Phytophthora ramorum is a generalist plant pathogen with differences in virulence between isolates from infectious and dead‐end hosts

Variation in virulence was examined among isolates of Phytophthora ramorum from epidemiologically important or infectious (non‐oak) and transmissive dead‐end (oak) hosts from North America. Twelve isolates representative of the genetic, geographic and host range of P. ramorum in the western United States were inoculated on leaves of Umbellularia californica (bay laurel or bay) and stems of Quercus agrifolia (coast live oak). In spite of extreme genetic similarity among the isolates employed, and even within the same genotype, significant differences in lesion size were measured, suggesting virulence in this pathogen is also controlled by epigenetic factors. A strong positive correlation between lesion size on bay laurel and coast live oak provides experimental evidence P. ramorum is a generalist pathogen that lacks host specificity. Isolates from non‐transmissive oaks were significantly less pathogenic both on oaks and bays than isolates from infectious hosts. These results are essential to further our understanding of the epidemiology and evolutionary potential of this pathogen. A quantitative differential in virulence of isolates from hosts with different epidemiological roles has been described for many animal diseases, but is a novel report for a plant disease.     

Cypress mortality (mal del cipres) in the Patagonian Andes: comparisons with similar forest diseases and declines in North America

Widespread mortality of Cordilleran cypress (Austrocedrus chilensis) occurs in developed and pristine forests in south-western Argentina and possibly south-eastern Chile. Affected trees may die rapidly but mortality is commonly preceded by several decades of severely restricted radial stem growth. Roots are often affected by one or more types of decay. Cypress mortality, locally termed ‘mal del cipres’, is similar to a major forest disease in North America: Port-Orford-cedar (Chamaecyparis lawsoniana) root disease in Oregon and California and a major tree decline: Alaska yellow-cedar (Chamaecyparis nootkatensis) decline in south-east Alaska. This paper discusses several hypotheses concerning mal del cipres and compares current forest decline research in Patagonia with North America.     

Radial variation of vessel size and distribution in cork oak wood (<Emphasis Type="Italic">Quercus suber</Emphasis> L.)

Quercus suber L. is an important species producing cork whose wood characteristics have not been investigated a lot. Cork oak wood vessels are a striking feature and the most abundant wood tissue largely influencing density and permeability. Vessel size and distribution were studied in approximately 40 year-old and never debarked cork oaks by continuously measuring along the radial direction in the transverse section of wood discs taken at 1.3 m of height using image analysis techniques. The vessel size increases with age from 7660 ± 2286 to 21136 ± 6119 μm², the conductive area from 5.4 ± 2.2 to 11.6 ± 3.9%, and the vessel density remains approximately constant between 5.2 ± 1.5 and 7.3 ± 3.5 vessels/mm². In comparison with ring-porous and some evergreen oaks, cork oaks show a similar conductive area but smaller vessels. Vessel architecture is known to play an important role on oaks tolerance to hydric stress, and these cork oak trees were growing under very harsh edaphoclimatic conditions, not tolerated by other oaks. The well-developed and deep root system allowing access to constant water supply may contribute to the cork oak’s relatively high conductive area.     

The condition of the phloem in declining oaks

Oaks (Quercus petraea, Q. robur) from several sites in eastern Austria affected by novel oak decline (NOD), as well as oaks (Q. robur) showing symptoms of oak yellows (OY), were tested for the presence of mycoplasma-like organisms (MLOs). The samples, comprising roots, annual shoots, and branches, were examined using light-, fluorescence-, and electron-nucroscopic techniques. Staining with the DNA-fluorochrome DAPI provided no evidence for the presence of MLOs in any of the samples. Furthermore, no pathological sieve-tube necrosis and no abnormal callose accumulation could be observed. An association of MLOs with‘novel oak decline’ or ‘oak yellows’ is, therefore, unlikely.     

