M X, LEVY M, TANOWITZ H B, PAN G Q, DELBAC F, ZHOU Z Y, WEISS L M. The role of microsporidian polar tube protein 4 (PTP4) in host cell infection. PLoS Pathogens, 2017, 13(4): e1006341.
[15]
WANG Y, MA Y Y, WANG D Y, LIU W, CHEN J, JIANG Y, YANG R, QIN L. Polar tube structure and three polar tube proteins identified from Nosema pernyi. Journal of Invertebrate Pathology, 2019, 168: 107272.
[16]
LV Q, WANG L J, FAN Y P, MENG X Z, LIU K K, ZHOU B Q, CHEN J, PAN G Q, LONG M X, ZHOU Z Y. Identification and characterization a novel polar tube protein (NbPTP6) from the microsporidian Nosema bombycis. Parasites and Vectors, 2020, 13(1): 475.
[17]
YANG D L, PAN G Q, DANG X Q, SHI Y W, LI C F, PENG P, LUO B, BIAN M F, SONG Y, MA C, et al. Interaction and assembly of two novel proteins in the spore wall of the microsporidian species Nosema bombycis and their roles in adherence to and infection of host cells. Infection and Immunity, 2015, 83(4): 1715-1731.
[18]
ESVARAN V G, PONNUVEL S, JAGADISH A, SAVITHRI H S, SUBRAMANYA H S, PONNUVEL K M. Cloning, expression and characterization of spore wall protein 5 (SWP5) of Indian isolate NIK-1S of Nosema bombycis. The Protein Journal, 2022, 41(6): 596-612.
[19]
YU B, ZHENG R, BIAN M F, LIU T, LU K, BAO J L, PAN G Q, ZHOU Z Y, LI C F. A monoclonal antibody targeting spore wall protein 1 inhibits the proliferation of Nosema bombycis in Bombyx mori. Microbiology Spectrum, 2023, 11(6): e0068123.
[20]
康乐, 魏丽亚. 中国蝗虫学研究60年. 植物保护学报, 2022, 49(1): 4-16.
KANG L, WEI L Y. Progress of acridology in China over the last 60 years. Journal of Plant Protection, 2022, 49(1): 4-16. (in Chinese)
[21]
石旺鹏, 谭树乾. 蝗虫生物防治发展现状及趋势. 中国生物防治学报, 2019, 35(3): 307-324.

doi: 10.16409/j.cnki.2095-039x.2019.03.020
SHI W P, TAN S Q. Current status and trend on grasshopper and locust biological control. Chinese Journal of Biological Control, 2019, 35(3): 307-324. (in Chinese)

doi: 10.16409/j.cnki.2095-039x.2019.03.020
[22]
高兴珂, 班丽萍. 蝗虫微孢子虫的基因组学研究进展及应用现状. 植物保护学报, 2021, 48(1): 60-64.
GAO X K, BAN L P. Genomics research progresses in microsporidia Antonospora locustae and its application status. Journal of Plant Protection, 2021, 48(1): 60-64. (in Chinese)
[23]
PARRELLA P, ELIKAN A B, KOGAN H V, WAGUE F, MARSHALLECK C A, SNOW J W. Bleomycin reduces Vairimorpha (Nosema) ceranae infection in honey bees with some evident host toxicity. Microbiology Spectrum, 2024, 12(2): e0334923.
[24]
黄诗迪, 黄彩萍, 于欢, 王敦. 棉铃虫核型多角体病毒感染对宿主昆虫GST活性及其表达水平的影响. 西北农林科技大学学报(自然科学版), 2015, 43(11): 129-133.
HUANG S D, HUANG C P, YU H, WANG D. Effect of Helicoverpa armigera nucleopolyhedrovirus infection on GST activity and GST expression on host insect. Journal of Northwest A&F University (Natural Science Edition), 2015, 43(11): 129-133. (in Chinese)
[25]
ENAYATI A A, RANSON H, HEMINGWAY J. Insect glutathione transferases and insecticide resistance. Insect Molecular Biology, 2005, 14(1): 3-8.

