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Metabolome and ionome analyses reveal the stoichiometric effects of contrasting geological phosphorus soils on seed-parasitic insects in subtropical oak forests

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Abstract

Phosphorus (P)-rich sites develop on phosphate-rock ores, while the soils are generally characterized with P deficiency in subtropical areas, resulting in contrasting nutrient environments for plants and herbivores. It remains unclear how in situ herbivorous insects cope with such two extreme nutrient habitats in terms of metabolome and ionome. Here, we investigated the metabolome and ionome of the weevil larvae (Curculio davidi Fairmaire), which were parasitizing in Quercus variabilis acorns at P-rich and P-deficient sites. Our results showed that there were significant differences in 34 identified metabolites (belonging to sugars, amino acids, lipids, vitamins, nucleosides, etc.) and four chemical elements (P, S, Mg, and Zn) in the two weevil larva populations of the two P-type sites. Moreover, the concentrations of P, Mg, Zn and the identified sugars were significantly higher; however, S, amino acids, and several other N-containing metabolites were lower in the weevil larvae at the P-rich site, in contrast to those at the P-deficient site. Arginine and proline metabolism and glutathione metabolism were the most relevant pathways differentially regulated between the two weevil larva populations at the two contrasting sites. In addition, some metabolites in the weevil larvae were indirectly associated with the P, Mg, Zn, and S concentrations of soils through bottom-up effects. Our results suggested that in situ herbivorous consumers altered their metabolites to a certain extent to adapt to nutrient-varying environments; and there were strong interactions between the nutrients of herbivorous insects and soil elements across variable nutrient sites.

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References

  • Amtmann A, Armengaud P (2009) Effects of N, P, K and S on metabolism: new knowledge gained from multi-level analysis. Curr Opin Plant Biol 12:275–283

    Article  CAS  Google Scholar 

  • Bender DA (2012) Amino acid metabolism. John Wiley & Sons, Ltd, Chichester, UK

    Google Scholar 

  • Boer VM, Crutchfield CA, Bradley PH, Botstein D, Rabinowitz JD (2010) Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol Biol Cell 21:198–211

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cease AJ, Elser JJ, Ford CF, Hao S, Kang L, Harrison JF (2012) Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content. Science 335:467–469

    CAS  PubMed  Google Scholar 

  • Cease AJ, Fay M, Elser JJ, Harrison JF (2016) Dietary phosphate affects food selection, post-ingestive phosphorus fate, and performance of a polyphagous herbivore. J Exp Biol 219:64–72

    PubMed  Google Scholar 

  • Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550

    Google Scholar 

  • FAO I (1998) World reference base for soil resources. World soil resources reports

  • Fester T, Merbach I, Schulz E, Härtig C (2014) Metabolic response of Medicago sativa to severe nutrient imbalances and disturbances under field conditions. J Plant Nutr Soil Sci 177:245–259

    CAS  Google Scholar 

  • Frisch D, Morton PK, Chowdhury PR, Culver BW, Colbourne JK, Weider LJ, Jeyasingh PD (2014) A millennial-scale chronicle of evolutionary responses to cultural eutrophication in Daphnia. Ecol Lett 17:360–368

    PubMed  Google Scholar 

  • Guo R, Shi L, Yang C, Yan C, Zhong X, Liu Q, Xia X, Li H (2016) Comparison of ionomic and metabolites response under alkali stress in old and young leaves of cotton (Gossypium hirsutum L.) seedlings. Front Plant Sci 7:1785

    PubMed  PubMed Central  Google Scholar 

  • Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385

    CAS  PubMed  Google Scholar 

  • Hänsch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    PubMed  Google Scholar 

  • Heby O (1986) Putrescine, spermidine, and spermine. News Physiol Sci 1:12–15

    CAS  Google Scholar 

  • Ibanez S, Millery A, D’ottavio M, Guilhot R, Vesin E (2017) Phosphorus-rich grasshoppers consume plants high in nitrogen and phosphorus. Ecol Entomol 42:610–616

    Google Scholar 

  • Jeyasingh PD, Weider LJ (2007) Fundamental links between genes and elements: evolutionary implications of ecological stoichiometry. Mol Ecol 16:4649–4661

    CAS  PubMed  Google Scholar 

  • Jeyasingh PD, Weider LJ, Sterner RW (2009) Genetically-based trade-offs in response to stoichiometric food quality influence competition in a keystone aquatic herbivore. Ecol Lett 12:1229–1237

    PubMed  Google Scholar 

  • Jeyasingh PD, Ragavendran A, Paland S, Lopez JA, Sterner RW, Colbourne JK (2011) How do consumers deal with stoichiometric constraints? Lessons from functional genomics using Daphnia pulex. Mol Ecol 20:2341–2352

    PubMed  Google Scholar 

  • Ji H, Du B, Liu C (2017) Elemental stoichiometry and compositions of weevil larvae and two acorn hosts under natural phosphorus variation. Sci Rep 7:45810

