Induced Volatile Emissions, Photosynthetic Characteristics, and Pigment Content in Juglans regia Leaves Infected with the Erineum-Forming Mite Aceria erinea

Persian walnut (Juglans regia L., Juglandaceae), one of the essential nut crops, is affected by different diseases, including mite attacks which result in gall and erineum formation. As the proportion of leaf area covered by mite galls or erineum is typically relatively low, the impact on tree photosynthetic productivity is often considered minor, and no pest control management is usually suggested. However, the effect of erineum-forming mites on walnut photosynthesis might be disproportionately larger than can be predicted from the leaf area impacted. In the present study, we studied how the foliage photosynthetic characteristics, pigment contents, and stress-induced volatile organic compounds scaled with the severity of infection varied from 0% (control trees) to 9.9%, by erineum-forming mite Aceria erinea in J. regia. Both leaf net assimilation rate (up to 75% reduction) and stomatal conductance (up to 82%) decreased disproportionately, increasing infection severity. Leaf total chlorophyll and β-carotene contents also decreased with infection severity, although the reduction was less than for photosynthetic characteristics (28% for chlorophyll and 25% for β-carotene). The infection induced significant emissions of green leaves volatiles ((Z)-3-hexenol, (E)-2-hexenal, (Z)-3-hexenyl acetate and 1-hexanol), monoterpenes and the homoterpene 3-(E)-4,8-dimethyl-1,3,7-nonatriene, and these emissions scaled positively with the percentage of leaf area infected. These results collectively indicate that erineum-forming mite infection of walnut leaves results in profound modifications in foliage physiological characteristics that can significantly impact tree photosynthetic productivity.

[1]  J. Grace,et al.  Temporal Changes in Ozone Concentrations and Their Impact on Vegetation , 2021, Atmosphere.

[2]  Ü. Niinemets,et al.  Gall- and erineum-forming Eriophyes mites alter photosynthesis and volatile emissions in infection severity-dependent manner in broad-leaved trees Alnus glutinosa and Tilia cordata. , 2020, Tree physiology.

[3]  J. Hui,et al.  Terpenes and Terpenoids in Plants: Interactions with Environment and Insects , 2020, International journal of molecular sciences.

[4]  Shuqing Kong,et al.  Comparison of the volatiles composition between healthy and buprestid infected Juglans regia (Juglandaceae) , 2020 .

[5]  E. de Lillo,et al.  Morphological and molecular characterization of the Colomerus vitis erineum strain (Trombidiformes: Eriophyidae) from grapevine erinea and buds , 2020, Experimental and Applied Acarology.

[6]  C. Faiola,et al.  Impact of insect herbivory on plant stress volatile emissions from trees: A synthesis of quantitative measurements and recommendations for future research , 2020, Atmospheric Environment: X.

[7]  M. Khanjani,et al.  Resistance of some commercial walnut cultivars and genotypes to Aceria tristriata (Nalepa) (Acari: Eriophyidae) and its correlation with some plant features. , 2020, Pest management science.

[8]  S. Welter Arthropod Impact on Plant Gas Exchange , 2019, Insect-Plant Interactions.

[9]  S. Raranciuc,et al.  Altitude affects the distribution and abundance of two non‐native insect pests of the common walnut , 2019, Journal of Applied Entomology.

[10]  R. Álvarez,et al.  Antioxidant metabolism in galls due to the extended phenotypes of the associated organisms , 2018, PloS one.

[11]  Ü. Niinemets,et al.  Petiole gall aphid (Pemphigus spyrothecae) infestation of Populus × petrovskiana leaves alters foliage photosynthetic characteristics and leads to enhanced emissions of both constitutive and stress-induced volatiles , 2018, Trees.

[12]  M. Khanjani,et al.  Impact of the erineum strain of Colomerus vitis (Acari: Eriophyidae) on the development of plants of grapevine cultivars of Iran , 2018, Experimental and Applied Acarology.

[13]  A. Khan,et al.  Pests of Walnut , 2018 .

[14]  Ü. Niinemets,et al.  Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics. , 2018, Plant, cell & environment.

