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1.  Morphological and physiological divergences within Quercus ilex support the existence of different ecotypes depending on climatic dryness 
Annals of Botany  2014;114(2):301-313.
Background and Aims
Several studies show apparently contradictory findings about the functional convergence within the Mediterranean woody flora. In this context, this study evaluates the variability of functional traits within holm oak (Quercus ilex) to elucidate whether provenances corresponding to different morphotypes represent different ecotypes locally adapted to the prevaling stress levels.
Several morphological and physiological traits were measured at leaf and shoot levels in 9-year-old seedlings of seven Q. ilex provenances including all recognized morphotypes. Plants were grown in a common garden for 9 years under the same environmental conditions to avoid possible biases due to site-specific characteristics.
Key Results
Leaf morphometry clearly separates holm oak provenances into ‘ilex’ (more elongated leaves with low vein density) and ‘rotundifolia’ (short and rounded leaves with high vein density) morphotypes. Moreover, these morphotypes represent two consistent and very contrasting functional types in response to dry climates, mainly in terms of leaf area, major vein density, leaf specific conductivity, resistance to drought-induced cavitation and turgor loss point.
The ‘ilex’ and ‘rotundifolia’ morphotypes correspond to different ecotypes as inferred from their contrasting functional traits. To the best of our knowledge, this is the first time that the combined use of morphological and physiological traits has provided support for the concept of these two holm oak morphotypes being regarded as two different species.
PMCID: PMC4111378  PMID: 24941998
Mediterranean vegetation; Quercus ilex; holm oak; ‘ilex’ morphotype; ‘rotundifolia’ morphotype; functional traits; palaeobotany; ecotype
2.  Selenium addition alters mercury uptake, bioavailability in the rhizosphere and root anatomy of rice (Oryza sativa) 
Annals of Botany  2014;114(2):271-278.
Background and Aims
Mercury (Hg) is an extremely toxic pollutant, especially in the form of methylmercury (MeHg), whereas selenium (Se) is an essential trace element in the human diet. This study aimed to ascertain whether addition of Se can produce rice with enriched Se and lowered Hg content when growing in Hg-contaminated paddy fields and, if so, to determine the possible mechanisms behind these effects.
Two cultivars of rice (Oryza sativa, japonica and indica) were grown in either hydroponic solutions or soil rhizobags with different Se and Hg treatments. Concentrations of total Hg, MeHg and Se were determined in the roots, shoots and brown rice, together with Hg uptake kinetics and Hg bioavailability in the soil. Root anatonmy was also studied.
Key Results
The high Se treatment (5 μg g–1) significantly increased brown rice yield by 48 % and total Se content by 2·8-fold, and decreased total Hg and MeHg by 47 and 55 %, respectively, compared with the control treatments. The high Se treatment also markedly reduced ‘water-soluble’ Hg and MeHg concentrations in the rhizosphere soil, decreased the uptake capacity of Hg by roots and enhanced the development of apoplastic barriers in the root endodermis.
Addition of Se to Hg-contaminated soil can help produce brown rice that is simultaneously enriched in Se and contains less total Hg and MeHg. The lowered accumulation of total Hg and MeHg appears to be the result of reduced bioavailability of Hg and production of MeHg in the rhizosphere, suppression of uptake of Hg into the root cells and an enhancement of the development of apoplastic barriers in the endodermis of the roots.
PMCID: PMC4111379  PMID: 24948669
Apoplastic barriers; mercury pollution; Hg bioavailability; methylmercury; Oryza sativa; rice; root endodermis; selenium; Se addition; uptake process
3.  Spatial genetic structure reflects extensive clonality, low genotypic diversity and habitat fragmentation in Grevillea renwickiana (Proteaceae), a rare, sterile shrub from south-eastern Australia 
Annals of Botany  2014;114(2):413-423.
Background and Aims
The association of clonality, polyploidy and reduced fecundity has been identified as an extinction risk for clonal plants. Compromised sexual reproduction limits both their ability to adapt to new conditions and their capacity to disperse to more favourable environments. Grevillea renwickiana is a prostrate, putatively sterile shrub reliant on asexual reproduction. Dispersal is most likely limited by the rate of clonal expansion via rhizomes. The nine localized populations constituting this species provide an opportunity to examine the extent of clonality and spatial genotypic diversity to evaluate its evolutionary prospects.
Ten microsatellite loci were used to compare genetic and genotypic diversity across all sites with more intensive sampling at four locations (n = 185). The spatial distribution of genotypes and chloroplast DNA haplotypes based on the trnQ–rps16 intergenic spacer region were compared. Chromosome counts provided a basis for examining genetic profiles inconsistent with diploidy.