Diplodia twig canker (Diplodia gallae) of northern red oak (Quercus rubra) in the northeastern United States

The 2015–2018 outbreak of spongy moth (Lymantria dispar) in southern New England initiated a severe oak decline and mortality event. While defoliation was a primary driver, increased secondary pest and pathogen activity contributed to decline and death. Following this large defoliation event, Diplodia was frequently recovered from northern red oaks (Quercus rubra) with serious outbreaks of twig cankering. Given the many recent reports of Diplodia corticola on oak in eastern North America, it was presumed to be the causal agent. To confirm, a limited survey was conducted from five states in the region (Maine, Massachusetts, New Hampshire, New York, and Vermont). Based on ITS, tef1 and tub2 sequences generated from 28 isolates collected primarily from northern red oak, Diplodia gallae, two potentially novel Diplodia species and Diplodia sapinea were identified. Surprisingly, D. corticola was not found in this study. ITS sequences alone failed to discriminate among isolates of D. gallae and D. corticola, creating uncertainty over previous reports of D. corticola in eastern North America. Only a combined ITS + tef1 dataset successfully distinguished D. gallae and D. corticola along with two other closely related species that also occur on oak (Diplodia quercicola and Diplodia quercivora). Additional cankering and endophytic fungi (Coryneum, Dendrostoma, Gnomoniopsis, Pestalotiopsis and Tubakia) were also found on symptomatic oaks in the region. Identification of Diplodia isolates from non-Quercus hosts also detected Diplodia neojuniperi on Juniperus chinensis and Microbiota decussata, which has not been reported previously in North America.     

Relationship between presence of basidiomes,above‐ground symptoms and root infection by Collybia fusipes in oaks

Collybia fusipes is a common cause of root rot on oak in the north of France. Collybia fusipes basidiomes can be as frequent on oaks in stands where no decline of the trees occurs compared with stands where the decline is chronic. This might be explained by differences in the amount of roots damaged by the parasite. To test that hypothesis, 430 oak trees, Quercus petraea, Quercus robur and Quercus rubra, located in six forests were selected. Half of them showed C. fusipes basidiomes at the trunk base. The association between presence of basidiomes and decline of affected trees depended on the forest. The level of infection of each tree by C. fusipes, as well as the crown appearance, the tree height : diameter at breast height ratio, age and sapwood width were determined. The presence of C. fusipes basidiomes was always associated with significant root infections. The crowns of the trees deteriorated with increasing level of root infection and the decline was severe only when the root damage was heavy. Although the decline of trees that were heavily damaged by C. fusipes was severe in some of the stands, in others, it was only mild, and so the differences in tree decline between the stands could not be attributed solely to differences in root infection severity. Trees damaged by C. fusipes seemed not to be subjected to more competition than their undamaged neighbour as reflected by a similar tree height: diameter at breast height ratio.     

The anatomical traits of trunk wood and their relevance to oak (Quercus robur L.) vitality

Oaks’ decline in vitality is attributed to a complex process that involves interactions of several factors leading to increased trees’ mortality. This study investigates the structure of trunk wood of oaks with reference to its physiological role in hydraulic conductivity. On the basis of the crown condition, the oaks were classified into three health groups: healthy trees, declining trees and dead trees. Anatomical traits of wood, such as annual ring width, vessel density, vessel diameter of earlywood and theoretical hydraulic conductivity, were measured and calculated. The narrowest annual rings formed by the cambium were observed in dead oaks. These trees were also characterized by the smallest diameter of earlywood vessels, not only in the period of occurrence of dieback symptoms, but also during their whole life. It is suggested that the formation of narrow annual rings and earlywood vessels of small diameter increases susceptibility of a tree to decay. A reduced vessel diameter implies changes in hydraulic conductivity of oak trunks and thus impairs the water transport, which affects the health of trees. The process of oak decline is considered to have characteristics of natural selection and leads to the elimination of the weakest trees.     

Phytophthora disease of Quercus ilex in south‐western Spain

Oak decline that was affecting three holm oak sites in the province of Huelva (south‐western Spain) was studied during 1998–1999. The syndromes of dieback and sudden death have been observed and, in both cases, foliar symptoms were associated with root rot. Characterization of the fungal isolates from necrotic roots led us to identify Phytophthora cinnamomi A2 as consistently associated with the disease. The optimum growth temperatures of these isolates were very high (30°C). Inoculation tests under controlled conditions demonstrated the pathogenicity of the isolates on holm and cork oak seedlings. None of the other biotic factors of Mediterranean oak decline that have been previously described were found in the present study and so, in this case, the forest decline model does not seem to be necessary in order to explain the disease observed. The defoliation and mortality of the oaks was primarily caused by P. cinnamomi, although some abiotic factors such as alternating periods of drought and wet weather in the region may play an important role.     

