Genome scanning for interspecific differentiation between two closely related oak species [Quercus robur L. and Q. petraea (Matt.) Liebl.

Interspecific differentiation values (G(ST)) between two closely related oak species (Quercus petraea and Q. robur) were compiled across different studies with the aim to explore the distribution of differentiation at the genome level. The study was based on a total set of 389 markers (isozymes, AFLPs, SCARs, microsatellites, and SNPs) for which allelic frequencies were estimated in pairs of populations sampled throughout the sympatric distribution of the two species. The overall distribution of G(ST) values followed an L-shaped curve with most markers exhibiting low species differentiation (G(ST) < 0.01) and only a few loci reaching >10% levels. Twelve percent of the loci exhibited significant G(ST) deviations to neutral expectations, suggesting that selection contributed to species divergence. Coding regions expressed higher differentiation than noncoding regions. Among the 389 markers, 158 could be mapped on the 12 linkage groups of the existing Q. robur genetic map. Outlier loci with large G(ST) values were distributed over 9 linkage groups. One cluster of three outlier loci was found within 0.51 cM; but significant autocorrelation of G(ST) was observed at distances <2 cM. The size and distribution of genomic regions involved in species divergence are discussed in reference to hitchhiking effects and disruptive selection.     

Strength, diversity and plasticity of postmating reproductive barriers between two hybridizing oak species (Quercus robur L. and Quercus petraea (Matt) Liebl.)

Very little is known about the nature and strength of reproductive isolation (RI) in Quercus species, despite extensive research on the estimation and evolutionary significance of hybridization rates. We characterized postmating pre- and postzygotic RI between two hybridizing oak species, Quercus robur and Quercus petraea, using a large set of controlled crosses between different genotypes. Various traits potentially associated with reproductive barriers were quantified at several life history stages, from pollen-pistil interactions to seed set and progeny fitness-related traits. Results indicate strong intrinsic postmating prezygotic barriers, with significant barriers also at the postzygotic level, but relatively weaker extrinsic barriers on early hybrid fitness measures assessed in controlled conditions. Using general linear modelling of common garden data with clonal replicates, we showed that most traits exhibited important genotypic differences, as well as different levels of sensitivity to micro-environmental heterogeneity. These new findings suggest a large potential genetic diversity and plasticity of reproductive barriers and are confronted with hybridization evidence in these oak species.     

Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L

Quercus petraea and Quercus robur are two closely related oak species that frequently hybridize. We sequenced 70 clones containing the 5.8S and ITS2 regions of ribosomal DNA (rDNA) from these two species and did not detect a species-specific difference. Surprisingly, three divergent (up to 12.6%) rDNA families were identified in both species, indicating that they predate the speciation event. Despite a large between-rDNA-families divergence, rDNA sequences were very similar within families, suggesting ongoing concerted evolution. Expression analysis, relative-rate tests, and mutation spectrum analyses indicated that only a single rDNA family is functional. We propose that past hybridization events, combined with nucleolar dominance, were the evolutionary processes underlying the contemporary rDNA variability in Q. petraea and Q. robur.     

Tree rooting patterns and soil water relations of healthy and damaged stands of mature oak (Quercus robur L. and Quercus petraea [Matt.] Liebl.)

At three sites in northwestern Germany, which represent the centres of the present oak damage, root distribution and biomass beneath healthy and damaged trees of mature pedunculate oak (Quercus robur L.; Neuenburg site) and sessile oak (Q. petraea [Matt.] Liebl.; Lappwald and Sprakensehl sites) were investigated, and soil texture, bulk density, duration of waterlogging periods and the water available in the mineral soil were determined. For Neuenburg and Sprakensehl, the available soil water was related to leaf water parameters determined in a separate investigation. At the clayey and hydromorphic sites of Neuenburg and Lappwald, the measurements were performed in each one healthy and one damaged part of the site, which differed in the number of oaks with crown damage. In the damaged stand of Neuenburg, the clay content of the subsoil was higher than in the healthy stand, and the soil water availability was reduced especially in dry periods. Compared to healthy oaks of the healthy stand, the density of finest plus fine roots as well as the biomasses of finest roots were lower beneath damaged oaks of the damaged stand. With decreasing relative available soil water (actually available water in relation to water available at the saturation state), the relative leaf water content decreased in damaged, but not in healthy oaks. At Lappwald, similar differences in soil water availability between the healthy and the damaged stand were found, but had no effect on the distribution or biomass of the roots. At the sandy site (Sprakensehl), the available soil water decreased drastically during a dry period, and predawn leaf water potentials of both healthy and damaged oaks declined with decreasing relative available soil water. However, the damaged oaks were not inferior to the healthy ones with respect to root density and biomass. It is concluded that, in the damaged stand of Neuenburg, the high clay content of the subsoil, which results in prolonged periods of waterlogging, in sharp changes from waterlogging to drought and decreased water availability in dry periods, is the reason for the reduced biomass and density of roots of the pedunculate oak. Thus, in northwestern Germany, unfavourable soil water relations are considered as a factor contributing to crown damage of pedunculate oak at hydromorphic sites, but not to damage of sessile oak.     