Key Results
Microsatellite analysis identified 46 multilocus genotypes (MLGs) in eight multilocus clonal lineages (MLLs). MLLs are not shared among sites, with two exceptions. Spatial autocorrelation was significant to 1·6 km. Genotypic richness ranged from 0 to 0·33. Somatic mutation is likely to contribute to minor variation between MLGs within clonal lineages. The eight chloroplast haplotypes identified were correlated with eight MLLs defined by ordination and generally restricted to single populations. Triploidy is the most likely reason for tri-allelic patterns.
Grevillea renwickiana comprises few genetic individuals. Sterility has most likely been induced by triploidy. Extensive lateral suckering in long-lived sterile clones facilitates the accumulation of somatic mutations, which contribute to the measured genetic diversity. Genetic conservation value may not be a function of population size. Despite facing evolutionary stagnation, sterile clonal species can play a vital role in mitigating ecological instability as floras respond to rapid environmental change.
PMCID: PMC4111381  PMID: 24737718
Climate change; clonality; clonal plant ecology; chloroplast haplotype; genet; Grevillea renwickiana; multilocus lineage; Proteaceae; ramet; somatic mutation; spatial distribution; triploidy
4.  Incomplete sequence homogenization in 45S rDNA multigene families: intermixed IGS heterogeneity within the single NOR locus of the polyploid species Medicago arborea (Fabaceae) 
Annals of Botany  2014;114(2):243-251.
Background and Aims
Ribosomal sequences have become the classical example of the genomic homogenization of nuclear multigene families. Despite theoretical advantages and modelling predictions that support concerted evolution of the 45S rDNA, several reports have found intragenomic polymorphisms. However, the origins and causes of these rDNA polymorphisms are difficult to assess because seed plants show a wide range of 45S rDNA loci number variation, especially in polyploids. Medicago arborea is a tetraploid species that has a single 45S rDNA locus. This feature makes this species a suitable case study to assess the fate of ribosomal IGS homogenization in polyploid species showing nucleolus organizer region (NOR) reduction.
The intergenic spacer (IGS) region was amplified by long PCR and the fragments were cloned and sequenced by a primer-walking strategy. The physical mapping of the whole and partial IGS variants was assessed by fluorescent in situ hybridization (FISH) and fibre-FISH methods on mitotic chromosomes and extended DNA fibres, respectively.
Key Results
Two IGS fragments of 4·8 and 3·5 kb were obtained showing structural features of functional sequences. The shorter variant appears to be a truncated copy of the 4·8 kb fragment that lacks the duplication of the transcription initiation site region and the entire D region. The physical localization of the two IGS variants on metaphase chromosomes and extended DNA fibres using FISH corroborated their joint presence within the same locus. In addition, no spatial structure of the two variants was detected within the NOR.
The results suggest that full sequence homogenization is not operating within the NOR locus of M. arborea. The structure of the NOR locus reported here departs from the models of IGS heterogeneity present in plants and caution against assuming the widespread belief that intragenomic ribosomal heterogeneity is mainly due to sequence variation between paralogous loci.
PMCID: PMC4111382  PMID: 24925322
45S rDNA; nuclear ribosomal cistron; intragenomic variation; intergenic spacer; IGS; transcription initiation site; fibre-FISH; polyploidy; Medicago arborea; Fabaceae
5.  Light limitation and litter of an invasive clonal plant, Wedelia trilobata, inhibit its seedling recruitment 
Annals of Botany  2014;114(2):425-433.
Background and Aims
Invasive clonal plants have two reproduction patterns, namely sexual and vegetative propagation. However, seedling recruitment of invasive clonal plants can decline as the invasion process proceeds. For example, although the invasive clonal Wedelia trilobata (Asteraceae) produces numerous seeds, few seedlings emerge under its dense population canopy in the field. In this study it is hypothesized that light limitation and the presence of a thick layer of its own litter may be the primary factors causing the failure of seedling recruitment for this invasive weed in the field.
A field survey was conducted to determine the allocation of resources to sexual reproduction and seedling recruitment in W. trilobata. Seed germination was also determined in the field. Effects of light and W. trilobata leaf extracts on seed germination and seedling growth were tested in the laboratory.
Key Results
Wedelia trilobata blooms profusely and produces copious viable seeds in the field. However, seedlings of W. trilobata were not detected under mother ramets and few emerged seedlings were found in the bare ground near to populations. In laboratory experiments, low light significantly inhibited seed germination. Leaf extracts also decreased seed germination and inhibited seedling growth, and significant interactions were found between low light and leaf extracts on seed germination. However, seeds were found to germinate in an invaded field after removal of the W. trilobata plant canopy.
