Metabolomic Changes in Sogatella furcifera under Southern rice black-streaked dwarf virus Infection and Temperature Stress
Abstract
:1. Introduction
2. Materials and Methods
2.1. Rice Plant Culturing and Maintenance of SRBSDV
2.2. S. furcifera Propagation
2.3. Temperature Stress Treatment for S. furcifera
2.4. Extraction of WBPH Metabolites
2.5. GC-TOF-MS
2.6. Data Analysis
3. Results
3.1. Global Metabolomics Changes in S. furciferainduced by SRBSDV Infection and/or Temperature Stress
3.2. SRBSDV Infection-Induced S. furcifera Metabolic Changes
3.3. Temperature Stress-Induced S. furcifera Metabolic Changes
3.4. Multiple Stresses Induced WBPH Metabolic Changes
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Zhou, G.; Wen, J.; Cai, D.; Li, P.; Xu, D.; Zhang, S. Southern rice black-streaked dwarf virus: A new proposed Fijivirus species in the family Reoviridae. Chin. Sci. Bull. 2008, 53, 3677–3685. [Google Scholar] [CrossRef]
- Zhou, G.; Xu, D.; Xu, D.; Zhang, M. Southern rice black-streaked dwarf virus: A white-backed planthopper-transmitted fijivirus threatening rice production in Asia. Front. Microbiol. 2013, 4, 270. [Google Scholar] [CrossRef] [PubMed]
- Heong, K.L.; Hardy, B. Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia; International Rice Research Institute: Los Baños, Philippines, 2009. [Google Scholar]
- Oliver, K.M.; Degnan, P.H.; Burke, G.R.; Moran, N.A. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 2010, 55, 247–266. [Google Scholar] [CrossRef] [PubMed]
- Feldhaar, H. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 2011, 36, 533–543. [Google Scholar] [CrossRef] [Green Version]
- Shan, H.; Lu, Y.; Bing, X.; Liu, S.; Liu, Y. Differential responses of the whitefly Bemisia tabaci symbionts to unfavorable low and high temperatures. Microb. Ecol. 2014, 68, 472–482. [Google Scholar] [CrossRef] [PubMed]
- Rubinstein, G.; Czosnek, H. Long-term association of tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci: Effect on the insect transmission capacity, longevity and fecundity. J. Gen. Virol. 1997, 78, 2683–2689. [Google Scholar] [CrossRef] [PubMed]
- Inoue, T.; Sakurai, T. Infection of Tomato spotted wilt virus (TSWV) shortens the life span of thelytokous Thrips tabaci (Thysanoptera: Thripidae). Appl. Entomol. Zool. 2006, 41, 239–246. [Google Scholar] [CrossRef]
- McKenzie, C. Effect of tomato mottle virus (ToMoV) on Bemisia tabaci biotype B (Homoptera: Aleyrodidae) oviposition and adult survivorship on healthy tomato. Fla. Entomol. 2002, 85, 367–368. [Google Scholar] [CrossRef]
- Belliure, B.; Janssen, A.; Sabelis, M.W. Herbivore benefits from vectoring plant virus through reduction of period of vulnerability to predation. Oecologia 2008, 156, 797–806. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pusag, J.C.A.; Jahan, S.H.; Lee, K.-S.; Lee, S.; Lee, K.-Y. Upregulation of temperature susceptibility in Bemisia tabaci upon acquisition of Tomato yellow leaf curl virus (TYLCV). J. Insect Physiol. 2012, 58, 1343–1348. [Google Scholar] [CrossRef] [PubMed]
- Bahar, M.H.; Hegedus, D.; Soroka, J.; Coutu, C.; Bekkaoui, D.; Dosdall, L. Survival and Hsp70 Gene Expression in Plutella xylostella and Its Larval Parasitoid Diadegma insulare Varied between Slowly Ramping and Abrupt Extreme Temperature Regimes. PLoS ONE 2013, 8, e73901. [Google Scholar] [CrossRef] [PubMed]