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ji H, Ossipov V, Du B, Wen J, Liu C (2019) Differences in the relationship between metabolomic and ionomic traits of Quercus variabilis growing at contrasting geologic-phosphorus sites in subtropics. Plant Soil 439:339–355

    CAS  Google Scholar 

  • Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93:1002–1015

    PubMed  Google Scholar 

  • Kind T, Wohlgemuth G, Lee DY, Lu Y, Palazoglu M, Shahbaz S, Fiehn O (2009) FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem 81:10038–10048

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lundstedt T, Seifert E, Abramo L, Thelin B, Nyström Å, Pettersen J, Bergman R (1998) Experimental design and optimization. Chemometrics Intellig Lab Syst 42:3–40

    CAS  Google Scholar 

  • Mapelli V, Olsson L, Nielsen J (2008) Metabolic footprinting in microbiology: methods and applications in functional genomics and biotechnology. Trends Biotechnol 26:490–497

    CAS  PubMed  Google Scholar 

  • Marschner P (2012) Mineral nutrition of higher plants. Elsevier, London

    Google Scholar 

  • Mitsuhashi J (1998) Polyamine as a growth promoter for cultured insect cells. Vitro Cell Dev Biol Anim 34:619–621

    CAS  Google Scholar 

  • Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, Bläsing O, Usadel B, Czechowski T, Udvardi MK, Stitt M (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30:85–112

    CAS  PubMed  Google Scholar 

  • Perkins MC, Woods HA, Harrison JF, Elser JJ (2004) Dietary phosphorus affects the growth of larval Manduca sexta. Arch Insect Biochem Physiol 55:153–168

    CAS  PubMed  Google Scholar 

  • Reich PB (2005) Global biogeography of plant chemistry: filling in the blanks. New Phytol 168:263–266

    CAS  PubMed  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006

    CAS  PubMed  Google Scholar 

  • Ribeiro DM, Silva Júnior DD, Cardoso FB, Martins AO, Silva WA, Nascimento VL, Araújo WL (2016) Growth inhibition by selenium is associated with changes in primary metabolism and nutrient levels in Arabidopsis thaliana. Plant Cell Environ 39:2235–2246

    CAS  PubMed  Google Scholar 

  • Rivas-Ubach A, Sardans J, Pérez-Trujillo M, Estiarte M, Peñuelas J (2012) Strong relationship between elemental stoichiometry and metabolome in plants. Proc Natl Acad Sci USA 109:4181–4186

    CAS  PubMed  Google Scholar 

  • Sanchez DH, Pieckenstain FL, Escaray F, Erban A, Kraemer U, Udvardi MK, Kopka J (2011) Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environ 34:605–617

    CAS  PubMed  Google Scholar 

  • Sardans J, Peñuelas J, Rivas-Ubach A (2011) Ecological metabolomics: overview of current developments and future challenges. Chemoecology 21:191–225

    CAS  Google Scholar 

  • Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett 6:96–101

    Google Scholar 

  • Shi C, Han R, Wu P, Fang M, Lai H, Shentu L (2011) Geochemistry and provenance of source rock for matoushan formation rocks (Late Cretaceous) in the Mouding area, Central Yunnan. Acta Sedimentol Sin 29:303–311

    CAS  Google Scholar 

  • Shi Z, Yu H, Sun Y, Yang C, Lian H, Cai P (2015) The energy metabolism in Caenorhabditis elegans under the extremely low-frequency electromagnetic field exposure. Sci Rep 5:8471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shim H, Fairlamb AH (1988) Levels of polyamines, glutathione and glutathione-spermidine conjugates during growth of the insect trypanosomatid Crithidia fasciculata. J Gen Microbiol 134:807–817

    CAS  PubMed  Google Scholar 

  • Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78:779–787. https://doi.org/10.1021/ac051437y

    Article  CAS  PubMed  Google Scholar 

  • Soetan KO, Olaiya CO, Oyewole OE (2010) The importance of mineral elements for humans, domestic animals and plants: a review. Afr J Food Sci 4:200–222

    CAS  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Sun X, Kang H, Kattge J, Gao Y, Liu C (2015) Biogeographic patterns of multi-element stoichiometry of Quercus variabilis leaves across China. Can J Forest Res 45:1827–1834

    CAS  Google Scholar 

  • Tao Y (2005) A proximate mathematical model of the content of main chemical constituents in an industrial phosphorus ore. Yunnan Geol 24:151–166

    Google Scholar 

  • Villas-Bôas SG, Mas S, Åkesson M, Smedsgaard J, Nielsen J (2005) Mass spectrometry in metabolome analysis. Mass Spectrom Rev 24:613–646

    PubMed  Google Scholar 

  • Wagner ND, Frost PC (2012) Responses of alkaline phosphatase activity in Daphnia to poor nutrition. Oecologia 170:1–10