The results indicate that lack of light and the presence of its own litter might be two major factors responsible for the low numbers of W. trilobata seedlings found in the field. New populations will establish from seeds once the limiting factors are eliminated, and seeds can be the agents of long-distance dispersal; therefore, prevention of seed production remains an important component in controlling the spread of this invasive clonal plant.
PMCID: PMC4111383  PMID: 24825293
Clonal plant ecology; leaf litter; biological invasion; invasive plant; light limitation; reproductive strategy; seedling recruitment inhibition; Wedelia trilobata; Asteraceae
6.  Salinity-mediated cyanogenesis in white clover (Trifolium repens) affects trophic interactions 
Annals of Botany  2014;114(2):357-366.
Background and Aims
Increasing soil salinity poses a major plant stress in agro-ecosystems worldwide. Surprisingly little is known about the quantitative effect of elevated salinity on secondary metabolism in many agricultural crops. Such salt-mediated changes in defence-associated compounds may significantly alter the quality of food and forage plants as well as their resistance against pests. In the present study, the effects of soil salinity on cyanogenesis in white clover (Trifolium repens), a forage crop of international importance, are analysed.
Experimental clonal plants were exposed to five levels of soil salinity, and cyanogenic potential (HCNp, total amount of accumulated cyanide in a given plant tissue), β-glucosidase activity, soluble protein concentration and biomass production were quantified. The attractiveness of plant material grown under the different salt treatments was tested using cafeteria-style feeding trials with a generalist (grey garden slug, Deroceras reticulatum) and a specialist (clover leaf weevil, Hypera punctata) herbivore.
Key Results
Salt treatment resulted in an upregulation of HCNp, whereas β-glucosidase activity and soluble protein concentration showed no significant variation among treatments. Leaf area consumption of both herbivore species was negatively correlated with HCNp, indicating bottom-up effects of salinity-mediated changes in HCNp on plant consumers.
The results suggest that soil salinity leads to an upregulation of cyanogenesis in white clover, which results in enhanced resistance against two different natural herbivores. The potential implications for such salinity-mediated changes in plant defence for livestock grazing remain to be tested.
PMCID: PMC4111384  PMID: 25006176
Bottom-up effects; β-glucosidase; cyanide; cyanogenesis; cyanogenic glucoside; HCNp; herbivore; forage crop; secondary metabolite; Trifolium repens; trophic interactions; white clover
7.  Physiological integration modifies δ15N in the clonal plant Fragaria vesca, suggesting preferential transport of nitrogen to water-stressed offspring 
Annals of Botany  2014;114(2):399-411.
Background and Aims
One of the most striking attributes of clonal plants is their capacity for physiological integration, which enables movement of essential resources between connected ramets. This study investigated the capacity of physiological integration to buffer differences in resource availability experienced by ramets of the clonal wild strawberry plant, Fragaria vesca. Specifically, a study was made of the responses of connected and severed offspring ramets growing in environments with different water availability conditions (well watered or water stressed) and nitrogen forms (nitrate or ammonium).
The experimental design consisted of three factors, ‘integration’ (connected, severed) ‘water status’ (well watered, water stressed) and ‘nitrogen form’ (nitrate, ammonium), applied in a pot experiment. The effects of physiological integration were studied by analysing photochemical efficiency, leaf spectral reflectance, photosynthesis and carbon and nitrogen isotope discrimination, the last of which has been neglected in previous studies.
Key Results
Physiological integration buffered the stress caused by water deprivation. As a consequence, survival was improved in water-stressed offspring ramets that remained connected to their parent plants. The nitrogen isotope composition (δ15N) values in the connected water-stressed ramets were similar to those in ramets in the ammonium treatment; however, δ15N values in connected well-watered ramets were similar to those in the nitrate treatment. The results also demonstrated the benefit of integration for offspring ramets in terms of photochemical activity and photosynthesis.
This is the first study in which carbon and nitrogen isotopic discrimination has been used to detect physiological integration in clonal plants. The results for nitrogen isotope composition represent the first evidence of preferential transport of a specific form of nitrogen to compensate for stressful conditions experienced by a member clone. Water consumption was lower in plants supplied with ammonium than in plants supplied with nitrate, and therefore preferential transport of ammonium from parents to water-stressed offspring could potentially optimize the water use of the whole clone.
PMCID: PMC4111385  PMID: 24769538
Clonal plant ecology; clonal integration; environmental heterogeneity; Fragaria vesca; wild strawberry; isotope discrimination; nitrogen forms; photosynthesis; water-use efficiency
8.  Relative growth rate variation of evergreen and deciduous savanna tree species is driven by different traits 
Annals of Botany  2014;114(2):315-324.
