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Drought events determine performance of Quercus ilex seedlings and increase their susceptibility to Phytophthora cinnamomi

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More frequent weather extremes are expected to occur in the Mediterranean region within the present context of climate change. These extremes could affect forests and plant diseases driven by pathogens. It is hypothesised that simulation of weather extremes during Quercus ilex growth will influence early performance and susceptibility to the invasive oomycete Phytophthora cinnamomi. In 2010, 140 Q. ilex seedlings were subjected to three watering regimes under greenhouse conditions: waterlogging (W), water stress (S) and optimal watering regime for growth (C). During the second vegetative period, conditions were altered to create the following scenarios: WW, WS, SS, SW and CC. After the second vegetative period, plants were artificially infested with P. cinnamomi. Holm oak (Q. ilex) was more sensitive to flooding in the first year of growth than in the second year. The altered scenarios produced plants with a lower fine-to-total root ratio than plants in unaltered scenarios. Plants with the highest growth rates maintained their relatively rapid growth and photosynthetic activity under altered scenarios. However, plants with the highest growth rates became the plants with the lowest growth rates when two consecutive years of drought occurred, indicating a trade-off by Q. ilex in growth investment, observed only if the water stress scenario persists. Seedlings were more sensitive to water shortage than to waterlogging, especially if they encountered a dry scenario during the first year. Exposure to drought events increased seedling mortality rates after P. cinnamomi infection. Waterlogging combined with subsequent water deprivation was the worst scenario when soil was infested with P. cinnamomi, causing 100% mortality of plants.
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... The main changes in plant status caused by P. cinnamomi infection have been related to physiological responses, such as stomatal closure, photosynthesis rate, and water imbalance [29][30][31]. As reported by , the response of Q. ilex seedlings to P. cinnamomi resembles the drought stress response, with differences between provenances; a general decrease in proteins related to photosynthesis and an increase in starch biosynthesis were observed. ...
... The effect of P. cinnamomi in combination with water deprivation on Q. ilex seedlings has also been studied at the phenotypic, physiological, biochemical, and molecular levels [30,33,34]. Previous studies demonstrated that drought increases susceptibility to P. cinnamomi in Q. ilex seedlings [9,30,33]. ...
... The effect of P. cinnamomi in combination with water deprivation on Q. ilex seedlings has also been studied at the phenotypic, physiological, biochemical, and molecular levels [30,33,34]. Previous studies demonstrated that drought increases susceptibility to P. cinnamomi in Q. ilex seedlings [9,30,33]. reported that the root mass fraction of Q. ilex seedlings was significantly reduced by P. cinnamomi infection, altering the growth pattern. However, the plants could not recover from the physiological effects of infection when the root rot coincided with water stress. ...
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Holm oak (Quercus ilex) is considered to be one of the major structural elements of Mediterranean forests and the agrosilvopastoral Spanish “dehesa”, making it an outstanding example of ecological and socioeconomic sustainability in forest ecosystems. The exotic Phytophthora cinnamomi is one of the most aggressive pathogens of woody species and, together with drought, is considered to be one of the main drivers of holm oak decline. The effect of and response to P. cinnamomi inoculation were studied in the offspring of mother trees from two Andalusian populations, Cordoba and Huelva. At the two locations, acorns collected from both symptomatic (damaged) and asymptomatic (apparently healthy) trees were sampled. Damage symptoms, mortality, and chlorophyll fluorescence were evaluated in seedlings inoculated under humid and drought conditions. The effect and response depended on the population and were more apparent in Huelva than in Cordoba. An integrated proteomic and metabolomic analysis revealed the involvement of different metabolic pathways in response to the pathogen in both populations, including amino acid metabolism pathways in Huelva, and terpenoid and flavonoid biosynthesis in Cordoba. However, no differential response was observed between seedlings inoculated under humid and drought conditions. A protective mechanism of the photosynthetic apparatus was activated in response to defective photosynthetic activity in inoculated plants, which seemed to be more efficient in the Cordoba population. In addition, enzymes and metabolites of the phenylpropanoid and flavonoid biosynthesis pathways may have conferred higher resistance in the Cordoba population. Some enzymes are proposed as markers of resilience, among which glyoxalase I, glutathione reductase, thioredoxin reductase, and cinnamyl alcohol dehydrogenase are candidates.