- Lei, W.; Liu, D.; Li, P.; Hou, M. Interactive effects of southern rice black-streaked dwarf virus infection of host plant and vector on performance of the vector, Sogatella furcifera (Homoptera: Delphacidae). J. Econ. Entomol. 2014, 107, 1721–1727. [Google Scholar] [CrossRef] [PubMed]
- Tu, Z.; Ling, B.; Xu, D.; Zhang, M.; Zhou, G. Effects of southern rice black-streaked dwarf virus on the development and fecundity of its vector, Sogatella furcifera. Virol. J. 2013, 10, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Xu, D.; Pu, L.; Zhou, G. Southern rice black-streaked dwarf virus Alters Insect Vectors’ Host Orientation Preferences to Enhance Spread and Increase Rice ragged stunt virus Co-Infection. Phytopathology 2014, 104, 196–201. [Google Scholar] [CrossRef] [PubMed]
- Lu, G.; Zhang, T.; He, Y.; Zhou, G. Virus altered rice attractiveness to planthoppers is mediated by volatiles and related to virus titre and expression of defence and volatile-biosynthesis genes. Sci. Rep. 2016, 6, 38581. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, D.; Zhong, T.; Feng, W.; Zhou, G. Tolerance and responsive gene expression of Sogatella furcifera under extreme temperature stresses are altered by its vectored plant virus. Sci. Rep. 2016, 6, 31521. [Google Scholar] [CrossRef] [PubMed]
- Kind, T.; Wohlgemuth, G.; Lee, D.Y.; Lu, Y.; Palazoglu, M.; Shahbaz, S.; Fiehn, O. FiehnLib: Mass Spectral and Retention Index Libraries for Metabolomics Based on Quadrupole and Time-of-Flight Gas Chromatography/Mass Spectrometry. Anal. Chem. 2009, 81, 10038–10048. [Google Scholar] [CrossRef] [PubMed]
- Lambrechts, L.; Paaijmans, K.P.; Fansiri, T.; Carrington, L.B.; Kramer, L.D.; Thomas, M.B.; Scott, T.W. Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti. Proc. Natl. Acad. Sci. USA 2011, 108, 7460–7465. [Google Scholar] [CrossRef] [PubMed]
- Carrington, L.B.; Armijos, M.V.; Lambrechts, L.; Scott, T.W. Fluctuations at a Low Mean Temperature Accelerate Dengue Virus Transmission by Aedes aegypti. PLoS Negl. Trop. Dis. 2013, 7, e2190. [Google Scholar] [CrossRef] [PubMed]
- Jia, D.; Mao, Q.; Chen, Y.; Liu, Y.; Chen, Q.; Wu, W.; Zhang, X.; Chen, H.; Li, Y.; Wei, T. Insect symbiotic bacteria harbour viral pathogens for transovarial transmission. Nat. Microbiol. 2017, 2, 17025. [Google Scholar] [CrossRef] [PubMed]
- Pu, L.; Xie, G.; Ji, C.; Ling, B.; Zhang, M.; Xu, D.; Zhou, G. Transmission characteristics of Southern rice black-streaked dwarf virus by rice planthoppers. Crop Prot. 2012, 41, 71–76. [Google Scholar] [CrossRef]
- Jia, D.; Chen, H.; Zheng, A.; Chen, Q.; Liu, Q.; Xie, L.; Wu, Z.; Wei, T. Development of an Insect Vector Cell Culture and RNA Interference System To Investigate the Functional Role of Fijivirus Replication Protein. J. Virol. 2012, 86, 5800–5807. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, Y.; Jia, D.; Chen, H.; Chen, Q.; Xie, L.; Wu, Z.; Wei, T. The P7-1 protein of southern rice black-streaked dwarf virus, a fijivirus, induces the formation of tubular structures in insect cells. Arch. Virol. 2011, 156, 1729–1736. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Zhou, W.; Zhou, Y.; Wu, J.; Zhou, X. Transcriptome and Comparative Gene Expression Analysis of Sogatella furcifera (Horváth) in Response to Southern Rice Black-Streaked Dwarf Virus. PLoS ONE 2012, 7, e36238. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.; He, X.; Zheng, X.; Yang, Y.; Tian, J.; Lu, Z. Southern rice black-streaked dwarf virus (SRBSDV) directly affects the feeding and reproduction behavior of its vector, Sogatella furcifera (Horvath) (Hemiptera: Delphacidae). Virol. J. 2014, 11, 55. [Google Scholar] [CrossRef] [PubMed]