Decline of Mediterranean oak trees and its association with Phytophthora cinnamomi: a review

Mortality events in cork and holm oaks have occurred in the Mediterranean basin since the beginning of the XX century, but severity of decline increased during the 1980s. By that time, the exotic soil borne pathogen Phytophthora cinnamomi was often recovered from declining stands and since then it has been considered the main factor associated with decline. This work analyses data concerning P. cinnamomi surveys in cork and holm oaks trees, pathogenicity tests carried out in controlled experiments, studies about the influence of site characteristics in tree decline and approaches to control the disease. Results of field surveys showed that the pathogen is widespread and pathogenicity tests suggested that host susceptibility to the pathogen is moderate when seedlings are in appropriate watering conditions, particularly cork oaks. Occurrence of decline is also associated with soil characteristics that interfere with root expansion and water retention. We assessed the relative importance of each factor involved in decline and revised the role of P. cinnamomi in cork and holm oak decline.     

Elm yellows: A phytoplasma disease of concern in forest and landscape ecosystems

Elm yellows (EY) is a lethal or decline phytoplasma disease that affects several Ulmus (elm) species and hybrids, which is widespread in North America and Europe. The symptoms vary among the elm species. In those native to North America, main symptoms include epinasty, chlorosis, premature casting of the leaves, yellow to brown discoloration of the phloem in the roots and stem and tree death that usually occurs within 1 or 2 years from the appearance of foliar symptoms. In contrast, affected trees of European and Asian species are primarily characterized by witches’ broom as a specific symptom, do not show phloem discoloration and are less prone to decline. The disease is caused by a relatively genetically homogeneous phytoplasma, the EY agent “Candidatus Phytoplasma ulmi,” a member of the EY phytoplasma group or 16SrV group, subgroup 16SrV‐A. In nature, this pathogen exhibits a high plant host specificity. The elm leafhopper Scaphoideus luteolus is the only confirmed vector of EY phytoplasma in North America, whereas Macropsis mendax has been reported as a natural vector in Northern Italy. However, other insect vectors are likely to be involved in its natural spread. Phytoplasmas of other taxonomic groups or 16SrV subgroups, which are known to infect a wide range of plant hosts, have been identified in naturally infected elm trees. However, the pathological relevance of these “non‐elm” phytoplasmas needs to be confirmed in many cases. Their detection is mainly based on the highly sensitive nested PCR assays, while pathological data are lacking. This study summarizes, within the framework of a single comprehensive review, the current knowledge of EY. Gaps in knowledge of this disease and prospects for future research are also critically discussed.     

Characteristics of the Cryphonectria parasitica isolated from Quercus in Slovakia

The occurrence of chestnut blight (Cryphonectria parasitica) on oaks in mixed chestnut‐oak forests was studied in 2003–2008 in Slovakia. Infections on living Quercus trees were found at four of seven localities. The disease incidence on oaks ranged from 1.3% to 15.8%. The symptoms on infected oaks were similar to those on chestnut, but less conspicuous. Cankers of C. parasitica were found only on Quercus robur and Q. petraea. A total of 22 isolates of C. parasitica, all virulent, were isolated. Each site yielded only a single vc type (EU12 or EU13). Field inoculation experiments on chestnuts with seven strains of C. parasitica from oaks and an isolate from Castanea sativa showed no differences in virulence. On Quercus robur stems, the cankered area was significantly smaller than on C. sativa and the cankers developed very slowly.     

Change in oak abundance in the eastern United States from 1980 to 2008

Although oaks (Quercus spp.) have historically dominated much of the forest land in eastern North America, a great deal of fragmentary and sometimes anecdotal evidence suggests that they have been yielding dominance in recent decades to other, typically more shade-tolerant species. Using FIA data, our work formally quantifies the change in oak abundance in the eastern U.S. during the period of 1980-2008. The results indicate that most areas in the eastern U.S. experienced some decline in oak abundance, but the decrease was not universal either geographically or among species. Declines were especially marked in the Central Hardwood Region, which lost oak abundance on 81% its forested area as measured by importance value (IV). Areas with a high oak abundance were more likely to see a reduction in abundance. Among all 25 species analyzed, eight species decreased significantly in IV while two increased. Both the top two most prevalent white oak species (white oak (Quercus alba) and post oak (Quercus stellata)) and red oak species (northern red oak (Quercus rubra) and black oak (Quercus velutina)) had significant decreases in density and IV. Water oak (Quercus nigra) is one of the red oak species that had a near universal increase of its abundance throughout its native range (83% of area). This study provided a comprehensive quantification of the dynamic of oak species in a regional-wide geographic context, which will provoke forest researchers and managers to revisit the oak decline problem by using knowledge from other regions and other species.     