Background and Aims
Plant relative growth rate (RGR) depends on biomass allocation to leaves (leaf mass fraction, LMF), efficient construction of leaf surface area (specific leaf area, SLA) and biomass growth per unit leaf area (net assimilation rate, NAR). Functional groups of species may differ in any of these traits, potentially resulting in (1) differences in mean RGR of groups, and (2) differences in the traits driving RGR variation within each group. We tested these predictions by comparing deciduous and evergreen savanna trees.
RGR, changes to biomass allocation and leaf morphology, and root non-structural carbohydrate reserves were evaluated for juveniles of 51 savanna species (34 deciduous, 17 evergreen) grown in a common garden experiment. It was anticipated that drivers of RGR would differ between leaf habit groups because deciduous species have to allocate carbohydrates to storage in roots to be able to flush leaves again, which directly compromises their LMF, whereas evergreen species are not subject to this constraint.
Key Results
Evergreen species had greater LMF and RGR than deciduous species. Among deciduous species LMF explained 27 % of RGR variation (SLA 34 % and NAR 29 %), whereas among evergreen species LMF explained between 2 and 17 % of RGR variation (SLA 32–35 % and NAR 38–62 %). RGR and LMF were (negatively) related to carbohydrate storage only among deciduous species.
Trade-offs between investment in carbohydrate reserves and growth occurred only among deciduous species, leading to differences in relative contribution made by the underlying components of RGR between the leaf habit groups. The results suggest that differences in drivers of RGR occur among savanna species because these have different selected strategies for coping with fire disturbance in savannas. It is expected that variation in the drivers of RGR will be found in other functional types that respond differently to particular disturbances.
PMCID: PMC4111386  PMID: 24958787
Carbohydrate storage; deciduous; ecological traits; evergreen; functional types; plant growth variation; relative growth rate; RGR; savanna trees
9.  Ecological consequences of plant clonality 
Annals of Botany  2014;114(2):367.
PMCID: PMC4111387  PMID: 25057149
10.  Clonal growth and plant species abundance 
Annals of Botany  2014;114(2):377-388.
Background and Aims
Both regional and local plant abundances are driven by species' dispersal capacities and their abilities to exploit new habitats and persist there. These processes are affected by clonal growth, which is difficult to evaluate and compare across large numbers of species. This study assessed the influence of clonal reproduction on local and regional abundances of a large set of species and compared the predictive power of morphologically defined traits of clonal growth with data on actual clonal growth from a botanical garden. The role of clonal growth was compared with the effects of seed reproduction, habitat requirements and growth, proxied both by LHS (leaf–height–seed) traits and by actual performance in the botanical garden.
Morphological parameters of clonal growth, actual clonal reproduction in the garden and LHS traits (leaf-specific area – height – seed mass) were used as predictors of species abundance, both regional (number of species records in the Czech Republic) and local (mean species cover in vegetation records) for 836 perennial herbaceous species. Species differences in habitat requirements were accounted for by classifying the dataset by habitat type and also by using Ellenberg indicator values as covariates.
Key Results
After habitat differences were accounted for, clonal growth parameters explained an important part of variation in species abundance, both at regional and at local levels. At both levels, both greater vegetative growth in cultivation and greater lateral expansion trait values were correlated with higher abundance. Seed reproduction had weaker effects, being positive at the regional level and negative at the local level.
Morphologically defined traits are predictive of species abundance, and it is concluded that simultaneous investigation of several such traits can help develop hypotheses on specific processes (e.g. avoidance of self-competition, support of offspring) potentially underlying clonal growth effects on abundance. Garden performance parameters provide a practical approach to assessing the roles of clonal growth morphological traits (and LHS traits) for large sets of species.
PMCID: PMC4111395  PMID: 24482153
Clonal plant growth; species abundance; botanical garden collections; LHS traits; leaf-specific area; plant height; seed mass; lateral expansion; seed reproduction; Ellenberg indicator values
11.  Variable response of three Trifolium repens ecotypes to soil flooding by seawater 
Annals of Botany  2014;114(2):347-355.
Background and Aims
Despite concerns about the impact of rising sea levels and storm surge events on coastal ecosystems, there is remarkably little information on the response of terrestrial coastal plant species to seawater inundation. The aim of this study was to elucidate responses of a glycophyte (white clover, Trifolium repens) to short-duration soil flooding by seawater and recovery following leaching of salts.
Using plants cultivated from parent ecotypes collected from a natural soil salinity gradient, the impact of short-duration seawater soil flooding (8 or 24 h) on short-term changes in leaf salt ion and organic solute concentrations was examined, together with longer term impacts on plant growth (stolon elongation) and flowering.