Morphological and physiological reactions of young deciduous trees (Quercus robur L., Q. petraea [Matt.] Liebl., Fagus sylvatica L.) to waterlogging

One-year-old seedlings of Quercus robur L., Q. petraea (Matt.) Liebl. and Fagus sylvatica L. were cultivated in lysimeters and subjected to waterlogging for 17 weeks, interrupted by a five-week drainage period during summer. The growth of Q. robur was less affected by waterlogging than that of Q. petraea and Fagus. Waterlogging resulted in the formation of adventitious roots in Q. robur and Q. petraea, but not in Fagus. In contrast to Fagus, Q. robur and, to a lesser extent, Q. petraea were able to generate roots even below the water table. The hydraulic conductance of the excised root systems, the stomatal conductance and, in Fagus, the leaf water potential and the leaf-mass related hydraulic conductance were decreased by waterlogging. The decrease in the hydraulic conductance was largest in Fagus, and smallest in Q. robur. The roots of Fagus responded to anaerobic conditions with an increase in ethanol concentration. The measurements of nitrate reductase activities in roots and leaves provided no indications of a persistent contribution of NO₃ ⁻ metabolism to the alleviation of waterlogging-induced stress. It is concluded that Q. robur and, to a lesser extent, Q. petraea can tolerate waterlogging periods better than Fagus due to a different pattern of root formation, and to a better adjustment of leaf biomass production to the hydraulic conductivity of the root system. This revised version was published online in June 2006 with corrections to the Cover Date.     

Pollen dispersal inferred from paternity analysis in a mixed oak stand of Quercus robur L. and Q. petraea (Matt.) Liebl.

Paternity analysis was used to determine the spatial distribution of male parents of 984 offspring collected from 13 identified mother trees in a natural stand of 5.76 ha and comprising 296 adult trees of Quercus petraea and Q . robur . For seven of the 13 maternal progeny arrays sampled, we found an excess of nearby matings and a preferential direction of pollination. For the remaining progeny arrays, no departure from random distribution of male parents was detected. A common trend among all families was a high percentage (averaging 65% for Q. robur and 69% for Q. petraea ) of offspring that were pollinated by male parents from outside the study site. By pooling the data over all families, the average pollen dispersal curve within the stand was inferred and fitted to a negative exponential distribution. This model extrapolated for distances over the spatial scale of the study stand was insufficient to explain the high level of gene flow detected by the paternity analysis, suggesting a substantial level of long-distance pollination events. The genetic composition of the pollen pools received by each maternal tree was compared and showed significant differentiation that could be attributed to differences in male reproductive success. By contrast, no significant differentiation between the pollen clouds from outside and inside the study stand was detected, suggesting genetic homogeneity between the surrounding forest and the study stand.     

The Description of Clones of Quercus robur L. and Q. petraea (Matt.) Liebl. with Microsatellites and AFLP in an Ancient Woodland

Abstract: In densely populated areas autochthonous Quercus robur L. (pedunculate oak) and Q. petraea (Matt.) Liebl. (sessile oak) (Fagaceae) populations have been maintained as ancient devastated woodlands. The continuous cutting, grazing and resprouting of such woodlands has enabled the development of clonal structures. For conservation purposes, an analysis of the actual number, size and spatial distribution of clones is necessary, especially when there is an interest in genetic variation of the population. This study describes for the first time - based on microsatellite and AFLP™ analysis - clones in an autochthonous mixed Q. robur and Q. petraea population that has been coppiced and grazed for several centuries. Based on six microsatellite loci and 69 polymorphic AFLP markers, only 14 unique genotypes were detected in a plot that consisted of 80 trees. Clones were observed for both Q. robur and Q. petraea. The largest clone diameters were observed for Q. robur, with distances up to 5.8 m. The observed clone sizes may indicate the age of the trees.     