Pines versus oaks: effects of fire on the composition of Madrean forests in Arizona

I examined contrasts in response to moderate-intensity fire between two pine species (Pinus leiophylla Schiede and Deppe and P. engelmannii Carr.) and four oak species (Quercus hypoleucoides Camus., Q. arizonica Sarg., Q. emoryi Torr., and Q. rugosa Nee.) in Madrean forests in southeastern Arizona. Stem survival of pines after fire was greater than for oaks, but oaks sprouted more successfully after top-kill than did the only sprouting pine species, P. leiophylla. As a result, post-fire decline and subsequent recovery in oak populations was more marked than for the pines, and the ratio of oaks to pines decreased as a result of fire but increased during recovery. In typical forest stands, most individuals established from 1860 to 1920 at the interface between a period of high fire frequency and the onset of fire exclusion. Ages of Q. hypoleucoides were more clustered than for the pines, suggesting post-fire sprouting rather than long-term top-survival of fire. The results point to contrasts in mechanisms of persistence in this fire-prone ecosystem: fire resistance in the pines versus post-fire sprouting in the oaks. As a result, fire regime controls the balance between the two groups, with moderate-intensity fire favoring the pines and periods of low fire frequency – due to natural causes or anthropogenic fire exclusion – favoring the oaks. The species and community response patterns found in this study may apply generally to other pine-oak communities.     

Contrasting net primary productivity and carbon distribution between neighboring stands of Quercus robur and Pinus sylvestris

Standing biomass, net primary production (NPP) and soil carbon (C) pools were studied in a 67-year-old pedunculate oak (Quercus robur L.) stand and a neighboring 74-year- old Scots pine (Pinus sylvestris L.) stand in the Belgian Campine region. Despite a 14% lower tree density and a lower tree height in the oak stand, standing biomass was slightly higher than in the pine stand (177 and 169 Mg ha(-1) in oaks and pines, respectively), indicating that individual oak trees contained more biomass than pine trees of similar diameter. Moreover, NPP in the oak stand was more than double that in the pine stand (17.7 and 8.1 Mg ha(-1) year(-1), respectively). Several observations indicated that soil organic matter accumulated at higher rates under pines than under oaks. We therefore hypothesized that the pines were exhibiting an age-related decline in productivity due to nutrient limitation. The poor decomposability of pine litter resulted in the observed accumulation of organic matter. The subsequent immobilization of nutrients in the organic matter, combined with the already nutrient-poor soil conditions, resulted in a decrease in total NPP over time, as well as in a substantial shift in the allocation of NPP toward fine roots. In the oak stand, litter is less recalcitrant to decay and soil acidity is less severe; hence, organic matter does not accumulate and nutrients are recycled. This probably explains why NPP was much higher in the oaks than in the pines and why only a small proportion of NPP was allocated to oak fine roots.     

Susceptibility of the Quercus rubra root system to Phytophthora cinnamomi; comparison with chestnut and other oak species

The susceptibility of oak seedlings (Quercus palustris, Quercus robur, Quercus rubra) and chestnut seedlings (Castanea sativa) to Phytophthora cinnamomi was tested. The dynamics of infection was examined in plant material raised in a rhizotron. In the oak species, primary root tissues were susceptible whereas secondary cortical tissues showed some resistance to P. cinnamomi. Secondary cortical tissues of the tap root in C. sativa were susceptible. Inoculations with P. cinnamomi were performed both in situ and on excised roots of mature Q. rubra. In both cases, the resistance of Q. rubra roots and shoots was negatively correlated with diameter at the inoculation point. Small roots (l–5-cm diameter) were resistant, whereas collar and trunk were susceptible. In contrast to oak, small excised roots of mature C. sativa (0.7–2-cm diameter) were susceptible to P. cinnamomi. This may explain why P. cinnamomi does not induce a decline of the attacked oaks, but rather a trunk canker.     

Specific hybridization real‐time PCR probes for Phytophthora ramorum detection and diagnosis

Sudden Oak Death, caused by Phytophthora ramorum, poses a serious threat to native American oaks, and is also present in Europe where it has been isolated from numerous European ornamental plant nurseries. Its proven aggressiveness against plants in the Fagaceae and Ericaceae and the damage it has caused in North America have lead to it being assigned quarantine status. The timely and accurate detection of P. ramorum is a critical aid in the study of the epidemiology and biology of this pathogen. As a regulated organism, the availability of a sensitive and reliable assay is essential when attempting to achieve early detection of the pathogen. In this work, new specific hybridization probes for a real‐time PCR amplification method were found to be rapid, robust and labour‐saving, and proved suitable for routine use in a molecular diagnostic laboratory.     

