Leaf UV-B Irradiation and Mycorrhizal Symbionts Affect Lettuce VOC Emissions and Defence Mechanisms, but Not Aphid Feeding Preferences

Simple Summary Arbuscular mycorrhizal fungi (AMF), as well as ultraviolet-B radiation (UV-B), could act as key factors affecting plant–insect interactions. The stress related to one of these two factors could be balanced by the positive effects of the other. In the present work, the feeding preferences of Myzus persicae aphids for lettuce plants exposed to two abiotic factors, i.e., AMF and UV-B, singly or in combination, was evaluated. Results showed that lettuce plants treated with UV-B increased in callose and oxidative stress indicators, signalling an alteration in the volatile organic compounds (VOCs) emitted. On the other hand, the negative effects of UV-B were partially mitigated in lettuces inoculated with AMF. Differently treated lettuces did not affect the feeding preferences of the M. persicae aphid population. Overall, this study shed light on how UV-B and AMF impact lettuce VOCs emission and defence mechanisms, but not the feeding behaviour of a polyphagous aphid species. Abstract Arbuscular mycorrhizal fungi (AMF) and ultraviolet-B radiation (UV-B) play important roles in plant–insect interactions by altering plant physiology and histology. We hypothesized that UV-B-induced oxidative stress was mitigated by AMF symbiosis. In this study, we conducted a multifactorial experiment to explore lettuce plant response to AMF inoculation and UV-B exposure (0.4 W m−2; 16 h d−1; 2 weeks), either together or individually, as well as the interaction with the polyphagous insect pest Myzus persicae (Sulzer). Lettuce plants subjected to UV-B radiation showed an increase in callose and oxidative stress indicators, as well as a decrease in stomatal density. Mycorrhizal colonization cancelled out the effect of UV-B on stomatal density, while the symbiosis was not affected by UV-B treatment. The plant volatile emission was significantly altered by UV-B treatment. Specifically, the non-terpene 1-undecene abundance (+M/+UVB: 48.0 ± 7.78%; −M/+UVB: 56.6 ± 14.90%) was increased, whereas the content of the non-terpene aldehydes decanal (+M/+UVB: 8.50 ± 3.90%; −M/+UVB: 8.0 ± 4.87%) and undecanal (+M/+UVB: 2.1 ± 0.65%; −M/+UVB: 1.20 ± 1.18%) and the sesquiterpene hydrocarbons (+M/+UVB: 18.0 ± 9.62 %; −M/+UVB: 19.2 ± 5.90%) was decreased. Mycorrhization, on the other hand, had no significant effect on the plant volatilome, regardless of UV-B treatment. Aphid population was unaffected by any of the treatments, implying a neutral plant response. Overall, this study provides new insights about the interactions among plants, UV-B, and AMF, outlining their limited impact on a polyphagous insect pest.

[1]  Y. Tamai,et al.  Single and combined effects of fertilization, ectomycorrhizal inoculation, and drought on container-grown Japanese larch seedlings , 2022, Journal of Forestry Research.

[2]  S. Scott,et al.  Prunus persica (Peach) , 2022, Encyclopedia of Plant Viruses and Viroids.

[3]  G. Flamini,et al.  Comparison of the Chemical and Sensorial Evaluation of Dark Chocolate Bars , 2021, Applied Sciences.

[4]  H. Matsuura,et al.  Plant-insect communication in urban forests: Similarities of plant volatile compositions among tree species (host vs. non-host trees) for alder leaf beetle Agelastica coerulea. , 2021, Environmental research.

[5]  O. Oguntibeju,et al.  Evaluating the Endophytic Activities of Beauveria bassiana on the Physiology, Growth, and Antioxidant Activities of Extracts of Lettuce (Lactuca sativa L.) , 2021, Plants.

[6]  D. Jaiswal,et al.  Ultraviolet-B induced changes in physiology, phenylpropanoid pathway, and essential oil composition in two Curcuma species (C. caesia Roxb. and C. longa L.). , 2021, Ecotoxicology and environmental safety.

[7]  H. Matsuura,et al.  Ozone disrupts the communication between plants and insects in urban and suburban areas: an updated insight on plant volatiles , 2021, Journal of Forestry Research.

[8]  Ninkovic Velemir,et al.  Plant volatiles as cues and signals in plant communication. , 2020, Plant, cell & environment.

