The effect of elevated CO2 and virus infection on the primary metabolism of wheat
Simone Vassiliadis A B , Kim M. Plummer C , Kevin S. Powell D , Piotr Trębicki E , Jo E. Luck F and Simone J. Rochfort A B G
+ Author Affiliations
- Author Affiliations
A Department of Economic Development, Jobs, Transport and Resources (DEDJTR), Molecular Phenomics, AgriBio, 5 Ring Road, Bundoora, Vic. 3083, Australia.
B School of Applied Systems Biology, AgriBio, La Trobe University, Bundoora, Vic. 3083, Australia.
C Department of Animal, Plant and Soil Sciences, La Trobe University, Bundoora, Vic. 3083, Australia.
D DEDJTR, Biosciences Research, Rutherglen Centre, 124 Chiltern Valley Road, Rutherglen, Vic. 3685, Australia.
E DEDJTR, Biosciences Research, Horsham Centre, 110 Natimuk Road, Horsham, Vic. 3685, Australia.
F Plant Biosecurity Cooperative Research Centre, The University of Melbourne, Burnley Campus, 500 Yarra Boulevard, Richmond, Vic. 3121, Australia.
G Corresponding author. Email: simone.rochfort@ecodev.vic.gov.au
Functional Plant Biology 43(9) 892-902 https://doi.org/10.1071/FP15242
Submitted: 17 August 2015 Accepted: 25 May 2016 Published: 27 June 2016
Abstract
Atmospheric CO2 concentrations are predicted to double by the end of this century. Although the effects of CO2 fertilisation in crop systems have been well studied, little is known about the specific interactions among plants, pests and pathogens under a changing climate. This growth chamber study focuses on the interactions among Barley yellow dwarf virus (BYDV), its aphid vector (Rhopalosiphum padi) and wheat (Triticum aestivum L. cv. Yitpi) under ambient (aCO2; 400 µmol mol–1) or elevated (eCO2; 650 µmol mol–1) CO2 concentrations. eCO2 increased the tiller number and biomass of uninoculated plants and advanced the yellowing symptoms of infected plants. Total foliar C content (percentage of the total DW) increased with eCO2 and with sham inoculation (exposed to early herbivory), whereas total N content decreased with eCO2. Liquid chromatography–mass spectrometry approaches were used to quantify the products of primary plant metabolism. eCO2 significantly increased sugars (fructose, mannitol and trehalose), irrespective of disease status, whereas virus infection significantly increased the amino acids essential to aphid diet (histidine, lysine, phenylalanine and tryptophan) irrespective of CO2 concentration. Citric acid was reduced by both eCO2 and virus infection. Both the potential positive and negative biochemical impacts on wheat, aphid and BYDV interactions are discussed.
Additional keywords: aphid, Barley yellow dwarf virus, pathogen, pest, Rhopalosiphum padi, Triticum aestivum.
References
Aghdasi M, Smeekens S, Schluepman H (2008) Microarray analysis of gene expression patterns in Arabidopsis seedlings under trehalose, sucrose and sorbitol treatment. International Journal of Plant Production 2, 309–320.Ajayi O (1986) The effect of barley yellow dwarf virus on the amino acid composition of spring wheat. Annals of Applied Biology 108, 145–149.
| The effect of barley yellow dwarf virus on the amino acid composition of spring wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XkvFClsbg%3D&md5=379becd6845ca066d1172b17ecb87bc4CAS |
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology 47, 817–844.
| Host plant quality and fecundity in herbivorous insects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVWlug%3D%3D&md5=87329449488ddea7c33a164de4d1b08bCAS | 11729092PubMed |
Awmack CS, Harrington R, Leather SR, Lawton JH (1996) The impacts of elevated CO2 on aphid–plant interactions. In ‘Implications of global environmental change for crops in Europe – Vol. 45’. (Eds R Froud-Williams, R Harrington, T Hocking, H Smith, T Thomas.) pp. 317–322. (Aspects of Applied Biology: Cambridge, UK)
Banks P, Waterhouse P, Larkin P (1992) Pathogenicity of three RPV isolates of Barley Yellow Dwarf Virus on barley, wheat and wheat alien addition lines. Annals of Applied Biology 121, 305–314.