... Despite the dry summers of the Mediterranean ecosystem, relatively warm and humid winter and spring conditions are ideal for this pathogen (De Sampaio et al. 2013). Additionally, P. cinnamomi infection during the rainy season makes plants even more vulnerable to drought-induced mortality, because of their already compromised root and vascular systems (Corcobado et al. 2014;Burgess et al. 2017). ...
... Recent studies have identified Phytophthora spp. and drought as the main cause of oak death in southwest Spain, however, even more intense, an unprecedented holm oak mortality is expected in infected soils areas subjected to drought-flood alternation stress (Marcais et al. 2004;Moralejo et al. 2009;Corcobado et al. 2014;Gallardo et al. 2019). However, it is difficult to identify the precise cause of holm oak forest decline, as it is challenging to distinguish between the impacts of drought, increased temperature, and P. cinnamomi infestation. ...
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Quercus ilex may be considered the queen tree of the Mediterranean Basin, dominating coastal forest areas up to 2000 m above sea level at some sites. However, an increase in holm oak decline has been observed in the last decade. In this review, we analysed the current literature to answer the following questions: what are the traits that allow holm oak to thrive in the Mediterranean environment, and what are the main factors that are currently weakening this species? In this framework, we attempt to answer these questions by proposing a triangle as a graphical summary. The first vertex focuses on the main morpho-anatomical, biochemical and physiological traits that allow holm oak to dominate Mediterranean forests. The other two vertices consider abiotic and biotic stressors that are closely related to holm oak decline. Here, we discuss the current evidence of holm oak responses to abiotic and biotic stresses and propose a possible solution to its decline through adequate forest management choices, thus allowing the species to maintain its ecological domain.
... Vários estudos têm observado que a presença de árvores infetadas está mais associada a solos de textura fina (argilosos ou limosos) do que a solos de textura grosseira (arenosos) (Jung et al. 2000;Jönsson et al. 2005 (Zentmyer, 1980;Sánchez et al., 2002) e, por outro lado, a seca severa pode reduzir os mecanismos de defesa do hospedeiro por depleção nas reservas de carbono (McDowell et al., 2008). A alternância entre períodos de encharcamento e de seca severa é particularmente favorável à infeção, podendo reduzir as defesas do hospedeiro e aumentar a severidade da doença Sánchez et al., 2002;Corcobado et al., 2014a). ...
... than the sum of their individual effects (Figure 1b). For example, in a forest affected by increasing drought and exotic pathogens, drought might amplify the negative effects of pathogens due to a weakening effect on trees that make them more vulnerable to biotic attack (Corcobado et al., 2014;Desprez-Loustau et al., 2006). ...
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Understanding the interactive effects of global change drivers on tree demography is fundamental for realistic predictions of future forest dynamics. Multiple studies have shown increasing drought and exotic pathogens to severely threaten forest persistence by increasing mortality and decreasing growth of adult trees. However, much less is known about their effects on regeneration, and how they might affect seedling performance in additive and non‐additive (synergistic or antagonistic) ways. Here we aimed to fill this gap by experimentally exploring the effects of increasing drought and soil‐borne pathogens on tree regeneration in two types of mixed oak forests (Quercus suber‐Q. canariensis and Q. suber‐Olea europaea) invaded by the exotic soil‐borne oomycete Phytophthora cinnamomi, one of the most aggressive plant pathogens on earth. We conducted a seed sowing experiment with oomycete‐specific fungicide taking advantage of rainfall exclusion infrastructures that excluded 30% of the annual rainfall, simulating predictions of climate change models for Mediterranean systems. Seedling emergence, survival and growth of the three tree species were followed during 3 years. We found that neutral or positive drought effects on regeneration dominated over negative effects in the tree community. Moreover, most positive drought effects on the dominant species (Q. suber) were not direct, but indirectly mediated by soil‐borne pathogens. This was shown by the fact that positive drought effects disappeared with fungicide application. Synthesis: Overall, our results suggest that rainfall reductions predicted by climate change models for the Mediterranean region might have minor direct negative effects on early regeneration of tree species, but could play a major indirect role by limiting the negative effects of exotic pathogens on highly susceptible tree species. These findings highlight that antagonisms among global change drivers should be recognized as important forces that might slow down the current loss of tree health.