[9]  Sofie Meeus,et al.  From leaf to label: A robust automated workflow for stomata detection , 2020, Ecology and evolution.

[10]  K. Kuča,et al.  Unraveling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. , 2020, Plant biology.

[11]  C. D'onofrio,et al.  The arbuscular mycorrhizal fungus Funneliformis mosseae induces changes and increases the concentration of volatile organic compounds in Vitis vinifera cv. Sangiovese leaf tissue. , 2020, Plant physiology and biochemistry : PPB.

[12]  J. T. Puthur,et al.  UV-B Priming of Oryza sativa Seeds Augments the Innate Tolerance Potential in a Tolerant Variety more Effectively Toward NaCl and PEG Stressors , 2020, Journal of Plant Growth Regulation.

[13]  J. T. Puthur,et al.  UV-B priming enhances specific secondary metabolites in Oryza sativa (L.) empowering to encounter diverse abiotic stresses , 2020, Plant Growth Regulation.

[14]  S. B. Agrawal,et al.  Effect on essential oil components and wedelolactone content of a medicinal plant Eclipta alba due to modifications in the growth and morphology under different exposures of ultraviolet-B , 2020, Physiology and Molecular Biology of Plants.

[15]  R. Kariyat,et al.  Arbuscular mycorrhizal fungi (AMF) influences growth and insect community dynamics in Sorghum-sudangrass (Sorghum x drummondii) , 2020, Arthropod-Plant Interactions.

[16]  Husna,et al.  The potential of arbuscular mycorrhizal fungi to conserve Kalappia celebica, an endangered endemic legume on gold mine tailings in Sulawesi, Indonesia , 2020, Journal of Forestry Research.

[17]  C. D'onofrio,et al.  Responses of Vitis vinifera cv. Cabernet Sauvignon roots to the arbuscular mycorrhizal fungus Funneliformis mosseae and the plant growth-promoting rhizobacterium Ensifer meliloti include changes in volatile organic compounds , 2020, Mycorrhiza.

[18]  J. T. Puthur,et al.  Effect of UV-B priming on the abiotic stress tolerance of stress-sensitive rice seedlings: Priming imprints and cross-tolerance. , 2019, Plant physiology and biochemistry : PPB.

[19]  J. T. Puthur,et al.  Amplification of abiotic stress tolerance potential in rice seedlings with a low dose of UV-B seed priming. , 2019, Functional plant biology : FPB.

[20]  G. Benelli,et al.  Prey selection behaviour in the multicoloured Asian ladybird, Harmonia axyridis (Coleoptera: Coccinellidae) , 2019, Applied Entomology and Zoology.

[21]  I. Khan,et al.  Host Selection Behavior of the Green Peach Aphid, Myzus persicae, in Response to Volatile Organic Compounds and Nitrogen Contents of Cabbage Cultivars , 2019, Front. Plant Sci..

[22]  D. Reinhardt,et al.  Beneficial Services of Arbuscular Mycorrhizal Fungi – From Ecology to Application , 2018, Front. Plant Sci..

[23]  A. Turrini,et al.  Designing the Ideotype Mycorrhizal Symbionts for the Production of Healthy Food , 2018, Front. Plant Sci..

[24]  T. M. Bezemer,et al.  Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology , 2018, Front. Ecol. Evol..

[25]  S. Karpiński,et al.  Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses , 2018, Free radical biology & medicine.

[26]  G. Flamini,et al.  VOCs as fingerprints for the chemical profiling of hashish samples analyzed by HS-SPME/GC–MS and multivariate statistical tools , 2018, Forensic Toxicology.

[27]  Sorina C. Popescu,et al.  The Arabidopsis thaliana Knockout Mutant for Phytochelatin Synthase1 (cad1-3) Is Defective in Callose Deposition, Bacterial Pathogen Defense and Auxin Content, But Shows an Increased Stem Lignification , 2018, Front. Plant Sci..

[28]  M. Erb,et al.  Tritrophic Interactions Mediated by Herbivore-Induced Plant Volatiles: Mechanisms, Ecological Relevance, and Application Potential. , 2018, Annual review of entomology.

[29]  Xu-dong Zhu,et al.  Ultraviolet-B enhances the resistance of multiple plant species to lepidopteran insect herbivory through the jasmonic acid pathway , 2018, Scientific Reports.