doi: 10.1111/j.1365-2583.2004.00529.x pmid: 15663770
[26]
赵玲, 赵莉, 肖宏伟, 王登元. 高效氯氟氰菊酯对意大利蝗的杀虫活性及对谷胱甘肽S-转移酶活性的影响. 植物保护, 2014, 40(3): 130-132, 142.
ZHAO L, ZHAO L, XIAO H W, WANG D Y. Insecticidal activities of lambda-cyhalothrin (EC) to Calliptamus italicus and effects on glutathione S-transferases (GSTs). Plant Protection, 2014, 40(3): 130-132, 142. (in Chinese)
[27]
李亚红. 昆虫谷胱甘肽硫转移酶农药解毒与内源代谢研究进展. 山西大同大学学报(自然科学版), 2014, 30(4): 49-51.
LI Y H. The progress in the research of insect GST on insecticide detoxification and endogenous metabolism. Journal of Datong University (Natural Science Edition), 2014, 30(4): 49-51. (in Chinese)
[28]
王薇, 韩岚岚, 赵奎军. 昆虫热休克蛋白Hsp70的研究进展. 东北农业大学学报, 2009, 40(11): 129-132.
WANG W, HAN L L, ZHAO K J. Research advance of heat shock protein 70 in entomology. Journal of Northeast Agricultural University, 2009, 40(11): 129-132. (in Chinese)
[29]
夏晓峰, 林海兰, 郑丹丹, 杨广, 尤民生. 小菜蛾热休克蛋白基因的鉴定及其表达模式分析. 昆虫学报, 2013, 56(5): 457-464.
XIA X F, LIN H L, ZHENG D D, YANG G, YOU M S. Identification and expression patterns of heat shock protein genes in the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Acta Entomologica Sinica, 2013, 56(5): 457-464. (in Chinese)
[30]
张彦丰, 王正浩, 农向群, 曹广春, 赵莉, 王广君, 张泽华. 绿僵菌侵染对东亚飞蝗中肠保护酶和解毒酶的影响. 中国生物防治学报, 2015, 31(6): 876-881.

doi: 10.16409/j.cnki.2095-039x.2015.06.009
ZHANG Y F, WANG Z H, NONG X Q, CAO G C, ZHAO L, WANG G J, ZHANG Z H. Effect of Metarhizium anisopliae on protective enzyme and detoxification enzyme in the midgut of Locusta migratoria manilensis. Chinese Journal of Biological Control, 2015, 31(6): 876-881. (in Chinese)
[31]
徐欣, 吴玉娇, 于滨, 孟宪志, 陈杰, 刘中文, 张永君, 潘国庆. 柞蚕微孢子虫感染后柞蚕卵转录组及免疫相关基因功能分析. 昆虫学报, 2023, 66(12): 1560-1569.
XU X, WU Y J, YU B, MENG X Z, CHEN J, LIU Z W, ZHANG Y J, PAN G Q. Transcriptome and immune-related gene function analyses of Antheraea pernyi (Lepidoptera: Saturniidae) eggs infected by Nosema pernyi. Acta Entomologica Sinica, 2023, 66(12): 1560-1569. (in Chinese)
[32]
KEELING P J, CORRADI N. Shrink it or lose it: Balancing loss of function with shrinking genomes in the microsporidia. Virulence, 2011, 2(1): 67-70.

pmid: 21217203
[33]
TIMOFEEV S, TOKAREV Y, DOLGIKH V. Energy metabolism and its evolution in Microsporidia and allied taxa. Parasitology Research, 2020, 119(5): 1433-1441.

doi: 10.1007/s00436-020-06657-9 pmid: 32200463
[34]
JOHN S, WEISS J N, RIBALET B. Subcellular localization of hexokinases I and II directs the metabolic fate of glucose. PLoS ONE, 2011, 6(3): e17674.
[35]
CUOMO C A, DESJARDINS C A, BAKOWSKI M A, GOLDBERG J, MA A T, BECNEL J J, DIDIER E S, FAN L, HEIMAN D I, LEVIN J Z, YOUNG S, ZENG Q D, TROEMEL E R. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Research, 2012, 22(12): 2478-2488.

doi: 10.1101/gr.142802.112 pmid: 22813931
[36]
VALDIVIA R H, HEITMAN J. Endosymbiosis: The evil within. Current Biology, 2007, 17(11): R408-R410.