Regeneration Patterns of European Oak Species (Quercus petraea (Matt.) Liebl., Quercus robur L.) in Dependence of Environment and Neighborhood

Quercus robur L. (pedunculate oak) and Quercus petraea (Matt.) Liebl. (sessile oak) are two European oak species of great economic and ecological importance. Even though both oaks have wide ecological amplitudes of suitable growing conditions, forests dominated by oaks often fail to regenerate naturally. The regeneration performance of both oak species is assumed to be subject to a variety of variables that interact with one another in complex ways. The novel approach of this research was to study the effect of many ecological variables on the regeneration performance of both oak species together and identify key variables and interactions for different development stages of the oak regeneration on a large scale in the field. For this purpose, overstory and regeneration inventories were conducted in oak dominated forests throughout southern Germany and paired with data on browsing, soil, and light availability. The study was able to verify the assumption that the occurrence of oak regeneration depends on a set of variables and their interactions. Specifically, combinations of site and stand specific variables such as light availability, soil pH and iron content on the one hand, and basal area and species composition of the overstory on the other hand. Also browsing pressure was related to oak abundance. The results also show that the importance of variables and their combinations differs among the development stages of the regeneration. Light availability becomes more important during later development stages, whereas the number of oaks in the overstory is important during early development stages. We conclude that successful natural oak regeneration is more likely to be achieved on sites with lower fertility and requires constantly controlling overstory density. Initially sufficient mature oaks in the overstory should be ensured. In later stages, overstory density should be reduced continuously to meet the increasing light demand of oak seedlings and saplings.     

Small‐scale genetic structure and mating patterns in an extensive sessile oak forest (Quercus petraea (Matt.) Liebl.)

Oaks (Quercus) are major components of temperate forest ecosystems in the Northern Hemisphere where they form intermediate or climax communities. Sessile oak (Quercus petraea) forests represent the climax vegetation in eastern Germany and western Poland. Here, sessile oak forms pure stands or occurs intermixed with Scots Pine (Pinus sylvestris). A large body of research is available on gene flow, reproduction dynamics, and genetic structure in fragmented landscapes and mixed populations. At the same time, our knowledge regarding large, contiguous, and monospecific populations is considerably less well developed. Our study is an attempt to further develop our understanding of the reproduction ecology of sessile oak as an ecologically and economically important forest tree by analyzing mating patterns and genetic structure within adult trees and seedlings originating from one or two reproduction events in an extensive, naturally regenerating sessile oak forest. We detected positive spatial genetic structure up to 30 meters between adult trees and up to 40 meters between seedlings. Seed dispersal distances averaged 8.4 meters. Pollen dispersal distances averaged 22.6 meters. In both cases, the largest proportion of the dispersal occurred over short distances. Dispersal over longer distances was more common for pollen but also appeared regularly for seeds. The reproductive success of individual trees was highly skewed. Only 41 percent of all adult trees produced any offspring while the majority did not participate in reproduction. Among those trees that contributed to the analyzed seedling sample, 80 percent contributed 1–3 gametes. Only 20 percent of all parent trees contributed four or more gametes. However, these relatively few most fertile trees contributed 51 percent of all gametes within the seedling sample. Vitality and growth differed significantly between reproducing and nonreproducing adult trees with reproducing trees being more vital and vigorous than nonreproducing individuals. Our study demonstrates that extensive, apparently homogenous oak forests are far from uniform on the genetic level. On the contrary, they form highly complex mosaics of remarkably small local neighborhoods. This counterbalances the levelling effect of long‐distance dispersal and may increase the species’ adaptive potential. Incorporating these dynamics in the management, conservation, and restoration of oak forests can support the conservation of forest genetic diversity and assist those forests in coping with environmental change.     