[30]  A. Turrini,et al.  Transcriptome changes induced by arbuscular mycorrhizal fungi in sunflower (Helianthus annuus L.) roots , 2018, Scientific Reports.

[31]  M. Giovannetti,et al.  Arbuscular mycorrhizal fungi alter the content and composition of secondary metabolites in Bituminaria bituminosa L. , 2017, Plant biology.

[32]  G. Jenkins.  Photomorphogenic responses to ultraviolet-B light. , 2017, Plant, cell & environment.

[33]  M. Giovannetti,et al.  Arbuscular mycorrhizal fungi affect total phenolics content and antioxidant activity in leaves of oak leaf lettuce varieties , 2017 .

[34]  P. Klinkhamer,et al.  Interactive Effects of UV-B Light with Abiotic Factors on Plant Growth and Chemistry, and Their Consequences for Defense against Arthropod Herbivores , 2017, Front. Plant Sci..

[35]  R. Kapoor,et al.  Terpenoids in plant and arbuscular mycorrhiza‐reinforced defence against herbivorous insects , 2017, Annals of botany.

[36]  R. Visser,et al.  Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism , 2016, Journal of experimental botany.

[37]  T. Rose,et al.  Arbuscular mycorrhizal fungi: effects on plant terpenoid accumulation. , 2016, Plant biology.

[38]  E. Guerrieri,et al.  Insights on the Impact of Arbuscular Mycorrhizal Symbiosis on Tomato Tolerance to Water Stress1[OPEN] , 2016, Plant Physiology.

[39]  L. Miozzi,et al.  Novel functional microRNAs from virus-free and infected Vitis vinifera plants under water stress , 2016, Scientific Reports.

[40]  I. Garmendia,et al.  Selenium fertilization and mycorrhizal technology may interfere in enhancing bioactive compounds in edible tissues of lettuces , 2015 .

[41]  F. Lescourret,et al.  Efficacy of pest and pathogen control, yield and quality of winter lettuce crops managed with reduced pesticide applications , 2015 .

[42]  M. Buiatti,et al.  The rat glucocorticoid receptor integration in Nicotiana langsdorffii genome affects plant responses to abiotic stresses and to arbuscular mycorrhizal symbiosis , 2015, Plant Biotechnology Reports.

[43]  T. Matthew Robson,et al.  Re-interpreting plant morphological responses to UV-B radiation. , 2015, Plant, cell & environment.

[44]  T. Köllner,et al.  Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect , 2015, Symbiosis.

[45]  Javier Martínez-Abaigar,et al.  UV‐B Induced Secondary Plant Metabolites , 2014 .

[46]  I. Garmendia,et al.  The arbuscular mycorrhizal symbiosis can overcome reductions in yield and nutritional quality in greenhouse-lettuces cultivated at inappropriate growing seasons , 2013 .

[47]  S. Dorn,et al.  Elevated carbon dioxide impairs the performance of a specialized parasitoid of an aphid host feeding on Brassica plants , 2013 .

[48]  B. Jordan,et al.  From ozone depletion to agriculture: understanding the role of UV radiation in sustainable crop production. , 2013, The New phytologist.

[49]  J. O’Brien,et al.  Detection of Hydrogen Peroxide by DAB Staining in Arabidopsis Leaves. , 2012, Bio-protocol.

[50]  M. Mescher,et al.  Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. , 2012, Insect biochemistry and molecular biology.

[51]  I. Kreft,et al.  UV-B radiation affects flavonoids and fungal colonisation in Fagopyrum esculentum and F. tataricum , 2012, Central European Journal of Biology.

[52]  D. Bergmann,et al.  Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway , 2011, Nature.

[53]  Gokare A. Ravishankar,et al.  Influence of abiotic stress signals on secondary metabolites in plants , 2011, Plant signaling & behavior.

[54]  M. Sánchez-Díaz,et al.  Improvement of nutritional quality of greenhouse-grown lettuce by arbuscular mycorrhizal fungi is conditioned by the source of phosphorus nutrition. , 2011, Journal of agricultural and food chemistry.

[55]  L. Marchetti,et al.  Emission and Function of Volatile Organic Compounds in Response to Abiotic Stress , 2011 .