doi: 10.1016/j.cub.2007.04.001 pmid: 17550764
[37]
LUO J, HE Q, XU J Z, XU C, HAN Y Z, GAO H L, MENG X Z, PAN G Q, LI T, ZHOU Z Y. Microsporidia infection upregulates host energy metabolism but maintains ATP homeostasis. Journal of Invertebrate Pathology, 2021, 186: 107596.
[38]
JIA J, HUANG W, SCHÖRKEN U, SAHM H, SPRENGER G A, LINDQVIST Y, SCHNEIDER G. Crystal structure of transaldolase B from Escherichia coli suggests a circular permutation of the alpha/beta barrel within the class I aldolase family. Structure, 1996, 4(6): 715-724.
[39]
TANG B, WANG S G, ZHANG F. Two storage hexamerins from the beet armyworm Spodoptera exigua: Cloning, characterization and the effect of gene silencing on survival. BMC Molecular Biology, 2010, 11: 65.
[1] WANG Chao,FANG DongLu,ZHANG PanRong,JIANG Wen,PEI Fei,HU QiuHui,MA Ning. Physiological Metabolic Rol e of Nanocomposite Packaged Agaricus bisporus During Postharvest Cold Storage Analyzed by TMT-Based Quantitative Proteomics [J]. Scientia Agricultura Sinica, 2022, 55(23): 4728-4742.
[2] ZHOU GuiYing,YANG XiaoMin,TENG ZiWen,SUN LiJuan,ZHENG ChangYing. Quantitative Proteomic Analysis of Spirotetramat Inhibiting Hatching of Frankliniella occidentalis Eggs [J]. Scientia Agricultura Sinica, 2022, 55(15): 2938-2948.
[3] MA Wen,LIU Jiao,ZHANG XueYao,SHEN GuoHua,QIN XueMei,ZHANG JianQin. Enzymatic Characteristics and Metabolic Analysis to Malathion and p,p’-DDT of LmGSTS2 from Locusta migratoria [J]. Scientia Agricultura Sinica, 2019, 52(8): 1389-1399.
[4] ZHANG Yan, DONG ZhaoMing, XI XingHang, ZHANG XiaoLu, YE Lin, GUO KaiYu, XIA QingYou, ZHAO Ping. Protein Components of Degumming Bombyx mori Silk [J]. Scientia Agricultura Sinica, 2018, 51(11): 2216-2224.
[5] LIU Lu, LU Jing, WANG Ying, PANG XiaoYang, XU Man, ZHANG ShuWen, Lü JiaPing. Antitumor Effect of Violacein Against HT29 by Comparative Proteomics [J]. Scientia Agricultura Sinica, 2017, 50(9): 1694-1704.
[6] HAO WenYuan, LI FeiWu, YAN Wei, LI CongCong, HAO DongYun, GUO ChangHong. Assessment of the Unintended Effects of Four Genetically Modified Maize Varieties by Proteomic Approach [J]. Scientia Agricultura Sinica, 2017, 50(19): 3652-3664.
[7] YU Tao, LI Geng, LIU Peng, DONG ShuTing, ZHANG JiWang, ZHAO Bin. Proteomic Analysis of Maize Reveals Expression Characteristics of Stress-Related Proteins During Grain Development [J]. Scientia Agricultura Sinica, 2017, 50(11): 2114-2128.
[8] XU Chuang, ZHU Kui-ling, CHEN Yuan-yuan, YANG Wei, XIA Cheng, ZHANG Hong-you, WU Ling, SHU Shi, SHEN Tai-yu, YU Hong-jiang, XU Qiu-shi, ZHANG Zi-yang . Isolation Identification and Bioinformatics of Differences Protein in Plasma of Cows Suffer from Fatty Liver with SELDI-TOF-MS Techniques [J]. Scientia Agricultura Sinica, 2016, 49(8): 1585-1598.
[9] XU Ying, YAN Guo-quan, ZHANG Yang, YU Hong-xiu. Differential Proteomic Research of Three Varieties of Tobacco in China [J]. Scientia Agricultura Sinica, 2016, 49(16): 3084-3097.
[10] WANG Xiang-yu, WEI Shan-shan, DONG Shu-ting, LIU Peng, ZHANG Ji-wang, ZHAO Bin. Regulation of Nitrogen on Protein Expression of Summer Maize (Zea mays L.) Leaves at Filling Stage [J]. Scientia Agricultura Sinica, 2015, 48(9): 1727-1736.
[11] SONG Li-ru, WANG Shuang, NIU Juan, MA Hong-yu, SHU Ying-jie, YANG Yan, GU Wei-hong, MA Hao. Differentially Proteomics Analysis of Pre-Harvest Seed Deterioration and Deterioration Resistance in Spring Soybean [J]. Scientia Agricultura Sinica, 2015, 48(1): 23-32.
[12] . Proteome Analysis of Cytoplasmic Male Sterility and Its Maintaince in JA-CMS Cotton [J]. Scientia Agricultura Sinica, 2014, 47(20): 3929-3940.
[13] ZHANG Hao, CHEN Jin-xiang, LIU Hai-he, ZHOU Zhong-hua, WANG Feng. Adaptation Mechanism to Aquatic Environment of Cotton Seedlings Roots in Floating Nursing Seedlings in Nutrient Water-Bed (FNSNW) [J]. Scientia Agricultura Sinica, 2014, 47(17): 3372-3381.
[14] LIAO Jiang-Lin, SONG Yu, ZHONG Ping-An, ZHOU Hui-Wen, ZHANG Hong-Yu, HUANG Ying-Jin. Identification of the Differentially Expressed Proteins Between Heat-Tolerant and Heat-Sensitive Rice Responding to High-Temperature Stress at the Early Milky Stage [J]. Scientia Agricultura Sinica, 2014, 47(16): 3121-3131.
[15] WANG Zhen-Hui-1, YUAN Kun-1, YANG Li-Fu-1, ZHANG Jun-Ling-2. Response of Maize Leaf Proteins Induced/Modulated by AM Mycorrhizal Inoculation and (or) Arsenic Stress [J]. Scientia Agricultura Sinica, 2013, 46(18): 3758-3767.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!