[15]  E. Dirlewanger,et al.  Walnut: past and future of genetic improvement , 2018, Tree Genetics & Genomes.

[16]  D. Sarker,et al.  Assessment of Chlorophyll Loss due to Infestation of Gall Mite in Bay Leaf , 2017 .

[17]  Jun-Hyung Tak,et al.  Acaricidal and repellent activity of plant essential oil-derived terpenes and the effect of binary mixtures against Tetranychus urticae Koch (Acari: Tetranychidae) , 2017 .

[18]  Daniel D. Timis,et al.  Diclofenac Influence on Photosynthetic Parameters and Volatile Organic Compounds Emision from Phaseolus vulgaris L.Plants , 2017 .

[19]  Ü. Niinemets,et al.  Ozone-induced foliar damage and release of stress volatiles is highly dependent on stomatal openness and priming by low-level ozone exposure in Phaseolus vulgaris. , 2017, Plant, cell & environment.

[20]  R. Isaias,et al.  Sink Status and Photosynthetic Rate of the Leaflet Galls Induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae) , 2017, Front. Plant Sci..

[21]  D. Tomescu,et al.  Disproportionate photosynthetic decline and inverse relationship between constitutive and induced volatile emissions upon feeding of Quercus robur leaves by large larvae of gypsy moth (Lymantria dispar). , 2017, Environmental and experimental botany.

[22]  Sandeep Chakraborty,et al.  The walnut (Juglans regia) genome sequence reveals diversity in genes coding for the biosynthesis of non-structural polyphenols. , 2016, The Plant journal : for cell and molecular biology.

[23]  C. M. Enescu,et al.  Juglans regia in Europe: distribution, habitat, usage and threats , 2016 .

[24]  Ü. Niinemets,et al.  Controls of the quantum yield and saturation light of isoprene emission in different-aged aspen leaves. , 2015, Plant, cell & environment.

[25]  C. Chireceanu,et al.  Contribution to knowledge of the gall insects and mites associated with plants in southern Romania. , 2015 .

[26]  Ü. Niinemets,et al.  Oak powdery mildew (Erysiphe alphitoides)-induced volatile emissions scale with the degree of infection in Quercus robur. , 2014, Tree physiology.

[27]  N. Chakraborty,et al.  Foliar Gall and Antioxidant Enzyme Responses in Alstonia scholaris, R. Br. after Psylloid Herbivory– An Experimental and Statistical Analysis  , 2014, Global Journal Of Botanical Science.

[28]  H. Chou,et al.  The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves , 2014 .

[29]  Ü. Niinemets,et al.  Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses. , 2014, Environmental and experimental botany.

[30]  Ü. Niinemets,et al.  Gas chromatography-mass spectrometry method for determination of biogenic volatile organic compounds emitted by plants. , 2014, Methods in molecular biology.

[31]  R. Gulati Eco-Friendly Management of Phytophagous Mites , 2014 .

[32]  M. Brändle,et al.  Changes in Clonal Poplar Leaf Chemistry Caused by Stem Galls Alter Herbivory and Leaf Litter Decomposition , 2013, PloS one.

[33]  James D. Blande,et al.  Where do herbivore-induced plant volatiles go? , 2013, Front. Plant Sci..

[34]  R. Padalia,et al.  Phytochemical analysis of the leaf volatile oil of walnut tree (Juglans regia L.) from western Himalaya , 2013 .

[35]  L. Copolovici,et al.  Influence of nine antibiotics on key secondary metabolites and physiological characteristics in Triticum aestivum: leaf volatiles as a promising new tool to assess toxicity. , 2013, Ecotoxicology and environmental safety.

[36]  J. P. Lemos-Filho,et al.  Source-sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae) , 2012 .

[37]  M. Rather,et al.  Chemical composition, antioxidant and antibacterial activities of the leaf essential oil of Juglans regia L. and its constituents. , 2012, Phytomedicine : international journal of phytotherapy and phytopharmacology.

[38]  M. Cramer,et al.  Benefits of photosynthesis for insects in galls , 2012, Oecologia.

