Induced Volatile Emissions, Photosynthetic Characteristics, and Pigment Content in Juglans Regia Leaves Infected with the Erineum-Forming Mite Aceria Erinea
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Article Induced Volatile Emissions, Photosynthetic Characteristics, and Pigment Content in Juglans regia Leaves Infected with the Erineum-Forming Mite Aceria erinea Corina Popitanu 1,†, Andreea Lupitu 2,† , Lucian Copolovici 2,* , Simona Bungău 1 , Ülo Niinemets 3,4 and Dana Maria Copolovici 2 1 Biomedical Sciences Doctoral School, University of Oradea, University St. no. 1, 410087 Oradea, Romania; [email protected] (C.P.); [email protected] (S.B.) 2 Institute for Research, Development and Innovation in Technical and Natural Sciences, Faculty of Food Engineering, Tourism and Environmental Protection, Aurel Vlaicu University of Arad, Elena Drăgoi St., no. 2, 310330 Arad, Romania; [email protected] (A.L.); [email protected] (D.M.C.) 3 Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, 51006 Tartu, Estonia; [email protected] 4 Estonian Academy of Sciences, Kohtu 6, 10130 Tallinn, Estonia * Correspondence: [email protected] † These authors contributed equally to this work. Abstract: 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 Citation: Popitanu, C.; Lupitu, A.; usually suggested. However, the effect of erineum-forming mites on walnut photosynthesis might be Copolovici, L.; Bung˘au,S.; Niinemets, disproportionately larger than can be predicted from the leaf area impacted. In the present study, we Ü.; Copolovici, D.M. Induced Volatile studied how the foliage photosynthetic characteristics, pigment contents, and stress-induced volatile Emissions, Photosynthetic organic compounds scaled with the severity of infection varied from 0% (control trees) to 9.9%, by Characteristics, and Pigment Content in Juglans regia Leaves Infected with erineum-forming mite Aceria erinea in J. regia. Both leaf net assimilation rate (up to 75% reduction) the Erineum-Forming Mite Aceria and stomatal conductance (up to 82%) decreased disproportionately, increasing infection severity. erinea. Forests 2021, 12, 920. Leaf total chlorophyll and β-carotene contents also decreased with infection severity, although https://doi.org/10.3390/f12070920 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, Academic Editor: Luís González (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 Received: 8 June 2021 infected. These results collectively indicate that erineum-forming mite infection of walnut leaves Accepted: 13 July 2021 results in profound modifications in foliage physiological characteristics that can significantly impact Published: 15 July 2021 tree photosynthetic productivity. Publisher’s Note: MDPI stays neutral Keywords: green leaf volatiles; induced emissions; monoterpene emission; photosynthesis; quantita- with regard to jurisdictional claims in tive responses; volatile organic compounds published maps and institutional affil- iations. 1. Introduction Persian walnut (Juglans regia L., Juglandaceae) is a deciduous tree species native to Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. central Asia. It is one of the most important nut crops with a wide area of cultivation, This article is an open access article including Europe, North America, Central, and East Asia, North Africa, New Zealand [1]. distributed under the terms and In Europe, it is primarily grown in central to southern countries, although cultivars selected conditions of the Creative Commons for superior cold hardiness can survive in the south part of Northern Europe [2]. The most Attribution (CC BY) license (https:// extensive J. regia plantations are in Turkey, France, Romania, Serbia, and Hungary. As a tree creativecommons.org/licenses/by/ species with a sequenced genome, it becomes one of the model species for physiological 4.0/). studies in woody plants [3]. Forests 2021, 12, 920. https://doi.org/10.3390/f12070920 https://www.mdpi.com/journal/forests Forests 2021, 12, 920 2 of 12 Juglans regia is an early-successional very light-demanding species growing best in deep fertile soils [4]. As a widely planted species, J. regia is confronted by a broad range of pests, including fungi, bacteria, viruses, insect and mite herbivores, and parasites that could disturb roots, fruits, stems, or leaves [1,2,5]. The J. regia leaves can be attacked by a diversity of mites and insects, including leaf miners, chewing and piercing insect herbivores [6–8], and gall- and erineum-forming mites [9–11] that can lead to extensive