Characterisation and natural variation of a dehydrin gene in Quercus petraea (Matt.) Liebl

For the first time in sessile oak [Quercus petraea (Matt.) Liebl.], the isolation and characterisation of a full-length dehydrin gene and its promoter region, as well as its allelic variation in natural populations, is reported. Dehydrins (Dhn) are stress-related genes important for the survival of perennial plants in a seasonal climate. A full-length dehydrin gene (Dhn3) was characterised at the nucleotide level and the protein structure was modelled. Additionally, the allelic variation was analysed in five natural populations of Quercus petraea (Matt.) Liebl. sampled along an altitudinal gradient in the French Pyrenees. The analysed sequences contain typical domains of the K(n) class of dehydrins in the coding region. Also, the 5'untranslated region (promoter) of the gene was amplified, which shows typical motifs essential for drought- and cold-responsive gene expression. Single nucleotide substitutions and indels (insertions/deletions) within the coding region determine large biochemical differences at the protein level. However, only low levels of genetic differentiation between populations from different altitudes were detectable.     

Genetic variation at allozyme and RAPD loci in sessile oak Quercus petraea (Matt.) Liebl.: the role of history and geography

The nuclear genetic variation within and among 21 populations of sessile oak was estimated at 31 RAPD loci in conjunction with previous estimates of variation at eight allozyme loci. The aim of the study was to assess the relative role of isolation-by-distance and postglacial history on patterns of nuclear variation. Because of its small effective population size and maternal transmission, the chloroplast genome is a good marker of population history. Both kinds of nuclear variation (RAPD and allozyme) were therefore compared, first, to the geographical distances among populations and, secondly, to chloroplast DNA restriction polymorphism in the same populations. Multiple Mantel tests were used for this purpose. Although RAPDs revealed less genetic diversity than allozymes, levels of genetic differentiation ( G _ST) were identical. The standard genetic distance calculated at all RAPD loci was correlated with geographical distances but not with the genetic distance calculated from chloroplast DNA data. Conversely, allozyme variation was correlated with chloroplast DNA variation, but not with geography. Possibly, divergent selection at two allozyme loci during the glacial period could explain this pattern. Because of its greater number of loci assayed, RAPDs probably provided a less biased picture of the relative role of geography and history.     

Natural hybridisation between Quercus petraea (Matt.) Liebl. and Quercus pubescens Willd. within an Italian stand as revealed by microsatellite fingerprinting

Interspecific gene flow is frequently reported in the genus Quercus . However, interfertile oak species often seem to remain distinct, even within areas of sympatry. This study employed molecular markers to verify, at a fine scale, the presence of interspecific gene flow in a natural population of Quercus petraea and Quercus pubescens . Within a delimited area of 6 ha, all adult trees belonging to the studied oak complex and seeds from a subsample of such trees were collected and analysed using molecular microsatellite markers. A low interspecific genetic differentiation and a high level of interspecific genetic admixture suggested past hybridisation. Paternity inference of seeds allowed the estimation of pollination frequencies from the three groups of pollen donors ( Q. petraea, Q. pubescens , intermediate). We also assayed pollen viability and germinability of each species group. We observed natural hybridisation between Q. petraea and Q. pubescens, with a predominant component in the direction Q. petraea → Q. pubescens : Q. pubescens displayed a higher level of heterospecific pollination by Q. petraea (25.8%) and intermediate morphotypes (14.7%), compared to Q. petraea acting as pollen receptor (with less than 5% heterospecific pollinations). Intermediate 'mother trees' were pollinated in similar proportions by Q. petraea (23.1%), Q. pubescens (37.8%) and intermediate morphotypes (39.1%). The asymmetrical introgression observed for the studied generation may be caused, among other factors, by the relative abundance of trees from each species group in the studied area.     

The Effect of Bud Position on Branch Growth and Bud Abscission in Quercus petraea (Matt.) Liebl.