[39]  J. Mano,et al.  Differential Metabolisms of Green Leaf Volatiles in Injured and Intact Parts of a Wounded Leaf Meet Distinct Ecophysiological Requirements , 2012, PloS one.

[40]  K. Karczmarz DYNAMICS OF POPULATION AND BIONOMICS OF Panaphis juglandis (Goeze, 1778) (Homoptera, Phyllaphididae) ON COMMON WALNUT (Juglans regia L.) IN LUBLIN'S PARKS AND GARDENS , 2012 .

[41]  A. Arneth,et al.  Estimations of isoprenoid emission capacity from enclosure studies: measurements, data processing, quality and standardized measurement protocols , 2011 .

[42]  Sean C. Thomas,et al.  A gall-inducing arthropod drives declines in canopy tree photosynthesis , 2011, Oecologia.

[43]  A. Karioti,et al.  Erinea formation on Quercus ilex leaves: anatomical, physiological and chemical responses of leaf trichomes against mite attack. , 2011, Phytochemistry.

[44]  Ü. Niinemets,et al.  High within‐canopy variation in isoprene emission potentials in temperate trees: Implications for predicting canopy‐scale isoprene fluxes , 2010 .

[45]  P. Thonart,et al.  The lipoxygenase metabolic pathway in plants: potential for industrial production of natural green leaf volatiles , 2010 .

[46]  Katrin Heinsoo,et al.  Leaf rust induced volatile organic compounds signalling in willow during the infection , 2010, Planta.

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

[48]  Ü. Niinemets,et al.  Volatile Emissions from Alnus glutionosa Induced by Herbivory are Quantitatively Related to the Extent of Damage , 2010, Journal of Chemical Ecology.

[49]  F. Dosba Breeding plantation tree crops. Temperate species , 2009 .

[50]  Ivo Feussner,et al.  Lipoxygenases - Structure and reaction mechanism. , 2009, Phytochemistry.

[51]  J. V. van Loon,et al.  Chemical complexity of volatiles from plants induced by multiple attack. , 2009, Nature chemical biology.

[52]  G. McGranahan,et al.  Breeding Walnuts (Juglans Regia) , 2009 .

[53]  G. Hemery,et al.  Early growth and form of common walnut (Juglans regia L.) in mixture with tree and shrub nurse species in southern England , 2008 .

[54]  M. Dicke,et al.  Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. , 2008, Plant, cell & environment.

[55]  M. Berenbaum,et al.  Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings , 2006, Oecologia.

[56]  J. D. Shorthouse,et al.  Gall-inducing insects – Nature's most sophisticated herbivores , 2005 .

[57]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[58]  E. M. Varanda,et al.  Morphological and histochemical study of leaf galls of Tabebuia ochracea (Cham.) Standl (Bignoniaceae) , 2003 .

[59]  S. Kreiter,et al.  The eriophyoid mites (Acarina) from walnut trees in Grenoble (Isere, France) , 2002 .

[60]  K. Larson The impact of two gall-forming arthropods on the photosynthetic rates of their hosts , 1998, Oecologia.

[61]  A. Cecílio,et al.  THE CONTROL OF WALNUT APHID, CHROMAPHIS JUGLANDICOLA (HOMOPTERA: APHIDOIDEA) IN WALNUT ORCHARDS IN PORTUGAL. , 1997 .

[62]  T. Whitham,et al.  Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling , 1997, Oecologia.

[63]  A. Knapp,et al.  Plant Tolerance of Gall-Insect Attack and Gall-Insect Performance , 1996 .

[64]  J. Amrine 4.1.2 Phyllocoptes fructiphilus and biological control of multiflora rose , 1996 .

[65]  R. Mizell,et al.  Physiological Effects of Galls Induced by Phylloxera notabilis (Homoptera: Phylloxeridae) on Pecan Foliage , 1987 .

[66]  E L Smith,et al.  Photosynthesis in Relation to Light and Carbon Dioxide. , 1936, Proceedings of the National Academy of Sciences of the United States of America.