    PubMed  Google Scholar 

  • Wagner ND, Lankadurai BP, Simpson MJ, Simpson AJ, Frost PC (2014) Metabolomic differentiation of nutritional stress in an aquatic invertebrate. Physiol Biochem Zoo 188:43–52

    Google Scholar 

  • Wagner ND, Yang Z, Scott AB, Frost PC (2017) Effects of algal food quality on free amino acid metabolism of Daphnia. Aquat Sci 79:127–137

    CAS  Google Scholar 

  • Want EJ, Masson P, Michopoulos F, Wilson ID, Theodoridis G, Plumb RS, Shockcor J, Loftus N, Holmes E, Nicholson JK (2013) Global metabolic profiling of animal and human tissues via UPLC–MS. Nat Protoc 8:17–32

    CAS  PubMed  Google Scholar 

  • Weider LJ, Lampert W, Wessels M, Colbourne JK, Limburg P (1997) Long-term genetic shifts in a microcrustacean egg bank associated with anthropogenic changes in the lake constance ecosystem. Proc R Soc Lond Ser B 264:1613–1618

    Google Scholar 

  • Wiklund S, Johansson E, Sjöström L, Mellerowicz EJ, Edlund U, Shockcor JP, Gottfries J, Moritz T, Trygg J (2008) Visualization of GC/TOF–MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models. Anal Chem 80:115–122

    CAS  PubMed  Google Scholar 

  • Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17. https://doi.org/10.1007/s00726-009-0269-0

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Zhu Y, Jiang H (1987) The vegetation of Yunnan. Science, Beijing

  • Wu D, Shen Q, Cai S, Chen Z, Dai F, Zhang G (2013) Ionomic responses and correlations between elements and metabolites under salt stress in wild and cultivated barley. Plant Cell Physiol 54:1976–1988

    CAS  PubMed  Google Scholar 

  • Xia J, Wishart DS (2010) MSEA: a web-based tool to identify biologically meaningful patterns in quantitative metabolomic data. Nucleic Acids Res 38:W71–W77. https://doi.org/10.1093/nar/gkq329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43:W251–W257. https://doi.org/10.1093/nar/gkv380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan K, Fu D, He F, Duan C (2011) Leaf nutrient stoichiometry of plants in the phosphorus-enriched soils of the Lake Dianchi watershed, southwestern China. Chin J Plant Ecol 35:353–361

    Google Scholar 

  • Yang SD, Lin T, Liu F, Liou CH (2006) Influence of dietary phosphorus levels on growth, metabolic response and body composition of juvenile silver perch (Bidyanus bidyanus). Aquaculture 253:592–601

    CAS  Google Scholar 

  • Zhang Z, Elser JJ, Cease AJ, Zhang X, Yu Q, Han X, Zhang G (2014) Grasshoppers regulate N: p stoichiometric homeostasis by changing phosphorus contents in their frass. PLoS One 9:e103697

    PubMed  PubMed Central  Google Scholar 

  • Zhou X, Sun X, Du B, Yin S, Liu C (2015) Multielement stoichiometry in Quercus variabilis under natural phosphorus variation in subtropical China. Sci Rep 5:7839

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This study was funded by the National Natural Science Foundation of China (31670626, 31270640, and 31070532) and the National Key R&D Program of China (2017YFC0505501). We thank the Instrumental Analysis Center of Shanghai Jiao Tong University for the support on chemical analysis.

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Authors and Affiliations

  1. School of Agriculture and Biology, Shanghai Jiao Tong University, Dongchuan Rd. 800, Shanghai, 200240, China

    Huawei Ji, Baoming Du, Jiahao Wen, Ningxiao Sun & Chunjiang Liu

  2. Shanghai Urban Forest Research Station, State Forestry Administration, Dongchuan Rd. 800, Shanghai, 200240, China

    Huawei Ji, Baoming Du, Jiahao Wen, Ningxiao Sun & Chunjiang Liu

  3. Yunnan Academy of Forestry, Lanan Rd. 2, Kunming, 600000, Yunnan, China

    Mingjun Peng

  4. Shanghai Jiao Tong University, Dongchuan Rd. 800, Shanghai, 200240, China

    Hongmei Du

  5. Key Laboratory of Urban Agriculture (South), Ministry of Agriculture, Dongchuan Rd. 800, Shanghai, 200240, China

    Chunjiang Liu

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  1. Huawei Ji
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Contributions

C. Liu conceived and designed the experiments and wrote the manuscript. J. Wen, B. Du, N. Sun, and M. Peng performed the experiments. H. Ji and H. Du performed the experiments, analyzed the data, and wrote the manuscript.

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Correspondence to Chunjiang Liu.

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Ji, H., Du, B., Wen, J. et al. Metabolome and ionome analyses reveal the stoichiometric effects of contrasting geological phosphorus soils on seed-parasitic insects in subtropical oak forests. Chemoecology 29, 199–210 (2019). https://doi.org/10.1007/s00049-019-00290-4

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