Adaptive evolution of chestnut forests to the impact of ink disease in Spain

Alcaide, Francisco; Solla, Alejandro; Cherubini, M.; Mattioni, Claudia; Cuenca, B.; Camisón, Álvaro; Martı́n, Mercedes

doi:10.1111/jse.12551

Cited by 22 publications

(9 citation statements)

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“…Chestnut ink disease is widespread in Europe (Alcaide et al., 2020; Vannini & Vettraino, 2001) and it will likely expand to new areas and increase its severity in a global warming context (Jung et al., 2018). In fact, the disease has already expanded to northern France (Cécile Robin, INRAE, Univ.…”

Section: Discussionmentioning

confidence: 99%

“…), highly susceptible to the oomycete Phytophthora ×alni Brasier & S. A. Kirk; and (3) U. minor , highly susceptible to the ascomycete Ophiostoma novo‐ulmi Brasier. These three pathosystems were selected as they are widespread and have resulted in extensive dieback and tree mortality in southern Europe (Alcaide et al., 2020; Ghelardini et al., 2017; Jung et al., 2018; Solla et al., 2010; Zamora‐Ballesteros et al., 2016).…”

Section: Methodsmentioning

confidence: 99%

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Invasive forest pathogens affect the characteristics, microbial colonisation, and decomposition of leaf litter in streams

2021

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Invasive tree pathogens threaten forests worldwide, but their effects on streams are poorly understood. Nevertheless, tree infections that lead to changes in the characteristics of litter inputs to streams may affect stream communities and ecosystem processes. We studied cross‐ecosystem effects derived from Phytophthora cinnamomi, Phytophthora ×alni, and Ophiostoma novo‐ulmi infection on Castanea sativa (chestnut), Alnus lusitanica (alder), and Ulmus minor (elm) trees, respectively, by assessing physical and chemical characteristics of senescent leaves from healthy, symptomatic, and highly symptomatic individuals. Leaf litter from the three health statuses per tree species was then incubated in laboratory microcosms and the effects of tree infection on microbial decomposers and leaf litter decomposition were assessed. Tree infection significantly affected leaf litter characteristics, microbial decomposers and leaf litter decomposition, and the health status of trees conditioned these effects differently depending on the tree species. In C. sativa, leaf litter of highly symptomatic trees had higher toughness, higher polyphenolic concentration and slower decomposition than leaf litter of symptomatic and healthy trees. In A. lusitanica, leaf litter of highly symptomatic trees had higher phosphorus concentration, lower carbon:phosphorus ratio and faster decomposition than leaf litter of symptomatic and healthy trees. Finally, in U. minor, leaf litter of highly symptomatic trees had higher nitrogen concentration and lower carbon:nitrogen ratio than leaf litter of healthy trees, and faster decomposition than leaf litter of symptomatic and healthy trees. Effects of changes in litter characteristics on litter decomposition were mediated by changes in microbial decomposer colonisation and activity. The composition of the aquatic hyphomycetes communities associated with C. sativa and U. minor litter varied depending on the tree health status. Most striking was the two‐fold higher aquatic hyphomycetes species richness in litter of U. minor trees infected with O. novo‐ulmi than in litter of healthy U. minor trees. Tree infection alters the nutritional quality of leaf litter, potentially affecting the functioning of aquatic ecosystems strongly dependent on riparian litter inputs.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Invasive forest pathogens affect the characteristics, microbial colonisation, and decomposition of leaf litter in streams

2021

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“…Several circumstances suggest that the three P. cinnamomiinfected mother trees used were not tolerant to ink disease: (i) there is no evidence of C. mollissima and C. crenata germplasm in Hervás forest, in contrast to other forests in northern Spain (Alcaide et al 2020) in which genes from Asiatic germplasm confer resistance to P. cinnamomi in offspring; (ii) inoculation with P. cinnamomi of progenies from 16 additional mother trees, selected in Hervás at random, resulted in circa 100% of seedling mortality (Alcaide et al 2020); and (iii) in spring 2019, tree 4 was almost dead and tree 6 was dead.…”

Section: Seed Weight and Offspring Of Ink-diseased Chestnutsmentioning

confidence: 99%

“…The high genetic diversity in C. sativa (Martin et al 2010;Cuestas et al 2017;Martín et al 2017), reflected in within-and among-population variation in traits of adaptive significance associated with tolerance to Phytophthora sp. (Robin et al 2006;Santos et al 2015;Alcaide et al 2020) and water stress (Pliura and Eriksson 2002;Ciordia et al 2012;Alcaide et al 2019), suggests that the species is highly adaptable to environmental changes. Phenotypic plasticity for adaptation can also be achieved through transmitted maternal effects (Marshall and Uller 2007).…”