defoliation and premature leaf senescence and reduction in leaf physiological activity, thereby potentially having significant economic impacts [5]. However, mite gall and erineum formation infrequent in J. regia plantations [9–11], the physiological effects of gall and erineum formation have not been characterized in this species. Gall and erineum formation result from an active growth reaction of cell plants in reaction to the insect or mite attacks, leading to the creation of tumor-like structures that provide shelter and food for the occupants [12,13]. The gall-inducing insects are found in the orders Hymenoptera, Thysanoptera, Diptera, gall- and erineum-forming mites in Trombidiformes (superfamily Eriophyoidea)[14]. Individual eriophyid species are highly specialized plant feeders affecting only a very narrow range of hosts. Besides high host specificity, a very high diversity of eriophyoid mites (more than 1000 species) can induce galls and erinea on plant species from a wide range of families [15,16]. As gall and erineum formation does not result in defoliation and the surface area covered by galls and erinea is generally a relatively small fraction of the total area, the impact of leaf galling on foliage physiological activity might be considered small. However, available evidence indicates that leaf infection by gall- and erineum-inducing parasites can result in disproportionately greater physiology and biochemistry alterations than predicted based on the percentage of the infected area [17]. In particular, infestation by gall-forming arthropods typically leads to strongly reduced leaf photosynthetic pigment content as observed in Populus nigra var. italica leaves by infestion with petiole gall aphid (Pemphi- gus spyrothecae)[18], and Alstonia scholaris leaves plagued by Pauropsylla tuberculata [19]. Typically, the gall or erineum-induced leaf physiological alterations include reductions in both light-saturated stomatal conductance and net assimilation rate as confirmed for gall-forming cynipid wasp infections in Quercus robur [17] and eriophyoid erineum-and gall-forming mite infections in Tilia cordata and Alnus glutinosa [20]. Similarly, both stomatal conductance and net assimilation rate were reduced in Carya illinoensis leaves infested by Phylloxera notabilis galls [21]. A lower photosystem II efficiency was found in Carya glabra infested with cecidomyiid midge galls [22]. Net assimilation rate, stomatal conductance, and photosystem II activity were reduced in the leaves of Machilus thunbergii galled by Daphnephila taiwanensis [23]. However, depending on the type of gall inducer, leaf CO2 and H2O exchange can be disturbed to a different extent, potentially leading to modifi- cations in leaf water use efficiency [17,20,24]. For example, in leaves of P. × petrovskiana infested with P. spyrothecae net assimilation rate per area decreased by almost five-fold likely due to restricted nitrogen and carbon availability for leaf lamina assembly. At the same time, increasing the infestation severity determinea the stomatal conductance in- crease [25]. Furthermore, net assimilation rate and stomatal conductance even increased in Silphium integrifolium leaves infested with the apical meristem galler Antistrophus silphii [26], suggesting profound modifications in sink–source relationships induced by the galler. Apart from photosynthetic modifications, to respond to herbivore feeding or fungal infection, plants emit various volatiles induced by stress, such as monoterpenes, sesquiter- penes, and green leaf volatiles (GLV) [27–31]. These compounds are implicated in at- mospherical chemical reactions with pollutants (as NOx) and determine tropospheric ozone concentration increasing [32]. Much fewer studies have looked at volatile emissions from plants infected with arthropod-formed galls or erinea. Leaves infected with gall- or erineum-forming arthropods typically have enhanced emissions of GLV [17,20], suggesting a sustained damage resulting from the feeding of arthropods. However, induced and constitutive emissions might be differently affected by different gall- or erineum-forming organisms. In [25], both constitutive isoprene and induced monoterpene emissions scaled Forests 2021, 12, 920 3 of 12 positively with the infestation severity by petiole gall aphids in leaves of P. × petrovskiana. In [17], in gall wasp-infected leaves of Quercus robur, constitutive isoprene emissions de- creased in all cases with increasing infection severity. In contrast, the emission of monoter- penes