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Drought Stress Can Induce the Pathogenicity of Cryptostroma Corticale, the Causal Agent of Sooty Bark Disease of Sycamore Maple

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Drought Stress Can Induce the Pathogenicity of Cryptostroma Corticale, the Causal Agent of Sooty Bark Disease of Sycamore Maple Article Drought Stress Can Induce the Pathogenicity of Cryptostroma corticale, the Causal Agent of Sooty Bark Disease of Sycamore Maple Nikica Ogris * , Ana Brglez and Barbara Piškur Slovenian Forestry Institute, Veˇcnapot 2, SI-1000 Ljubljana, Slovenia; [email protected] (A.B.); [email protected] (B.P.) * Correspondence: [email protected] Abstract: Reports of sooty bark disease of maples caused by the fungus Cryptostroma corticale have recently been emerging from across Europe. The aims of our study were to describe the first report of sooty bark disease in Slovenia, to determine the pathogenicity of C. corticale, to confirm the optimum temperature for the growth of the fungus, and to determine the mass loss of Acer pseudoplatanus wood inoculated by C. corticale. We confirmed the presence of C. corticale on A. pseudoplatanus via morphological and molecular analysis. The optimal growth of C. corticale was measured in vitro on potato dextrose agar and was determined to occur at 25 ◦C. Pathogenicity tests were performed on 30 saplings of A. pseudoplatanus under two treatments, humid and drought stress, and the fungus was pathogenic in both treatments. The mean length of bark lesions and wood discoloration of the drought-stressed saplings was significantly greater than that in the humid treatment. Re-isolations of C. corticale were successful from all inoculated saplings, and thus Koch’s postulates were confirmed. The mass loss of A. pseudoplatanus wood was determined by mini-block test in a period of 10 weeks Citation: Ogris, N.; Brglez, A.; and was observed as minimal. Based on the results, we conclude that C. corticale is a weak and Piškur, B. Drought Stress Can Induce opportunistic pathogen that most likely expresses itself intensively under hot and dry conditions. the Pathogenicity of Cryptostroma corticale, the Causal Agent of Sooty Keywords: pathogenicity; drought stress; optimal growth; climate change; mass loss; mini-block test; Bark Disease of Sycamore Maple. wood rot; opportunistic pathogen; saprophyte; endophyte Forests 2021, 12, 377. https:// doi.org/10.3390/f12030377 Academic Editor: Angus Carnegie 1. Introduction Sooty bark disease of maples is caused by the fungus Cryptostroma corticale (Ellis & Received: 16 February 2021 Everh.) P.H. Greg. & S. Waller [1]. It is distributed in North America [2] and in most Accepted: 18 March 2021 countries of Western and Central Europe, i.e., Great Britain [3], France [4], the Nether- Published: 21 March 2021 lands [5], Belgium [6], Germany [7,8], the Czech Republic [9,10], Austria [11,12], Italy [13], Switzerland [14], and Bulgaria [15]. Most of the countries surrounding Slovenia have Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in already reported the disease, but it has not been reported in Slovenia until now. published maps and institutional affil- The hosts of C. corticale are maples (Acer spp.). It most frequently infects sycamore iations. maple (A. pseudoplatanus L.), field maple (A. campestre L.), Norway maple (A. platanoides L.) and box elder (A. negundo L.) [16]. Maples are one of the most important hardwood tree species in Slovenia, and therefore the presence and spread of sooty bark disease would raise serious concerns. Wounds serve as entry points for the fungus, which quickly invades the wood and Copyright: © 2021 by the authors. later also the phloem [9,16,17]. Cryptostroma corticale is recognized as an endophyte, latent Licensee MDPI, Basel, Switzerland. This article is an open access article invader, saprophyte, and weak pathogen that favors hot and dry periods [9,10,13,15,17,18]. distributed under the terms and Because of its preference for hot and dry weather, some studies predict more frequent conditions of the Creative Commons outbreaks of sooty bark disease in the future due to climate change [9,10,19]. Attribution (CC BY) license (https:// The first suspicious case of sooty bark disease was observed in October 2019 on a creativecommons.org/licenses/by/ chunk of Acer pseudoplatanus that was collected in February 2019 in the central part of ◦ ◦ 4.0/). Slovenia (46.13369 N, 14.77848 E) and displayed in the hallway of the Slovenian Forestry Forests 2021, 12, 377. https://doi.org/10.3390/f12030377 https://www.mdpi.com/journal/forests Forests 2021, 12, x FOR PEER REVIEW 2 of 13 The first suspicious case of sooty bark disease was observed in October 2019 on a Forests 2021, 12, 377 2 of 12 chunk of Acer pseudoplatanus that was collected in February 2019 in the central part of Slovenia (46.13369° N, 14.77848° E) and displayed in the hallway of the Slovenian Forestry Institute for educational purposes because it had typical symptoms of Eutypella canker of mapleInstitute caused for educational by Eutypella purposes parasitica because R.W. itDavidson had typical & symptomsR.C. Lorenz. of EutypellaSurprisingly, canker after of sevenmaple months