Section: Introductionmentioning

confidence: 99%

Increased tolerance to Phytophthora cinnamomi in offspring of ink-diseased chestnut (Castanea sativa Miller) trees

Camisón

Martı́n

Oliva

et al. 2019

Annals of Forest Science

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& Key message Increased tolerance to Phytophthora cinnamomi was observed in small-sized offspring of ink-diseased chestnut trees, suggesting that a virulent pathogen can trigger a defence response of trees in the subsequent generation. Increased tolerance to water stress was not observed in offspring of chestnut trees. & Context In sweet chestnut (Castanea sativa Miller), P. cinnamomi Rands is responsible for the widespread and destructive ink disease. & Aims We investigated if the susceptibility of C. sativa to water stress and P. cinnamomi depends on the health status of mother trees. & Methods Plants were grown from seeds collected from healthy and ink-diseased chestnut trees. Leaf wilting after drought exposure and plant mortality after pathogen inoculation were assessed. & Results Offspring of ink-diseased trees had poorer performance in plant height and root biomass than offspring of healthy trees, with allocation of biomass to seeds mediating this effect. Leaf wilting due to water stress was similar in offspring of healthy and P. cinnamomi-infected trees. However, increased tolerance to P. cinnamomi was observed in small-sized seedlings, suggesting that tolerance in C. sativa may involve growth costs. This is the first report of increased tolerance to P. cinnamomi in plants germinating from a diseased tree. & Conclusion The results suggest that an invasive pathogen can regulate the performance and prime a defence response of a forest tree species in the subsequent generation, and generate conflicting selection pressures related to plant size.

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“…Gene editing (Doudna and Charpentier, 2014;Dort et al, 2020) and transgenics (Campbell et al, 2003) can also transfer or silence allelic variants of major effects within a single generation (Pereira-Lorenzo et al, 2019). These may replicate the success of tolerant chestnuts (Alcaide et al, 2019a;Westbrook et al, 2019) and promote reproductive sterility (Meilan et al, 2001;Fritsche et al, 2018). Yet, molecular breeding via MAS, MAB and gene editing is often inefficient to trace quantitative traits as growth and adaptation to abiotic stresses.…”

Section: Predictive Breeding Promises Boosting Forest Tree Genetic Immentioning

confidence: 99%

Modern Strategies to Assess and Breed Forest Tree Adaptation to Changing Climate

2020

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Studying the genetics of adaptation to new environments in ecologically and industrially important tree species is currently a major research line in the fields of plant science and genetic improvement for tolerance to abiotic stress. Specifically, exploring the genomic basis of local adaptation is imperative for assessing the conditions under which trees will successfully adapt in situ to global climate change. However, this knowledge has scarcely been used in conservation and forest tree improvement because woody perennials face major research limitations such as their outcrossing reproductive systems, long juvenile phase, and huge genome sizes. Therefore, in this review we discuss predictive genomic approaches that promise increasing adaptive selection accuracy and shortening generation intervals. They may also assist the detection of novel allelic variants from tree germplasm, and disclose the genomic potential of adaptation to different environments. For instance, natural populations of tree species invite using tools from the population genomics field to study the signatures of local adaptation. Conventional genetic markers and whole genome sequencing both help identifying genes and markers that diverge between local populations more than expected under neutrality, and that exhibit unique signatures of diversity indicative of "selective sweeps." Ultimately, these efforts inform the conservation and breeding status capable of pivoting forest health, ecosystem services, and sustainable production. Key long-term perspectives include understanding how trees' phylogeographic history may affect the adaptive relevant genetic variation available for adaptation to environmental change. Encouraging "big data" approaches (machine learning-ML) capable of comprehensively merging heterogeneous genomic and ecological datasets is becoming imperative, too.

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Adaptive evolution of chestnut forests to the impact of ink disease in Spain

Cited by 22 publications

References 72 publications

Invasive forest pathogens affect the characteristics, microbial colonisation, and decomposition of leaf litter in streams

Invasive forest pathogens affect the characteristics, microbial colonisation, and decomposition of leaf litter in streams

Increased tolerance to Phytophthora cinnamomi in offspring of ink-diseased chestnut (Castanea sativa Miller) trees

Modern Strategies to Assess and Breed Forest Tree Adaptation to Changing Climate

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