European Oak Powdery Mildew: Impact on Trees, Effects of Environmental Factors, and Potential Effects of Climate Change Benoit Marçais, Marie-Laure Desprez-Loustau
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European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change Benoit Marçais, Marie-Laure Desprez-Loustau To cite this version: Benoit Marçais, Marie-Laure Desprez-Loustau. European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change. Annals of Forest Science, Springer Nature (since 2011)/EDP Science (until 2010), 2014, 71 (6), pp.633-642. 10.1007/s13595- 012-0252-x. hal-01102701 HAL Id: hal-01102701 https://hal.archives-ouvertes.fr/hal-01102701 Submitted on 13 Jan 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Annals of Forest Science (2014) 71:633–642 DOI 10.1007/s13595-012-0252-x REVIEW PAPER European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change Benoit Marçais & Marie-Laure Desprez-Loustau Received: 19 April 2012 /Accepted: 6 November 2012 /Published online: 18 December 2012 # The Author(s) 2012. This article is published with open access at SpringerLink.com Abstract mature trees. Climate change might influence the disease sever- • Context Powdery mildew is one of the most common ity mainly by altering the host pathogen phenological synchro- diseases of oaks in Europe. After alarming reports in the ny. Process-based models are required for reliable predictions. beginning of the twentieth century following the presumed introduction of the invasive fungus, the disease has become Keyword Erysiphe alphitoides; Quercus . Phenological familiar to foresters. However, its impact may vary greatly synchrony . Oak decline . Natural regeneration according to intrinsic and extrinsic factors. • Aims We aimed at providing updated and synthesised information on the impact of powdery mildew on oak and 1 Introduction on the effects of environment on disease. • Methods A comprehensive literature review was per- Powdery mildew is one of the most common diseases of oaks formed, including old reports of the early epidemics to more in Europe. For example, it represented 13 % of all biotic and recent data. abiotic health problems reported on deciduous oak species in • Results Tree growth patterns are of critical importance to France from 1989 to 2006 (database of the Département de la explain the severity of the disease and the differences be- Santé des Forêts (DSF)). However, the disease was not tween juvenile and mature trees. A critical element, espe- reported in Europe before 1907 when sudden severe outbreaks cially for infection of mature trees, is the availability of were observed; the causal pathogen was then reported as spores during the production of the first leaf flush. High invasive. It identity and origin was the subject of considerable disease impact is often related to modified growth patterns, debate in the years following the emergence of oak powdery either by environmental factors (insects or frost) or silvicul- mildew (reviewed in Mougou et al. 2008 and Desprez- tural practices (e.g., coppicing). Loustau et al. 2011). The use of molecular tools has recently • Conclusion Powdery mildew can have important impacts in allowed more precise characterization of the causal agent. natural oak regenerations and a significant role in decline of Mougou et al. (2008) showed that the same symptoms can be associated with four different powdery mildew lineages Handling Editor: Nathalie Breda (probably cryptic species) currently co-existing in Europe. In a Contribution of the co-authors Both authors contributed in writing a large survey in France, Erysiphe alphitoides, the species part of the manuscript which was described in 1911, was the most common species B. Marçais (*) (Mougou-Hamdane et al. 2010). However, another species, INRA, Université de Lorraine, UMR1136 Interactions Erysiphe quercicola first described on oak in Japan by Arbres/Microorganismes, F 54280 Champenoux, France Takamatsu et al. (2007), was detected in about 20 % of oak e-mail: [email protected] powdery mildew samples. Two other species, Erysiphe M.-L. Desprez-Loustau hypophylla and Phyllactinia roboris were far less fre- UMR1202 BIOGECO, INRA, F 33610 Cestas, France quent, representing only few percent of the samples (Mougou-Hamdane et al. 2010). M.-L. Desprez-Loustau UMR1202 BIOGECO, Univesrité de Bordeaux, Oak powdery mildews infect young developing leaves in F 33400 Talence, France spring and summer. Indeed susceptibility of the leaf tissues 634 B. Marçais, M.