The time at which a bud began to expand was related to its positionnot only on an individual shoot but also within the crown. Thedistribution of buds and branches on the shoot was uneven; theshoot tip, where they were densely clustered, was termed the'whorl; and the remainder of the shoot, where they were widelyspaced, the ‘interwhorl’ stem. In spring, the terminalbud started expanding before the ’whorl’ buds whichpreceded the ‘interwhorl’ stem buds; completionof the flush of growth, determined by the end of leaf expansion,occurred in the reverse order, ‘interwhorl’     

Soil N and C trace gas fluxes and microbial soil N turnover in a sessile oak (Quercus petraea (Matt.) Liebl.) forest in Hungary

During two intensive field campaigns in summer and autumn 2004 nitrogen (N₂O, NO/NO₂) and carbon (CO₂, CH₄) trace gas exchange between soil and the atmosphere was measured in a sessile oak (Quercus petraea (Matt.) Liebl.) forest in Hungary. The climate can be described as continental temperate. Fluxes were measured with a fully automatic measuring system allowing for high temporal resolution. Mean N₂O emission rates were 1.5 μg N m⁻² h⁻¹ in summer and 3.4 μg N m⁻² h⁻¹ in autumn, respectively. Also mean NO emission rates were higher in autumn (8.4 μg N m⁻² h⁻¹) as compared to summer (6.0 μg N m⁻² h⁻¹). However, as NO₂ deposition rates continuously exceeded NO emission rates (−9.7 μg N m⁻² h⁻¹ in summer and −18.3 μg N m⁻² h⁻¹ in autumn), the forest soil always acted as a net NO _x sink. The mean value of CO₂ fluxes showed only little seasonal differences between summer (81.1 mg C m⁻² h⁻¹) and autumn (74.2 mg C m⁻² h⁻¹) measurements, likewise CH₄uptake (summer: −52.6 μg C m⁻² h⁻¹; autumn: −56.5 μg C m⁻² h⁻¹). In addition, the microbial soil processes net/gross N mineralization, net/gross nitrification and heterotrophic soil respiration as well as inorganic soil nitrogen concentrations and N₂O/CH₄ soil air concentrations in different soil depths were determined. The respiratory quotient (ΔCO_{2 resp} ΔO_{2 resp}⁻¹) for the uppermost mineral soil, which is needed for the calculation of gross nitrification via the Barometric Process Separation (BaPS) technique, was 0.8978 ± 0.008. The mean value of gross nitrification rates showed only little seasonal differences between summer (0.99 μg N kg⁻¹ SDW d⁻¹) and autumn measurements (0.89 μg N kg⁻¹ SDW d⁻¹). Gross rates of N mineralization were highest in the organic layer (20.1–137.9 μg N kg⁻¹ SDW d⁻¹) and significantly lower in the uppermost mineral layer (1.3–2.9 μg N kg⁻¹ SDW d⁻¹). Only for the organic layer seasonality in gross N mineralization rates could be demonstrated, with highest mean values in autumn, most likely caused by fresh litter decomposition. Gross mineralization rates of the organic layer were positively correlated with N₂O emissions and negatively correlated with CH₄ uptake, whereas soil CO₂ emissions were positively correlated with heterotrophic respiration in the uppermost mineral soil layer. The most important abiotic factor influencing C and N trace gas fluxes was soil moisture, while the influence of soil temperature on trace gas exchange rates was high only in autumn.     

The Effect of Bud Position on Branch Growth and Bud Abscission in Quercus petraea (Matt.) Liebl.

The time at which a bud began to expand was related to its positionnot only on an individual shoot but also within the crown. Thedistribution of buds and branches on the shoot was uneven; theshoot tip, where they were densely clustered, was termed the‘whorl; and the remainder of the shoot, where they werewidely spaced, the ‘interwhorl’ stem. In spring,the terminal bud started expanding before the ‘whorl’buds which preceded the ‘interwhorl’ stem buds;completion of the flush of growth, determined by the end ofleaf expansion, occurred in the reverse order, ‘interwhorl’> ‘whorl’ > terminal. Similarly bud expansionstarted at the top of the crown and progressed downwards, andthe first shoots to complete their flush were at the bottomof the crown. Approximately 60% of the buds on each shoot beganexpanding in spring but only about half of these formed branches.Bud abscission began in May and by Sep. 45% of buds originallypresent had abscised. Most of-the buds that did not abscisewere the small buds at the base of the shoot that were not originallyassociated with a leaf. Approximately 42% of ‘whorl’buds and 28% of MnterwhorP stem buds formed branches. ‘Whorl’branches were approx. 60% longer that ‘interwhorl’stem branches; buds on the lower surface of the shoot producedlonger branches than those on the upper surface. The implicationsof the results for the development of crown form and selectionof superior oak are discussed. Quercus petraea, oak, buds, branches, crown form     