Key Results
There was substantial Cl– and Na+ accumulation in leaves, especially for plants subjected to 24 h soil flooding with seawater, but no consistent variation linked to parent plant provenance. Proline and sucrose concentrations also increased in plants following seawater flooding of the soil. Plant growth and flowering were reduced by longer soil immersion times (seawater flooding followed by drainage and freshwater inputs), but plants originating from more saline soil responded less negatively than those from lower salinity soil.
The accumulation of proline and sucrose indicates a potential for solute accumulation as a response to the osmotic imbalance caused by salt ions, while variation in growth and flowering responses between ecotypes points to a natural adaptive capacity for tolerance of short-duration seawater soil flooding in T. repens. Consequently, it is suggested that selection for tolerant ecotypes is possible should the predicted increase in frequency of storm surge flooding events occur.
PMCID: PMC4111396  PMID: 24942000
Climate change; flooding; glycophyte; osmotic stress; salinity; saline soil waterlogging; salt ions; sea level rise; stress metabolites; storm surge; Trifolium repens; white clover
12.  Drought tolerance and plasticity in the invasive knapweed Centaurea stoebe s.l. (Asteraceae): effect of populations stronger than those of cytotype and range 
Annals of Botany  2014;114(2):289-299.
Background and Aims
Spotted knapweed (Centaurea stoebe s.l., Asteraceae) is native to Europe, where it occurs as a diploid (2xEU) and tetraploid cytotype (4xEU), but so far only the tetraploid has been reported in the introduced range in North America (4xNA). In previous studies, significant range shifts have been found towards drier climates in 4xEU compared with 2xEU, and in 4xNA when compared with the native range. In addition, 4x plants showed thicker leaves and reduced specific leaf area compared with 2x plants, suggesting higher drought tolerance in 4x plants. It is thus hypothesized that the 4x cytotype might be better pre-adapted to drought than the 2x, and the 4xNA better adapted than the 4xEU due to post-introduction selection.
Plants of the three geocytotypes (2xEU, 4xEU and 4xNA ), each represented by six populations, were subjected to three water treatments over 6 weeks in a greenhouse experiment. Plasticity and reaction norms of above- and below-ground biomasses and their ratio, survival rate, stomatal conductance and carbon isotope discrimination were analysed using linear and generalized linear mixed effect models.
Key Results and Conclusions
Above-ground and total biomasses of European tetraploids were slightly less affected by drought than those of European diploids, and 4xEU plants maintained higher levels of stomatal conductance under moderate drought than 4xNA plants, thus supporting the pre-adaptation but not the post-introduction evolution hypothesis. Plasticity indexes for most of the traits were generally higher in 2xEU and 4xNA than in 4xEU plants, but these differences were not or were only marginally significant. Interestingly, the effect of population origin and its interaction with treatment was more important than the effects of geocytotype and range. Population means for the control treatment showed several significant associations either with latitude or some aspect of climatic data, suggesting evolution of local adaptations, especially within the 2xEU and 4xEU geocytotypes.
PMCID: PMC4111397  PMID: 24918204
Biological invasions; biomass partitioning; carbon isotope discrimination; Centaurea stoebe; drought tolerance; local adaptations; plasticity; polyploidy; spotted knapweed; water use efficiency
13.  Holoparasitic Rafflesiaceae possess the most reduced endophytes and yet give rise to the world's largest flowers 
Annals of Botany  2014;114(2):233-242.
Background and Aims
Species in the holoparasitic plant family Rafflesiaceae exhibit one of the most highly modified vegetative bodies in flowering plants. Apart from the flower shoot and associated bracts, the parasite is a mycelium-like endophyte living inside their grapevine hosts. This study provides a comprehensive treatment of the endophytic vegetative body for all three genera of Rafflesiaceae (Rafflesia, Rhizanthes and Sapria), and reports on the cytology and development of the endophyte, including its structural connection to the host, shedding light on the poorly understood nature of this symbiosis.
Serial sectioning and staining with non-specific dyes, periodic–Schiff's reagent and aniline blue were employed in order to characterize the structure of the endophyte across a phylogenetically diverse sampling.
Key Results
A previously identified difference in the nuclear size between Rafflesiaceae endophytes and their hosts was used to investigate the morphology and development of the endophytic body. The endophytes generally comprise uniseriate filaments oriented radially within the host root. The emergence of the parasite from the host during floral development is arrested in some cases by an apparent host response, but otherwise vegetative growth does not appear to elicit suppression by the host.