- Lei, W.; Li, P.; Han, Y.; Gong, S.; Yang, L.; Hou, M. EPG Recordings Reveal Differential Feeding Behaviors in Sogatella furcifera in Response to Plant Virus Infection and Transmission Success. Sci. Rep. 2016, 6, 30240. [Google Scholar] [CrossRef] [PubMed]
- Burke, G.; Fiehn, O.; Moran, N. Effects of facultative symbionts and heat stress on the metabolome of pea aphids. ISME J. 2010, 4, 242–252. [Google Scholar] [CrossRef] [PubMed]
- Sisterson, M.S. Transmission of insect-vectored pathogens: Effects of vector fitness as a function of infectivity status. Environ. Entomol. 2009, 38, 345–355. [Google Scholar] [CrossRef] [PubMed]
- Wernegreen, J.J. Mutualism meltdown in insects: Bacteria constrain thermal adaptation. Curr. Opin. Microbiol. 2012, 15, 255–262. [Google Scholar] [CrossRef] [PubMed]
- Coleman-Derr, D.; Tringe, S.G. Building the crops of tomorrow: Advantages of symbiont-based approaches to improving abiotic stress tolerance. Front. Microbiol. 2014, 5, 283. [Google Scholar] [CrossRef] [PubMed]
- Zug, R.; Hammerstein, P. Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol. Rev. 2015, 90, 89–111. [Google Scholar] [CrossRef] [PubMed]
- Stumpf, C.F.; Kennedy, G.G. Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis. Entomol. Exp. Appl. 2007, 123, 139–147. [Google Scholar] [CrossRef]
- Zhou, C.; Yang, H.; Wang, Z.; Long, G.-Y.; Jin, D.-C. Comparative transcriptome analysis of Sogatella furcifera (Horváth) exposed to different insecticides. Sci. Rep. 2018, 8, 8773. [Google Scholar] [CrossRef] [PubMed]
- Than, W.; Qin, F.; Liu, W.; Wang, X. Analysis of Sogatella furcifera proteome that interact with P10 protein of Southern rice black-streaked dwarf virus. Sci. Rep. 2016, 6, 32445. [Google Scholar] [CrossRef] [PubMed]
Category | Peak | Similarity | VIP | p-Value | Fold Change |
---|---|---|---|---|---|
Nucleic acids | Adenine | 753 | 1.35 | 0.019 | 1.17 |
Adenosine | 812 | 1.84 | 2.91 × 10–5 | 1.17 | |
Uracil | 968 | 1.48 | 0.007 | 1.05 | |
Guanosine | 813 | 1.61 | 0.002 | 1.10 | |
Inosine | 909 | 1.73 | 2.82 × 10–4 | 1.09 | |
Uridine | 688 | 1.80 | 5.14 × 10–5 | 0.76 | |
Sugars and polyols | Trehalose | 946 | 2.00 | 6.64 × 10–13 | 0.65 |
Phosphate | 772 | 1.39 | 0.025 | 2.31 × 107 | |
Lactic acid | 967 | 1.59 | 0.003 | 1.14 | |
Fatty acids | Myristic acid | 846 | 1.34 | 0.023 | 1.11 |
Oleic acid | 863 | 1.68 | 0.004 | 3.27 × 106 | |
Palmitoleic acid | 902 | 1.18 | 0.044 | 1.05 |
Category | Peak | Similarity | VIP | p-Value | Fold Change |
---|---|---|---|---|---|
TCA cycle | Oxalacetic acid | 470 | 1.67 | 7.21 × 10–4 | 1.90 |
Pyruvic acid | 926 | 1.59 | 1.50 × 10–4 | 1.50 | |
α-Ketoglutaric acid | 910 | 1.75 | 1.36 × 10–8 | 1.44 | |
Citric acid | 881 | 1.24 | 0.015 | 0.95 | |
Fumaric acid | 654 | 1.19 | 0.017 | 0.78 | |
l-Malic acid | 888 | 1.78 | 2.92 × 10–10 | 0.55 | |
Sugars and polyols | Glucose | 336 | 1.08 | 0.032 | 0.82 |
Palatinitol | 411 | 1.34 | 6.60 × 10–3 | 0.82 | |
Sucrose | 778 | 1.79 | 6.52 × 10–7 | 3.22 × 10–5 | |
2-Deoxyerythritol | 785 | 1.76 | 3.25 × 10–8 | 0.47 | |
1,5-Anhydroglucitol | 436 | 1.55 | 1.69 × 10–5 | 0.07 |
Category | Peak | Similarity | VIP | p-Value | Fold Change |
---|---|---|---|---|---|