| Pathogenicity of three RPV isolates of Barley Yellow Dwarf Virus on barley, wheat and wheat alien addition lines.Crossref | GoogleScholarGoogle Scholar |
Barbehenn RV, Chen Z, Karowe DN, Spickard A (2004) C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2. Global Change Biology 10, 1565–1575.
| C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar |
Burke DG, Hilliard E, Watkins K, Russ V, Scott BJ (1985) Determination of organic acids in seven wheat varieties by capillary gas chromatography. Analytical Biochemistry 149, 421–429.
| Determination of organic acids in seven wheat varieties by capillary gas chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltF2itr0%3D&md5=8b158e9b167c8ca910d7d1f53dc82387CAS | 4073499PubMed |
Chakraborty S, Newton AC (2011) Climate change, plant diseases and food security: an overview. Plant Pathology 60, 2–14.
| Climate change, plant diseases and food security: an overview.Crossref | GoogleScholarGoogle Scholar |
Chakraborty S, Luck J, Hollaway G, Freeman A, Norton R, Garrett KA, Percy K, Hopkins A, Davis C, Karnosky DF (2008) Impacts of global change on diseases of agricultural crops and forest trees. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 3, 1–15.
| Impacts of global change on diseases of agricultural crops and forest trees.Crossref | GoogleScholarGoogle Scholar |
Conroy J, Hocking P (1993) Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations. Physiologia Plantarum 89, 570–576.
| Nitrogen nutrition of C3 plants at elevated atmospheric CO2 concentrations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXns1CrtA%3D%3D&md5=5c28e52d7b342ff120c778f4a96143f5CAS |
Conroy JP, Seneweera S, Basra AS, Rogers G, Nissen-Wooller B (1994) Influence of rising atmospheric CO2 concentrations and temperature on growth, yield and grain quality of cereal crops. Functional Plant Biology 21, 741–758.
D’Arcy CJ (1995) Symptomatology and host range of barley yellow dwarf. In ‘Barley yellow dwarf: 40 years of progress’. (Eds CJ D’Arcy, PA Burnett.) pp. 9–28. (American Phytopathological Society: St Paul, MN)
Dadd RH (1985) Nutrition: organisms. In ‘Comprehensive insect physiology, biochemistry and pharmacology. Vol. 4’. (Eds G Kerkut, L Gilbert.) pp. 313–390. (Pergamon Press: Oxford, UK)
Dáder B, Fereres A, Moreno A, Trębicki P (2016) Elevated CO2 impacts bell pepper growth with consequences to Myzus persicae life history, feeding behaviour and virus transmission ability. Scientific Reports 6,
| Elevated CO2 impacts bell pepper growth with consequences to Myzus persicae life history, feeding behaviour and virus transmission ability.Crossref | GoogleScholarGoogle Scholar | 26941044PubMed |
De Barro PJ (1991) Attractiveness of four colours of traps to cereal aphids (Hemiptera: Aphididae) in South Australia. Australian Journal of Entomology 30, 263–264.
| Attractiveness of four colours of traps to cereal aphids (Hemiptera: Aphididae) in South Australia.Crossref | GoogleScholarGoogle Scholar |
Douglas AE (2003) The nutritional physiology of aphids. Advances in Insect Physiology 31, 73–140.
| The nutritional physiology of aphids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtFOm&md5=acad35dccd5239a58a1a7515b2c2f78bCAS |
Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annual Review of Plant Biology 48, 609–639.
| More efficient plants: a consequence of rising atmospheric CO2?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1eltbY%3D&md5=862c5c6600bd48f8ee77fe979b94e75cCAS |
Esau K (1957) Phloem degeneration in Gramineae affected by the barley yellow-dwarf virus. American Journal of Botany 44, 245–251.
| Phloem degeneration in Gramineae affected by the barley yellow-dwarf virus.Crossref | GoogleScholarGoogle Scholar |
Farrar J, Williams M (1991) The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source–sink relations and respiration. Plant, Cell & Environment 14, 819–830.