Rafflesiaceae produce greatly reduced and modified vegetative bodies even when compared with the other holoparasitic angiosperms once grouped with Rafflesiaceae, which possess some vegetative differentiation. Based on previous studies of seeds together with these findings, it is concluded that the endophyte probably develops directly from a proembryo, and not from an embryo proper. Similarly, the flowering shoot arises directly from the undifferentiated endophyte. These filaments produce a protocorm in which a shoot apex originates endogenously by formation of a secondary morphological surface. This degree of modification to the vegetative body is exceptional within angiosperms and warrants additional investigation. Furthermore, the study highlights a mechanical isolation mechanism by which the host may defend itself from the parasite.
PMCID: PMC4111398  PMID: 24942001
Comparative morphology; endophyte; gigantism; holoparasitism; host–parasite relationship; heterochrony; proembryo; Rafflesiaceae; Rafflesia; Rhizanthes; Sapria; Tetrastigma
14.  Changes in tracheid and ray traits in fire scars of North American conifers and their ecophysiological implications 
Annals of Botany  2014;114(2):223-232.
Background and Aims
Fire scars have been widely used as proxies for the reconstruction of fire history; however, little is known about the impact of fire injury on wood anatomy. This study investigates changes in tracheid and ray traits in fire scars of Douglas fir (Pseudotsuga menziesii), western larch (Larix occidentalis) and ponderosa pine (Pinus ponderosa), and discusses their ecophysiological implications for tree recovery from fire.
Transverse and tangential microsections were prepared for light microscopy and image analysis. Measurements of tracheids and rays were made in the three spatial dimensions: axially (at different section heights), radially (in different rings) and tangentially (with increasing distance from the wound margin).
Key Results
Changes were strongest in the first year after fire injury, with a decrease in tracheid size (by 25–30 %) and an increase in tracheid density (by 21–53 %) for the three species. In addition, an increase in ray size (by 5–27 %) and an increase in ray density (by 19–36 %) were found in P. menziesii and L. occidentalis. Changes were comparable along the fire-injured stem and were often most marked close to the fire scar.
The differentiation after fire injury of narrower and more numerous tracheids expresses a trade-off between hydraulic safety and hydraulic efficiency, while that of larger and more numerous rays serves compartmentalization and wound closure, mechanical strength and defence responses. Pinus ponderosa does not generally produce more ray tissue after fire injury and thus appears to be more adapted to fire.
PMCID: PMC4111399  PMID: 24941999
Ecophysiology; conifer; fire scar; Larix occidentalis; western larch; Pinus ponderosa; ponderosa pine; Pseudotsuga menziesii; Douglas fir; ray; tracheid; wood anatomy
15.  Patch size and distance: modelling habitat structure from the perspective of clonal growth 
Annals of Botany  2014;114(2):389-398.
Background and Aims
This study considers the spatial structure of patchy habitats from the perspective of plants that forage for resources by clonal growth. Modelling is used in order to compare two basic strategies, which differ in the response of the plant to a patch boundary. The ‘avoiding plant’ (A) never grows out of a good (resource-rich) patch into a bad (resource-poor) region, because the parent ramet withdraws its subsidy from the offspring. The ‘entering plant’ (E) always crosses the boundary, as the offspring is subsidized at the expense of the parent. In addition to these two extreme scenarios, an intermediate mixed strategy (M) will also be tested. The model is used to compare the efficiency of foraging in various habitats in which the proportion of resource-rich areas (p) is varied.
A stochastic cellular automata (CA) model is developed in which habitat space is represented by a honeycomb lattice. Each cell within the lattice can accommodate a single ramet, and colonization can occur from a parent ramet's cell into six neighbouring cells. The CA consists of two layers: the population layer and the habitat. In the population layer, a cell can be empty or occupied by a ramet; in the habitat layer, a cell can be good (resource-rich) or bad (resource-poor). The habitat layer is constant; the population layer changes over time, according to the birth and death of ramets.
Key Results
Strategies M and E are primarily limited by patch distance, whereas A is more sensitive to patch size. At a critical threshold of the proportion of resource-rich areas, p = 0·5, the mean patch size increases abruptly. Below the threshold, E is more efficient than A, whilst above the threshold the opposite is true. The mixed strategy (M) is more efficient than either of the pure strategies across a broad range of p values.
The model predicts more species/genotypes with the ‘entering’ strategy, E, in habitats where resource-rich patches are scattered, and more plants with the ‘avoiding’ strategy, A, in habitats where the connectivity of resource-rich patches is high. The results suggest that the degree of physiological integration between a parent and an offspring ramet is important even across a very short distance because it can strongly influence the efficiency of foraging.