[56]  J. Pickett,et al.  Perception of plant volatile blends by herbivorous insects--finding the right mix. , 2011, Phytochemistry.

[57]  D. Ulrich,et al.  UV-B-induced changes of volatile metabolites and phenolic compounds in blueberries (Vaccinium corymbosum L.) , 2011 .

[58]  I. Garmendia,et al.  Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse-grown lettuce. , 2011, Journal of agricultural and food chemistry.

[59]  D. Tuinen,et al.  Arbuscular mycorrhizal fungi associated with Artemisia umbelliformis Lam, an endangered aromatic species in Southern French Alps, influence plant P and essential oil contents , 2011, Mycorrhiza.

[60]  I. Baldwin,et al.  The evolutionary context for herbivore-induced plant volatiles: beyond the 'cry for help'. , 2010, Trends in plant science.

[61]  C. Müller,et al.  UV-B impact on aphid performance mediated by plant quality and plant changes induced by aphids. , 2009, Plant biology.

[62]  A. Bennett,et al.  Mycorrhizal Fungal-Plant-Insect Interactions: The Importance of a Community Approach * , 2009, Environmental entomology.

[63]  L. Arnaud,et al.  Aphid and Plant Volatiles Induce Oviposition in an Aphidophagous Hoverfly , 2008, Journal of Chemical Ecology.

[64]  S. Heuskin,et al.  Electrophysiological and Behavioral Responses of the Multicolored Asian Lady Beetle, Harmonia axyridis Pallas, to Sesquiterpene Semiochemicals , 2007, Journal of Chemical Ecology.

[65]  P. Winge,et al.  Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae , 2007 .

[66]  R. Kapoor,et al.  Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. , 2007, Mycorrhiza.

[67]  R. Adams,et al.  Identification of Essential Oil Components By Gas Chromatography/Mass Spectrometry , 2007 .

[68]  A. Copetta,et al.  Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese , 2006, Mycorrhiza.

[69]  J. Sullivan,et al.  Ultraviolet-B effects on stomatal density, water-use efficiency, and stable carbon isotope discrimination in four glasshouse-grown soybean (Glyicine max) cultivars , 2005 .

[70]  Christine Woodcock,et al.  Insect host location: a volatile situation. , 2005, Trends in plant science.

[71]  E. Haubruge,et al.  Is the (E)‐β‐farnesene only volatile terpenoid in aphids? , 2005 .

[72]  J. Rozema,et al.  Increased solar UV-B radiation may reduce infection by arbuscular mycorrhizal fungi (AMF) in dune grassland plants: evidence from five years of field exposure , 2001, Plant Ecology.

[73]  J. Klironomos.  UV-Bmediated changes on below-ground communities associated with the roots of Acer saccharum. , 1995 .

[74]  B. S. Vergara,et al.  Effects of UVB Radiation on Stomatal Density and Opening in Rice (Oryza sativa L.) , 1995 .

[75]  Manuela Giovannetti,et al.  AN EVALUATION OF TECHNIQUES FOR MEASURING VESICULAR ARBUSCULAR MYCORRHIZAL INFECTION IN ROOTS , 1980 .

[76]  J. T. Puthur,et al.  Halo- and UV-B priming-mediated drought tolerance and recovery in rice seedlings , 2021 .

[77]  R. Mittler.  ROS Are Good. , 2017, Trends in plant science.

[78]  C. Müller,et al.  Impacts of Ultraviolet Radiation on Interactions Between Plants and Herbivorous Insects: A Chemo-Ecological Perspective , 2010 .

[79]  J. Peñuelas,et al.  Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. , 2008, Plant biology.

[80]  A. Gange.  Ecological Communities: Insect–mycorrhizal interactions: patterns, processes, and consequences , 2007 .

[81]  Øyvind Hammer,et al.  PAST - PAlaeontological STatistics, ver. 1.34 , 2005 .

[82]  H. Matsumoto,et al.  Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. , 2001, Plant physiology.

[83]  N. Davies.  Gas chromatographic retention indices of monoterpenes and sesquiterpenes on methyl silicon and Carbowax 20M phases , 1990 .

[84]  Y. Masada.  Analysis of essential oils by gas chromatography and mass spectrometry , 1976 .

[85]  Fred W. McLafferty,et al.  Registry of mass spectral data , 1974 .