| The effects of increased atmospheric carbon dioxide and temperature on carbon partitioning, source–sink relations and respiration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xht1Crs7o%3D&md5=0a0c8e2d6ed5e9703147021398a8258fCAS |
Fernando N, Panozzo J, Tausz M, Norton RM, Neumann N, Fitzgerald GJ, Seneweera S (2014) Elevated CO2 alters grain quality of two bread wheat cultivars grown under different environmental conditions. Agriculture, Ecosystems & Environment 185, 24–33.
| Elevated CO2 alters grain quality of two bread wheat cultivars grown under different environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkslSqurs%3D&md5=4d6fb72cf6154411acc79e4d7ec8c83aCAS |
Fiebig M, Poehling HM, Borgemeister C (2004) Barley yellow dwarf virus, wheat, and Sitobion avenae: a case of trilateral interactions. Entomologia Experimentalis et Applicata 110, 11–21.
| Barley yellow dwarf virus, wheat, and Sitobion avenae: a case of trilateral interactions.Crossref | GoogleScholarGoogle Scholar |
Freeman AJ, Aftab M (2011) Effective management of viruses in pulse crops in south eastern Australia should include management of weeds. Australasian Plant Pathology 40, 430–441.
| Effective management of viruses in pulse crops in south eastern Australia should include management of weeds.Crossref | GoogleScholarGoogle Scholar |
Fuhrer J (2003) Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change. Agriculture, Ecosystems & Environment 97, 1–20.
| Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVCmsb4%3D&md5=623b5e8737ff2bb36e8ced34d0a8e020CAS |
Geiger M, Walch‐Liu P, Engels C, Harnecker J, Schulze ED, Ludewig F, Sonnewald U, Scheible WR, Stitt M (1998) Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in young tobacco plants. Plant, Cell & Environment 21, 253–268.
| Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in young tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVCjtrk%3D&md5=69e382e63f0044e40ef27fae0c85a212CAS |
Gray S, Gildow FE (2003) Luteovirus–aphid interactions. Annual Review of Phytopathology 41, 539–566.
| Luteovirus–aphid interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFWlsbc%3D&md5=1a2cc5dbb55be070557cbbd6929b2ab0CAS | 12730400PubMed |
Hawker J (1985) Sucrose. In ‘Biochemistry of storage carbohydrates in green plants’. (Eds PM Dey, R Dixon.) pp. 1–51. (Academic Press: London)
Hikosaka K, Onoda Y, Kinugasa T, Nagashima H, Anten NPR, Hirose T (2005) Plant responses to elevated CO2 concentration at different scales: leaf, whole plant, canopy, and population. Ecological Research 20, 243–253.
| Plant responses to elevated CO2 concentration at different scales: leaf, whole plant, canopy, and population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlCntb0%3D&md5=1f33ec28e9dc6adb6033912058241d5eCAS |
Hodge S, Ward JL, Beale MH, Bennett M, Mansfield JW, Powell G (2013) Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237, 1057–1064.
| Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFKmurc%3D&md5=3e21b560f40f61ac9b4c51517dd79cc7CAS | 23242075PubMed |
Ingwell LL, Eigenbrode SD, Bosque-Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Scientific Reports 2, 1–6.
| Plant viruses alter insect behavior to enhance their spread.Crossref | GoogleScholarGoogle Scholar |
Intergovernmental Panel on Climate Change (2013) ‘Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change.’ (Cambridge University Press: Cambridge, UK)
Irwin ME, Thresh JM (1990) Epidemiology of barley yellow dwarf: a study in ecological complexity. Annual Review of Phytopathology 28, 393–424.
| Epidemiology of barley yellow dwarf: a study in ecological complexity.Crossref | GoogleScholarGoogle Scholar |
Jensen SG, D’Arcy CJ (1995) Effects of barley yellow dwarf on host plants. In ‘Barley yellow dwarf: 40 years of progress. Vol. 40’. (Eds CJ D’Arcy, PA Burnett.) pp. 55–74. (American Phytopathological Society: St Paul, MN)
Jiménez-Martínez ES, Bosque-Pérez NA, Berger PH, Zemetra RS, Ding H, Eigenbrode SD (2004) Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental Entomology 33, 1207–1216.
| Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat.Crossref | GoogleScholarGoogle Scholar |
Kazemi MH, van Emden HF (1992) Partial antibiosis to Rhopalosiphum padi in wheat and some phytochemical correlations. Annals of Applied Biology 121, 1–9.
| Partial antibiosis to Rhopalosiphum padi in wheat and some phytochemical correlations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXht1Wgsrc%3D&md5=4d4216b953bf9868cceb7827914747feCAS |
Khattab H (2007) The defense mechanism of cabbage plant against phloem-sucking aphid (Brevicoryne brassicae L.). Australian Journal of Basic and Applied Sciences 1, 56–62.
Kimball BA, Pinter P, Garcia RL, LaMorte RL, Wall GW, Hunsaker DJ, Wechsung G, Wechsung F (1995) Productivity and water use of wheat under free-air CO2 enrichment. Global Change Biology 1, 429–442.
| Productivity and water use of wheat under free-air CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |
Kimball BA, Kobayashi K, Bindi M (2002) Responses of agricultural crops to free-air CO2 enrichment. Advances in Agronomy 77, 293–368.
| Responses of agricultural crops to free-air CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |
Krumbein A, Kläring H-P, Schonhof I, Schreiner M (2010) Atmospheric carbon dioxide changes photochemical activity, soluble sugars and volatile levels in broccoli (Brassica oleracea var. italica). Journal of Agricultural and Food Chemistry 58, 3747–3752.
| Atmospheric carbon dioxide changes photochemical activity, soluble sugars and volatile levels in broccoli (Brassica oleracea var. italica).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvF2ksr8%3D&md5=500c3fd6d336ee243fb0c5cf0f626e7bCAS | 20158238PubMed |
Leckstein P, Llewellyn M (1974) The role of amino acids in diet intake and selection and the utilization of dipeptides by Aphis fabae. Journal of Insect Physiology 20, 877–885.
| The role of amino acids in diet intake and selection and the utilization of dipeptides by Aphis fabae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXktlKksLk%3D&md5=23173dd918a8201e3e80eda9fcf304bdCAS | 4840687PubMed |
Li F, Kang S, Zhang J (2004) Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat. Agricultural Water Management 67, 221–233.
| Interactive effects of elevated CO2, nitrogen and drought on leaf area, stomatal conductance, and evapotranspiration of wheat.Crossref | GoogleScholarGoogle Scholar |
Liu Z, Rochfort S (2013) A fast liquid chromatography mass spectrometry (LC-MS) method for quantification of major polar metabolites in plants. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences 912, 8–15.
| A fast liquid chromatography mass spectrometry (LC-MS) method for quantification of major polar metabolites in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVSgsg%3D%3D&md5=2436cdbbe3502ce80c39345a6749481fCAS | 23246845PubMed |
Livingston DP, Gildow FE (1991) Barley yellow dwarf virus effects on fructan and sugar concentration in winter oat crowns. Crop Science 31, 1081–1082.
| Barley yellow dwarf virus effects on fructan and sugar concentration in winter oat crowns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmslGqtbY%3D&md5=6d5a779c530c54f54aee85272f450e85CAS |
Lokeshwari D, Verghese A, Shivashankar S, Kumar NKK, Manjunatha H, Venugopalan R (2014) Effect of Aphis odinae (Hemiptera: Aphididae) infestation on sugars and amino acid content in mango. African Entomology 22, 823–827.
| Effect of Aphis odinae (Hemiptera: Aphididae) infestation on sugars and amino acid content in mango.Crossref | GoogleScholarGoogle Scholar |
López-Bucio J, Nieto-Jacobo MF, Ramírez-Rodríguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Science 160, 1–13.
| Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils.Crossref | GoogleScholarGoogle Scholar | 11164572PubMed |
Luck J, Spackman M, Freeman A, Griffiths W, Finlay K, Chakraborty S (2011) Climate change and diseases of food crops. Plant Pathology 60, 113–121.
| Climate change and diseases of food crops.Crossref | GoogleScholarGoogle Scholar |
Macedo TB, Peterson RKD, Weaver DK, Ni X (2009) Impact of Diuraphis noxia and Rhopalosiphum padi (Hemiptera: Aphididae) on primary physiology of four near-isogenic wheat lines. Journal of Economic Entomology 102, 412–421.