PMCID: PMC4217637  PMID: 24942002
Clonal plant ecology; ramet; genet; phenotypic plasticity; physiological integration; foraging; population dynamics; modelling; cellular automata; percolation theory; habitat connectivity; patchy environment
16.  Stomatal and pavement cell density linked to leaf internal CO2 concentration 
Annals of Botany  2014;114(2):191-202.
Background and Aims
Stomatal density (SD) generally decreases with rising atmospheric CO2 concentration, Ca. However, SD is also affected by light, air humidity and drought, all under systemic signalling from older leaves. This makes our understanding of how Ca controls SD incomplete. This study tested the hypotheses that SD is affected by the internal CO2 concentration of the leaf, Ci, rather than Ca, and that cotyledons, as the first plant assimilation organs, lack the systemic signal.
Sunflower (Helianthus annuus), beech (Fagus sylvatica), arabidopsis (Arabidopsis thaliana) and garden cress (Lepidium sativum) were grown under contrasting environmental conditions that affected Ci while Ca was kept constant. The SD, pavement cell density (PCD) and stomatal index (SI) responses to Ci in cotyledons and the first leaves of garden cress were compared. 13C abundance (δ13C) in leaf dry matter was used to estimate the effective Ci during leaf development. The SD was estimated from leaf imprints.
Key Results
SD correlated negatively with Ci in leaves of all four species and under three different treatments (irradiance, abscisic acid and osmotic stress). PCD in arabidopsis and garden cress responded similarly, so that SI was largely unaffected. However, SD and PCD of cotyledons were insensitive to Ci, indicating an essential role for systemic signalling.
It is proposed that Ci or a Ci-linked factor plays an important role in modulating SD and PCD during epidermis development and leaf expansion. The absence of a Ci–SD relationship in the cotyledons of garden cress indicates the key role of lower-insertion CO2 assimilation organs in signal perception and its long-distance transport.
PMCID: PMC4217638  PMID: 24825295
Stomatal density; stomata development; pavement cells; cotyledons; leaf internal CO2; 13C discrimination; Lepidium sativum; Helianthus annuus; Fagus sylvatica; Arabidopsis thaliana
17.  Modelling the mechanical behaviour of pit membranes in bordered pits with respect to cavitation resistance in angiosperms 
Annals of Botany  2014;114(2):325-334.
Background and Aims
Various correlations have been identified between anatomical features of bordered pits in angiosperm xylem and vulnerability to cavitation, suggesting that the mechanical behaviour of the pits may play a role. Theoretical modelling of the membrane behaviour has been undertaken, but it requires input of parameters at the nanoscale level. However, to date, no experimental data have indicated clearly that pit membranes experience strain at high levels during cavitation events.
Transmission electron microscopy (TEM) was used in order to quantify the pit micromorphology of four tree species that show contrasting differences in vulnerability to cavitation, namely Sorbus aria, Carpinus betulus, Fagus sylvatica and Populus tremula. This allowed anatomical characters to be included in a mechanical model that was based on the Kirchhoff–Love thin plate theory. A mechanistic model was developed that included the geometric features of the pits that could be measured, with the purpose of evaluating the pit membrane strain that results from a pressure difference being applied across the membrane. This approach allowed an assessment to be made of the impact of the geometry of a pit on its mechanical behaviour, and provided an estimate of the impact on air-seeding resistance.
Key Results
The TEM observations showed evidence of residual strains on the pit membranes, thus demonstrating that this membrane may experience a large degree of strain during cavitation. The mechanical modelling revealed the interspecific variability of the strains experienced by the pit membrane, which varied according to the pit geometry and the pressure experienced. The modelling output combined with the TEM observations suggests that cavitation occurs after the pit membrane has been deflected against the pit border. Interspecific variability of the strains experienced was correlated with vulnerability to cavitation. Assuming that air-seeding occurs at a given pit membrane strain, the pressure predicted by the model to achieve this mechanical state corresponds to experimental values of cavitation sensitivity (P50).
The results provide a functional understanding of the importance of pit geometry and pit membrane structure in air-seeding, and thus in vulnerability to cavitation.
PMCID: PMC4111388  PMID: 24918205
Tree; wood; air-seeding; cavitation resistance; embolism; bordered pit membrane; mechanical modelling; strain; xylem anatomy; Fagus sylvatica; beech; Sorbus aria; whitebeam; Populus tremula; poplar; Carpinus betulus; hornbeam
18.  Impact of warming and drought on carbon balance related to wood formation in black spruce 
Annals of Botany  2014;114(2):335-345.