-L. Desprez-Loustau strongly decreases as the leaf gets older (Edwards and Ayres E. alphitoides induces necrosis and/or deformation of the 1982). Conidia are abundantly produced on infected leaves leaf and can induce a reduced functional leaf area (Marçais and are important for the infection of second and third leaf and Bréda 2006; Hajji et al. 2009). An extreme impact of flush and the pathogen dispersal. In autumn, chasmothecia, powdery mildew is leaf shedding. Indeed, severe powdery the sexual structures, develop on the senescing leaves and mildew infection, above 50 % of the leaf surface, was are shed. Overwintering usually occurs in bark cracks and shown to greatly reduce the infected leaf lifespan compared ascospores are produced in late spring (Marçais et al. 2009). to healthy leaves (Hajji et al. 2009). The median time before Another overwintering mode is as mycelium in infected shedding was estimated to be 10–31 days for oak leaves buds (Kerling, 1966; Yarwood, 1957). These infected buds showing deformation or necrosis. As a consequence of severe develop in spring giving rise to so-called flags shoots, infection, complete defoliation of the second and third growth shoots that are severely infected by the pathogen with strong unit formed in June and August has been reported in young production of conidia. In a large survey in France, only E. oak seedlings (Jarvis 1964; Soutrenon 2003). This premature quercicola was detected from flag shoot (Feau et al. 2011). shedding could be a consequence of the altered water relations The initial impact of the disease at the beginning of the of infected leaves because their ability to reduce their temper- twentieth century was described as very severe, especially ature through stomatal conductance regulation is impeded on coppices (Langhoffer 1929; Woodward et al. 1929; Foex (Hewitt and Ayres 1975; Hajji et al. 2009). 1941). Powdery mildew was reported to have different A more common consequence of powdery mildew infec- impact depending on the oak species. The most severely tion is reduced carbon acquisition. As biotroph parasites, affected species was the so-called Pyrenean oak, Quercus powdery mildew fungi acquire their nutrients from living pyrenaica (0Quercus toza), for which high mortality rates host cells thanks to specialised feeding structures called were observed in southwest and western France (Bureau haustoria (Divon and Fluhr 2007). Infection by powdery 1908; Aubert 1919; Desprez-Loustau et al. 2011). Quercus mildew thus results in the derivation of plant metabolism robur was then reported as more susceptible than Quercus for fungal benefit. The impact of E. alphitoides on the leaf petraea while Mediterranean evergreen oaks, Quercus cer- carbohydrate metabolism has been studied in detail. The ris and red oaks such as Quercus rubra and Quercus pal- pathogen was shown to reduce carbon assimilation (An) ustris were considered resistant (Woodward et al. 1929; and translocation of carbohydrates from the infected leaves Foex 1941). After a few years, the disease was considered to the rest of the plant (Hewitt and Ayres 1975, 1976; less dramatic (Aubert 1919;Raymond1927)andtheauthors Percival and Fraser 2002; Hajji et al. 2009). The reduction wondered whether this could have been linked to a real de- of An is linked to an impact of the infection on both maximal crease in the disease severity, because of less favourable cli- light driven electron flux (Jmax) and on apparent maximal mate or the action of mycoparasites or to a better appraisal of velocity of RuBP carboxylation (Vcmax; Hajji et al. 2009). the disease long-term impact (Aubert 1919;Foex1941). The In the latter study, the decrease of An in infected leaves was disease is now well established but in spite of its frequent not compensated by an increased An in the healthy leaves of occurrence, its impact has often been considered as minor, the same seedling, leading to an overall reduction in carbon except in a few situations (Delatour 1983;Thomasetal.2002). assimilation. However, the impact on leaf functioning was In this review, we will first examine the impact of pow- less than what could be expected from the observed fraction dery mildew on oaks, from the leaf to the plant level, of leaf area infected: leaves with 100 % leaf area affected by distinguishing the young seedlings and the mature trees. E. alphitoides still displayed levels of An of about 50 % of As most available information refers to Q. robur and Q. the value observed in healthy leaves (Hewitt and Ayres petraea, we will mainly focus on impact of powdery mildew 1975; Brüggemann and Schnitzler 2001; Hajji et al. 2009). on these two species. Then, we will analyse the effect of This is in contrast to what is generally observed for foliar environment. In conclusion, we will discuss the possible pathogens where the impact on leaf physiology is greater impact of climate change. than what would be expected from the fraction of the leaf affected (Bastiaans 1991). In particular, powdery mildews of wheat, pepper, peach, or grape have a greater impact on net 2 Impacts of powdery mildew on oak trees photosynthesis than expected from the fraction of apparent- ly affected area (Shtienberg 1992).