caused byunderEutypella room parasiticatemperatureR.W. and Davidson natural & daylight, R.C. Lorenz. the sample Surprisingly, developed afterseven typi- calmonths symptoms under of room sooty temperature bark disease and caused natural by daylight, C. corticale the (Figure sample 1): developed the barktypical cracked symp- and peeledtoms of off, sooty revealing bark disease dark brown caused masses by C. corticale of ovoid(Figure conidia1): the which bark measured cracked and 4.9–6.1 peeled × 3.1– off, 4.0revealing µm. dark brown masses of ovoid conidia which measured 4.9–6.1 × 3.1–4.0 µm. Figure 1. The firstfirst suspicious case of sooty bark disease of sycamore maple (Acer pseudoplatanus) caused by Cryptostroma corticale inin Slovenia:Slovenia: ( a(a)) The The bark bark cracked cracked and and peeled peeled off, off, revealing revealing dark dark brown brown masses masses of conidia; of conidia; (b) masses (b) masses of dark of brown dark brown conidia; (c) ovoid, dark brown conidia. conidia; (c) ovoid, dark brown conidia. TheThe aims aims of of the the study study were were (1) (1) to to investigat investigatee the the first first report report of ofsooty sooty bark bark disease disease of sycamoreof sycamore maple maple in Slovenia, in Slovenia, (2) (2)to determine to determine the theoptimum optimum temperature temperature for growth for growth of the of fungusthe fungus in pure in pure culture, culture, (3) to (3) test to its test pathogenicity its pathogenicity under under two watering two watering treatments treatments simu- latingsimulating humid humid and anddrought drought conditions, conditions, and and (4) (4)to todetermine determine the the mass mass loss loss of of sycamore sycamore wood samples exposed to C. corticale . TheThe first first report report of sooty bark disease of of sycamore maple maple in in Slovenia Slovenia was was accompa- accompa- niednied by pathogenicity trials. Pathogenicity Pathogenicity tests tests and and mass mass loss loss of of sycamore wood were performed underunder optimaloptimal temperature temperature for for growth growth of C.of corticaleC. corticale. Therefore,. Therefore, the optimalthe optimal tem- temperatureperature was was obtained obtained prior prior to performing to performing those those experiments. experiments. Furthermore, Furthermore, the collected the col- lectedsamples samples for first for report first showedreport showed wood decay; wood therefore, decay; therefore, the additional the additional aim was addedaim was to addedinvestigate to investigate the mass the loss mass of sycamore loss of sycamore wood. wood. 2.2. Materials Materials and and Methods Methods 2.1.2.1. Identification Identification A. pseudoplatanus ThreeThree 1-m-long andand 12–15-cm-thick12–15-cm-thick chunks chunks of of A. pseudoplatanuswere were collected collected in Novem- in No- ber 2019 in the central part of Slovenia, in a managed, mixed forest stand (46.13369◦ N, vember 2019 in the central part of Slovenia, in a managed, mixed forest stand (46.13369° N, 14.77848◦ E) from which the first suspected case also originated. One chunk was cut from a 14.77848° E) from which the first suspected case also originated. One chunk was cut from visually healthy tree, and the other two from trees that had old, but healed, wounds. No a visually healthy tree, and the other two from trees that had old, but healed, wounds. No visible symptoms of the disease were observed at the location. The end parts of the chunks visible symptoms of the disease were observed at the location. The end parts of the chunks were sealed with wax to slow down desiccation and were incubated at room temperature were sealed with wax to slow down desiccation and were incubated at room temperature under natural daylight. under natural daylight. After the symptoms were expressed, the samples were morphologically examined, After the symptoms were expressed, the samples were morphologically examined, and the identity of the causal agent was determined. Morphological analysis was done with and the identity of the causal agent was determined. Morphological analysis was done an Olympus SZX16 stereomicroscope and an Olympus BX53 microscope, both equipped with an Olympus SZX16 stereomicroscope and an Olympus BX53 microscope, both with an Olympus UC90 digital camera and Olympus CellSens Standard 1.18 software. equippedThe conidiawith an ofOlympusC. corticale UC90were digital aseptically camera transferredand Olympus on CellSens the tip of Standard a needLe 1.18 to software.growing medium containing 3.9% (w/v) potato dextrose agar (PDA; Becton Dickinson, Sparks,The MD, conidia USA) of and C. corticale incubated were in aaseptically KambiˇcI-190 transferred CK chamber on the (Kambiˇc,Semiˇc,Slovenia) tip of a needle to grow- ingat 23.9 medium± 0.3 containing◦C. During 3.9% this (w/v process,) potato a representativedextrose agar (PDA; pure cultureBecton Dickinson, of C. corticale Sparks,was obtained, and the isolate was deposited at the culture collection of the Laboratory of Forest Protection at the Slovenian Forestry Institute (ZLVG 859). This isolate was used Forests 2021, 12, 377 3 of 12 in all further experiments.
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