Gene flow and hybridisation in a mixed oak forest (Quercus pyrenaica Willd. and Quercus petraea (Matts.) Liebl.) in central Spain

Oaks are long-standing models for the study of gene flow and hybridisation. Temperate (Quercus petraea) and sub-Mediterranean (Quercus pyrenaica) oaks coexist in central Spain, showing remarkable differences in population size and structure. Q. petraea has a scattered distribution in central Spain, where it is at one of the southernmost limits of its range, and forms low-density stands; in contrast, Q. pyrenaica is widespread in the region. We selected a mixed population of the two species ( approximately 13 ha, 176 adults and 96 saplings) to compare the patterns of gene flow within each species and the extent of introgression between them. Using five nuclear microsatellite markers, we performed a parentage analysis and found considerable immigration from outside the stand ( approximately 38% for Q. petraea and approximately 34% for Q. pyrenaica), and estimated average seed-dispersal distances of 42 and 14 m for Q. petraea and Q. pyrenaica, respectively. Introgression between species was also estimated using our microsatellite battery. First, we developed a multivariate discriminant approach and, second, we compared our results with a widely used clustering method (STRUCTURE). Both analyses were consistent with a low level of introgression between Q. petraea and Q. pyrenaica. Indeed, only 15 adult trees, approximately 8.5%, were identified as putative hybrids when both methods of analysis were combined. Hybrids may be most common in contact zones due merely to physical proximity.     

Long-term radial growth and climate-growth relationships of Quercus petraea (Matt.) Liebl. and Quercus cerris L. in a xeric low elevation site from Hungary

Sessile oak (Quercus petraea [Matt.] Liebl.) and Turkey oak (Quercus cerris L.) dominated mixed forests are common in low montane and hilly regions in Hungary. Here, we aimed to describe the long-term pattern and climatic responses of the radial growth of Q. petraea and Q. cerris in a xeric low-elevation forest, using retrospective tree-ring analysis for the period 1910–2019. We performed separate analyses with time series of full tree-ring (TRW), earlywood (EW) and latewood (LW) widths. Our results showed that the radial growth of the two species was largely synchronous over time, but became transiently divergent for a 20-year period after a drought in 1968, due to the greater-than-expected growth of Q. cerris and the supressed growth of Q. petraea. Precipitation was the major growth-limiting factor for both species, with a strong positive influence on LW particularly during the current early growing season (March-June), on EW in the previous late summer (August-September) and in the current early spring (March), and on all tree-ring traits in the previous December. The radial growth of both species was negatively related to temperature in the spring (May) and late summer (August) of both current and previous years. The climate-growth relationships showed general instability over time: the most striking temporal change was a gradual shift of positive correlations with precipitation and SPEI during the growing season from spring (March-May) to summer (June-August) since the 1980s over the analysed period. The two species had similarly low growth resistance to droughts in four studied pointer years (1968, 1993, 2002 and 2012), but Q. cerris exhibited a greater capacity to recover over the four post-drought years, and thus higher growth resilience, particularly after the drought of 1968. Our results contribute to the better understanding of the role of climate variability and droughts in the growth of the two co-existing species in transitional locations between closed forests and forest-steppes.     

Dendroclimatic regions of pedunculate oak (Quercus robur L.) in Belarus

In this study, we present the boundaries of five dendrochronologically homogeneous regions of pedunculate oak (Quercus robur L.) and the master chronologies for them for the period 1703–2018 based on 27 tree-ring chronologies from different locations around Belarus. The average length of the master chronologies ranges from 70 to 310 years. Our research shows that the radial increment of a pedunculate oak in Belarus is primarily limited by the previous year’s August-September temperature, by the current year’s May temperature and by June precipitation. Oak growth in northern Belarus is mostly limited by air temperature, whereas precipitation plays more significant role in central and southern parts of the country. The most unfavorable years for oak growth in Belarus were 1940 and 1952, both of which were years when a very frosty winter was followed by a droughty summer. The results provide an important achievement in Belarusian dendrochronology, since they represent a significant breakthrough for Eastern Europe, where there is a considerable lack of dendroclimatic researches of broadleaved species.