| Impact of Diuraphis noxia and Rhopalosiphum padi (Hemiptera: Aphididae) on primary physiology of four near-isogenic wheat lines.Crossref | GoogleScholarGoogle Scholar | 19253663PubMed |
Malmström CM, Field CB (1997) Virus-induced differences in the response of oat plants to elevated carbon dioxide. Plant, Cell & Environment 20, 178–188.
| Virus-induced differences in the response of oat plants to elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Medina-Ortega KJ, Bosque-Pérez NA, Ngumbi E, Jiménez-Martínez ES, Eigenbrode SD (2009) Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from Barley yellow dwarf virus-infected wheat. Environmental Entomology 38, 836–845.
| Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from Barley yellow dwarf virus-infected wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVCnt74%3D&md5=c567da7056244753a0a777ba01edbe7fCAS | 19508794PubMed |
Moriones E, Ortego F, Ruiz-Tapiador M, Gutiérrez C, Castañera P, García-Arenal F (1993) Epidemiology of RPV-and PAV-like barley yellow dwarf viruses on winter barley in central Spain. Crop Protection 12, 224–228.
| Epidemiology of RPV-and PAV-like barley yellow dwarf viruses on winter barley in central Spain.Crossref | GoogleScholarGoogle Scholar |
Nancarrow N, Constable FE, Finlay KJ, Freeman AJ, Rodoni BC, Trebicki P, Vassiliadis S, Yen AL, Luck JE (2014) The effect of elevated temperature on Barley yellow dwarf virus-PAV in wheat. Virus Research 186, 97–103.
| The effect of elevated temperature on Barley yellow dwarf virus-PAV in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtV2qtbk%3D&md5=19a78662d22f40782dd6177c10bc2f80CAS | 24374266PubMed |
Oehme V, Högy P, Zebitz CPW, Fangmeier A (2013) Effects of elevated atmospheric CO2 concentrations on phloem sap composition of spring crops and aphid performance. Journal of Plant Interactions 8, 74–84.
| Effects of elevated atmospheric CO2 concentrations on phloem sap composition of spring crops and aphid performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1ShtrfM&md5=45e90ebff542a15668841cca54ec1d40CAS |
R Development Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.r-project.org/ [Verified 31 May 2016]
Reich PB, Hungate BA, Luo Y (2006) Carbon–nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annual Review of Ecology Evolution and Systematics 37, 611–636.
| Carbon–nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide.Crossref | GoogleScholarGoogle Scholar |
Rustamani MA, Kanehisa K, Tsumuki H (1992a) Aconitic acid content of some cereals and its effect on aphids. Applied Entomology and Zoology 27, 79–87.
Rustamani MA, Kanehisa K, Tsumuki H, Shiraga T (1992b) Further observations on the relationship between aconitic acid contents and aphid densities on some cereal plants. Bulletin of the Research Institute for Bioresources 1, 9–20.
Sandström J, Moran N (1999) How nutritionally imbalanced is phloem sap for aphids? Entomologia Experimentalis et Applicata 91, 203–210.
| How nutritionally imbalanced is phloem sap for aphids?Crossref | GoogleScholarGoogle Scholar |
Seneweera SP, Conroy JP, Ishunaru K, Ghannoum O, Okada M, Lieffering M, Han Yong K, Kobayashi K (2002) Changes in source–sink relations during development influence photosynthetic acclimation of rice to free air CO2 enrichment (FACE). Functional Plant Biology 29, 945–953.
| Changes in source–sink relations during development influence photosynthetic acclimation of rice to free air CO2 enrichment (FACE).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntFyqtL0%3D&md5=93637569c65585f64f51c358bba96981CAS |
Sicher RC (2008) Effects of CO2 enrichment on soluble amino acids and organic acids in barley primary leaves as a function of age, photoperiod and chlorosis. Plant Science 174, 576–582.