... Whereas some future climate scenarios, including drying, may reduce the severity of Phytophthora diseases in certain regions, other regions may experience an increase in severity of the disease due to optimal conditions for the manifestation of the phenomenon (Aguayo et al. 2014;Homet et al. 2019). Phytophthora diseases may also interact with climate drivers of tree stress to cause greater tree die-off and mortality (Corcobado et al. 2014). Finally, climate change is likely to result in tree damage that is rarely documented, which has the potential to mimic disease symptoms and lead to misdiagnosis. ...
Article
Context Forest ecosystems experience compositional and structural changes as species’ environmental envelopes shift with climate change. Extreme climate events and pests/pathogens are driving these ecosystem changes. Determining which of the two potential drivers is causing a particular forest die-off can be challenging. In south-western Australia, widespread forest die-off in 2011 coincided with extremely hot and dry conditions. It occurred in a forest ecosystem that has historically experienced Phytophthora cinnamomi root disease (Phytophthora dieback). Aims To determine whether the causal agent of Phytophthora dieback, P. cinnamomi, was associated with forest die-off in the Northern Jarrah Forest. Methods A combination of direct (isolation of pathogen) and indirect (survey of susceptible indicator plant species) measurements were taken inside and outside patches of forest experiencing the die-off. Key results There was no consistent association between die-off patches and the presence of P. cinnamomi. P. cinnamomi was isolated from 3 of 33 control plots and 3 of 33 die-off plots. Although several plant species susceptible to P. cinnamomi were absent from die-off plots, the findings were inconsistent across species. This may be explained by plant tolerance to high temperatures and drought. Conclusions P. cinnamomi was not the proximate cause of the observed die-off in the Northern Jarrah Forest in 2011. Implications Novel disturbance caused by extreme climate events can mimic damage caused by certain pests/pathogens. More research is needed to determine the tolerances of plants to extreme temperature and drought conditions to disentangle abiotic and biotic drivers of tree die-off.
... The combination of treering δ 13 C with genetic data has already proven to be a promising approach to investigate the prospects of artificial stands for ex situ conservation (Santini et al., 2020); therefore, we suggest its use in the selection of drought-tolerant genotypes of seed-bearing plants to preserve Mediterranean holm oak ecosystem types. It should be noted that the association of drought with pathogenic infections may have a destructive impact on Mediterranean oak forest ecosystems (Corcobado et al., 2014). In particular, the interaction of pathogens such as P. cinammonni or Biscogniauxia spp. with drought events can make Q. ilex particularly susceptible to dieback, even in the case of non-lethal infections (Corcobado et al., 2013;Ruiz-Gómez et al., 2019;San-Eufrasio et al., 2021;Encinas-Valero et al., 2022). ...
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Oak decline has been a serious problem in Europe since the beginning of the twentieth century. In south-west Spain, Quercus ilex and Q. suber are the main affected species, and their decline has been associated with Phytophthora cinnamomi. During the last 10 years, a severe decline of Q. ilex and Q. faginea accompanied by a significant decrease in the production of acorns affecting natural regeneration was observed in the eastern part of the Iberian Peninsula. Therefore, the aim of this study was to investigate the possible involvement of Phytophthora spp. in the decline. A forest in the Natural Park ‘Carrascar de la Font Roja’ in Comunidad Valenciana (eastern Spain), which is dominated by Q. ilex and Q. faginea, was surveyed during 2010–2011. Symptomatic trees showed thinning and dieback of the crown, withering of leaves and death. An extensive loss of both lateral small woody roots and fine roots and callusing or open cankers on suberized roots were observed. Soil samples containing fine roots were baited using both Q. robur leaves and apple fruits. Six Phytophthora species were isolated: P. cryptogea, P. gonapodyides, P. megasperma, P. quercina, P. psychrophila and P. syringae. These are the first records of P. quercina and P. psychrophila on Q. faginea, of P. quercina in Spain and of P. psychrophila in mainland Spain. A soil infestation trial was conducted for 6 months under controlled conditions with 1-year-old seedlings of Q. ilex and Q. faginea. Phytophthora cinnamomi was included in the pathogenicity test for comparison. The results showed that Q. ilex seedlings were generally more susceptible to infection than Q. faginea with P. cinnamomi being the most aggressive pathogen to both oak species. The two most commonly isolated Phytophthora species, P. quercina and P. psychrophila, also proved their pathogenicity towards both Q. ilex and Q. faginea.