Strain‐related pathogenicity in Diplodia corticola

Diplodia corticola is one of the most aggressive fungal pathogens of Quercus species and is involved in the decline of Mediterranean cork oak forests and Californian oaks. Information regarding variation in virulence between strains is scarce. We hypothesize that D. corticola strains differ in virulence and consequently induce different symptoms in infected plants. To test this, infection assays were carried out on Quercus suber half‐sib seedlings with seven strains of D. corticola. Visual symptoms of infection (external lesions, leaf wilting, exudation and others) were recorded in parallel with physiological and biochemical parameters. All strains were able to cause lesions but at differing levels of aggressiveness. We show that internal lesion length did not correlate directly with strain aggressiveness and this agrees with physiological parameters that should be taken into account to infer about strain pathogenicity. Infection by all strains induced an overall negative impact on the net photosynthetic rate and an increase in the oxidative stress status of plants; however, significant differences were found when the effects of different strains were compared. Results also suggest that being under optimum growth conditions, prior to and during infection, allowed plants to respond to the pathogen. At the end of the experiment, some strains of D. corticola established a latent pathogen‐like relationship with cork oak. This is the first study to show that D. corticola virulence is strain‐dependent.     

Recent insights into the pandemic disease butternut canker caused by the invasive pathogen Ophiognomonia clavigignenti‐juglandacearum

In the 25 years following the initial 1967 report of the disease, butternut canker was able to quickly spread throughout the entire range of butternut (Juglans cinerea) in North America, from Minnesota in the upper Midwest to Tennessee in the south and Quebec in the north‐east. The speed of this dispersal is notable as butternut trees do not make up a significant proportion of any single forest type. Instead, they are usually found sparingly in most mixed hardwood forests. In this review, we synthesize the current knowledge of the invasion process of the butternut canker pathogen, Ophiognomonia clavigignenti‐juglandacearum, an invasive fungal pathogen, that as its emergence has spread across North America and is now found wherever butternut naturally occurs. Taxonomic studies have determined that the fungus belongs in the genus Ophiognomonia, which includes a number of saprophytes, endophytes and pathogens of members of the Fagales, rather than the genus Sirococcus, which includes several important pine pathogens. The ability of fungus to be dispersed by rain splash, transported on and in beetle vectors, transmitted by infected seed and successfully colonized several species of Juglans and Carya have all likely contributed to the rapid increase in abundance and severity of disease and tree mortality in the invaded forest ecosystems. Recent genomic and population genetic analyses have determined that there were at least three emergence events. A less virulent strain of the fungus likely has been present in the north eastern United States for over a century, but it was the emergence of a more virulent strain of the fungus in Minnesota and Wisconsin in the 1960s that resulted in range‐wide mortality and pushed butternut to be listed as an endangered species in Canada and a number of states in the United States.     

Intra- and interspecific competition differently influence growth and stem quality of young oaks (Quercus robur L. and Quercus petraea (Mattuschka) Liebl.)

Context

Cluster planting has become a conventional establishment method for oaks in Central Europe, where the spacing of seedlings within clusters varies between ‘nests’ (0.2?×?0.2 m) and ‘groups’ (1?×?1 m). Although the space between clusters is expected to fill with voluntary regeneration, its competitive effect on oak growth and quality had not been studied yet.

Aims

The aim of the study was to analyse the effects of inter- and intraspecific interactions on growth and quality of oaks grown in cluster plantings by quantifying the influence of neighbouring trees. In addition, we analysed whether the spatial position of oaks within groups (inner section or periphery) influenced their quality development.

Methods

Using Hegyi’s competition index, the influence of competition from intra- and interspecific trees from early, mid- and late-successional species, on diameter, height, slenderness and quality (length of branch-free bole) of 10- to 26-year-old oaks grown in cluster planting stands was quantified at seven sites in Baden-Württemberg and Hessen, Germany.

Results

In general, mid- and late-successional trees exerted a stronger competitive influence on growth of target oaks in clusters than the conspecific oaks and pioneer tree species. Oak quality development benefited from intraspecific competition, but self-pruning was not further promoted through additional interspecific competition. Within groups, inner oaks had a higher probability of developing into potential future crop trees than outer oaks.

Conclusion

Our study showed that intra- and interspecific competition had different effects on target oak trees and that these effect differed between nest and group plantings. The development of naturally regenerated and planted trainer trees in group plantings should be monitored carefully and if necessary be controlled through thinning or pollarding.