| Effects of CO2 enrichment on soluble amino acids and organic acids in barley primary leaves as a function of age, photoperiod and chlorosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslynsLs%3D&md5=3536d03fc333a611b3de211b294cbf7cCAS |
Sicher RC (2010) Daily changes of amino acids in soybean leaflets are modified by CO2 enrichment. International Journal of Plant Biology 1, 89–93.
| Daily changes of amino acids in soybean leaflets are modified by CO2 enrichment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGju7%2FP&md5=d982ad74021390fd62c04352258679a7CAS |
Smith PR, Sward RJ (1982) Crop loss assessment studies on the effects of barley yellow dwarf virus in wheat in Victoria. Crop and Pasture Science 33, 179–185.
| Crop loss assessment studies on the effects of barley yellow dwarf virus in wheat in Victoria.Crossref | GoogleScholarGoogle Scholar |
Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Global Change Biology 13, 1823–1842.
| How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance.Crossref | GoogleScholarGoogle Scholar |
Sun YC, Ge F (2011) How do aphids respond to elevated CO2? Journal of Asia-Pacific Entomology 14, 217–220.
| How do aphids respond to elevated CO2?Crossref | GoogleScholarGoogle Scholar |
Sun YC, Chen FJ, Ge F (2009a) Elevated CO2 changes interspecific competition among three species of wheat aphids: Sitobion avenae, Rhopalosiphum padi, and Schizaphis graminum. Environmental Entomology 38, 26–34.
| Elevated CO2 changes interspecific competition among three species of wheat aphids: Sitobion avenae, Rhopalosiphum padi, and Schizaphis graminum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjs1Kht7s%3D&md5=7e5907146592d5770bb929337f1675edCAS | 19791595PubMed |
Sun YC, Jing BB, Ge F (2009b) Response of amino acid changes in Aphis gossypii (Glover) to elevated CO2 levels. Journal of Applied Entomology 133, 189–197.
| Response of amino acid changes in Aphis gossypii (Glover) to elevated CO2 levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksF2hu78%3D&md5=1452bfd0c2112e950a6a209307da632dCAS |
Trębicki P, Nancarrow N, Cole E, Bosque‐Pérez NA, Constable FE, Freeman AJ, Rodoni B, Yen AL, Luck JE, Fitzgerald GJ (2015) Virus disease in wheat predicted to increase with a changing climate. Global Change Biology 21, 3511–3519.
| Virus disease in wheat predicted to increase with a changing climate.Crossref | GoogleScholarGoogle Scholar | 25846559PubMed |
Trębicki P, Vandegeer RK, Bosque-Pérez NA, Powell KS, Dader B, Freeman AJ, Yen AL, Fitzgerald GJ, Luck JE (2016) Virus infection mediates the effects of elevated CO2 on plants and vectors. Scientific Reports 6,
| Virus infection mediates the effects of elevated CO2 on plants and vectors.Crossref | GoogleScholarGoogle Scholar | 26941044PubMed |
Watt AD, Whittaker JB, Docherty M, Brooks G, Lindsay E, Salt DT (1995) The impact of elevated atmospheric CO2 on insect herbivores. In ‘Insects in a changing environment: Symposium of the Royal Entomological Society’. (Eds R Harrington, NE Stork) pp. 197–217. (Academic Press: London)
Weibull JHW (1988) Free amino acids in the phloem sap from oats and barley resistant to Rhopalosiphum padi. Phytochemistry 27, 2069–2072.
| Free amino acids in the phloem sap from oats and barley resistant to Rhopalosiphum padi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXltVOkt7g%3D&md5=c5fe9959697bf97870e80948ee379319CAS |
Yoshihara T, Sogawa K, Pathak M, Juliano B, Sakamura S (1980) Oxalic acid as a sucking inhibitor of the brown planthopper in rice (Delphacidae, Homoptera). Entomologia Experimentalis et Applicata 27, 149–155.
| Oxalic acid as a sucking inhibitor of the brown planthopper in rice (Delphacidae, Homoptera).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXkt1Sksrc%3D&md5=763675ca2feb404353a9b8a044b4a10aCAS |
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Research 14, 415–421.
| A decimal code for the growth stages of cereals.Crossref | GoogleScholarGoogle Scholar |