TCA cycle | Pyruvic acid | 926 | 1.34 | 0.006 | 0.77 |
α-Ketoglutaric acid | 910 | 1.66 | 1.44 × 10–5 | 0.77 | |
Citric acid | 881 | 1.76 | 3.14 × 10–10 | 0.29 | |
l-Malic acid | 888 | 1.76 | 3.14 × 10–10 | 0.25 |
Category | Peak | Similarity | VIP | p-Value | Fold Change |
---|---|---|---|---|---|
Amino acids | Asparagine | 911 | 1.73 | 6.98 × 10–7 | 0.70 |
Glutamine | 891 | 1.24 | 0.020 | 0.64 | |
Isoleucine | 962 | 1.64 | 3.64 × 10–5 | 0.87 | |
Lysine | 865 | 1.79 | 7.64 × 10–10 | 0.83 | |
Methionine | 865 | 1.64 | 4.88 × 10–5 | 0.87 | |
Phenylalanine | 943 | 1.74 | 1.22 × 10–7 | 0.84 | |
Proline | 596 | 1.41 | 0.003 | 0.96 | |
Threonine | 957 | 1.69 | 3.85 × 10–6 | 0.87 | |
Tryptophan | 897 | 1.78 | 9.77 × 10–11 | 0.81 | |
Ornithine | 918 | 1.72 | 1.06 × 10–6 | 0.82 | |
l-homoserine | 918 | 1.41 | 0.002 | 0.94 | |
β-Alanine | 925 | 1.79 | 4.85 × 10–12 | 0.58 | |
Sugars and polyols | d-talose | 929 | 1.73 | 1.70 × 10–6 | 1.23 |
Fructose | 958 | 1.72 | 1.82 × 10–6 | 1.12 | |
Fructose-6-phosphate | 753 | 1.68 | 1.24 × 10–5 | 1.35 | |
Sucrose | 778 | 1.61 | 4.21 × 10–5 | 1.30 | |
Tagatose | 725 | 1.25 | 0.010 | 1.28 | |
Trehalose | 946 | 1.77 | 1.81 × 10–8 | 1.15 | |
Glycerol | 823 | 1.70 | 2.56 × 10–6 | 1.17 |
Category | Peak | Similarity | VIP | p-Value | Fold Change |
---|---|---|---|---|---|
Amino acids | Alanine | 800 | 1.67 | 2.11 × 10–11 | 1.32 |
Asparagine | 911 | 1.65 | 3.86 × 10–9 | 1.58 | |
Glutamic acid | 866 | 1.62 | 6.20 × 10–7 | 1.37 | |
Glycine | 860 | 1.46 | 1.78 × 10–4 | 1.23 | |
Methionine | 865 | 1.61 | 1.04 × 10–6 | 1.21 | |
Proline | 596 | 1.66 | 4.35 × 10–10 | 1.21 | |
Serine | 964 | 1.15 | 0.015 | 1.05 | |
Threonine | 957 | 1.67 | 9.44 × 10–11 | 1.74 | |
Valine | 880 | 1.62 | 6.08 × 10–7 | 1.27 | |
β-Alanine | 925 | 1.66 | 7.49 × 10–9 | 1.42 | |
Norvaline | 614 | 1.57 | 5.50 × 10–6 | 1.45 | |
Ornithine | 945 | 1.59 | 2.89 × 10–6 | 1.39 | |
l-homoserine | 918 | 1.65 | 1.99 × 10–8 | 1.39 | |
Sugars and polyols | Allose | 589 | 1.43 | 6.02 × 10–4 | 3.12 |
d-glucoheptose | 601 | 1.47 | 1.67 × 10–4 | 4.19 | |
d-talose | 929 | 1.61 | 6.77 × 10–7 | 1.25 | |
Fructose | 958 | 1.47 | 2.24 × 10–4 | 1.08 | |
Lactose | 547 | 1.05 | 0.042 | 1.79 | |
Trehalose | 946 | 1.24 | 0.029 | 1.22 | |
Lactulose | 488 | 1.09 | 0.022 | 1.87 | |
2-Deoxyerythritol | 785 | 1.27 | 0.005 | 1.15 | |
1,5-Anhydroglucitol | 436 | 1.09 | 0.026 | 1.12 | |
Glycerol | 823 | 1.05 | 0.030 | 1.04 |
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Zhang, T.; Feng, W.; Ye, J.; Li, Z.; Zhou, G. Metabolomic Changes in Sogatella furcifera under Southern rice black-streaked dwarf virus Infection and Temperature Stress. Viruses 2018, 10, 344. https://doi.org/10.3390/v10070344
Zhang T, Feng W, Ye J, Li Z, Zhou G. Metabolomic Changes in Sogatella furcifera under Southern rice black-streaked dwarf virus Infection and Temperature Stress. Viruses. 2018; 10(7):344. https://doi.org/10.3390/v10070344
Chicago/Turabian StyleZhang, Tong, Wendi Feng, Jiajie Ye, Zhanbiao Li, and Guohui Zhou. 2018. "Metabolomic Changes in Sogatella furcifera under Southern rice black-streaked dwarf virus Infection and Temperature Stress" Viruses 10, no. 7: 344. https://doi.org/10.3390/v10070344
APA StyleZhang, T., Feng, W., Ye, J., Li, Z., & Zhou, G. (2018). Metabolomic Changes in Sogatella furcifera under Southern rice black-streaked dwarf virus Infection and Temperature Stress. Viruses, 10(7), 344. https://doi.org/10.3390/v10070344