Background and Aims
Wood formation in trees represents a carbon sink that can be modified in the case of stress. The way carbon metabolism constrains growth during stress periods (high temperature and water deficit) is now under debate. In this study, the amounts of non-structural carbohydrates (NSCs) for xylogenesis in black spruce, Picea mariana, saplings were assessed under high temperature and drought in order to determine the role of sugar mobilization for osmotic purposes and its consequences for secondary growth.
Four-year-old saplings of black spruce in a greenhouse were subjected to different thermal conditions with respect to the outside air temperature (T0) in 2010 (2 and 5 °C higher than T0) and 2011 (6 °C warmer than T0 during the day or night) with a dry period of about 1 month in June of each year. Wood formation together with starch, NSCs and leaf parameters (water potential and photosynthesis) were monitored from May to September.
Key Results
With the exception of raffinose, the amounts of soluble sugars were not modified in the cambium even if gas exchange and photosynthesis were greatly reduced during drought. Raffinose increased more than pinitol under a pre-dawn water potential of less than –1 Mpa, presumably because this compound is better suited than polyol for replacing water and capturing free radicals, and its degradation into simple sugar is easier. Warming decreased the starch storage in the xylem as well the available hexose pool in the cambium and the xylem, probably because of an increase in respiration.
Radial stem growth was reduced during drought due to the mobilization of NSCs for osmotic purposes and due to the lack of cell turgor. Thus plant water status during wood formation can influence the NSCs available for growth in the cambium and xylem.
PMCID: PMC4111389  PMID: 24950772
Cambium; black spruce; Picea mariana; drought; non-structural carbohydrate; soluble sugars; raffinose; starch; global warming; climate change; wood formation; xylogenesis
19.  Aerial and soil seed banks enable populations of an annual species to cope with an unpredictable dune ecosystem 
Annals of Botany  2014;114(2):279-287.
Background and Aims
Simultaneous formation of aerial and soil seed banks by a species provides a mechanism for population maintenance in unpredictable environments. Eolian activity greatly affects growth and regeneration of plants in a sand dune system, but we know little about the difference in the contributions of these two seed banks to population dynamics in sand dunes.
Seed release, germination, seedling emergence and survival of a desert annual, Agriophyllum squarrosum (Chenopodiaceae), inhabiting the Ordos Sandland in China, were determined in order to explore the different functions of the aerial and soil seed banks.
Key Results
The size of the aerial seed bank was higher than that of the soil seed bank throughout the growing season. Seed release was positively related to wind velocity. Compared with the soil seed bank, seed germination from the aerial seed bank was lower at low temperature (5/15 °C night/day) but higher in the light. Seedling emergence from the soil seed bank was earlier than that from the aerial seed bank. Early-emerged (15 April–15 May) seedlings died due to frost, but seedlings that emerged during the following months survived to reproduce successfully.
The timing of seed release and different germination behaviour resulted in a temporal heterogeneity of seedling emergence and establishment between the two seed banks. The study suggests that a bet-hedging strategy for the two seed banks enables A. squarrosum populations to cope successfully with the unpredictable desert environment.
PMCID: PMC4111390  PMID: 24918206
Aerial seed bank; soil seed bank; Agriophyllum squarrosum; Chenopodiaceae; seed germination; seedling establishment; fitness; sand dune ecology
20.  Cucurbits depicted in Byzantine mosaics from Israel, 350–600 ce 
Annals of Botany  2014;114(2):203-222.
Background and Aims
Thousands of floor mosaics were produced in lands across the Roman and Byzantine empires. Some mosaics contain depictions of agricultural produce, potentially providing useful information concerning the contemporary presence and popularity of crop plants in a particular geographical region. Hundreds of floor mosaics produced in Israel during the Byzantine period have survived. The objective of the present work was to search these mosaics for Cucurbitaceae in order to obtain a more complete picture of cucurbit crop history in the eastern Mediterranean region.
Results and Conclusions
Twenty-three mosaics dating from 350–600 ce were found that had images positively identifiable as cucurbits. The morphological diversity of the cucurbit fruits in the mosaics of Israel is greater than that appearing in mosaics from any other Roman or Byzantine provincial area. The depicted fruits vary in shape from oblate to extremely long, and some are furrowed, others are striped and others lack definite markings. The cucurbit taxa depicted in the mosaics are Cucumis melo (melon), Citrullus lanatus (watermelon), Luffa aegyptiaca (sponge gourd) and Lagenaria siceraria (bottle gourd). Cucumis melo is the most frequently found taxon in the mosaics and is represented by round dessert melons and long snake melons. Fruits of at least two cultivars of snake melons and of watermelons are represented. To our knowledge, images of sponge gourds have not been found in Roman and Byzantine mosaics elsewhere. Indeed, the mosaics of Israel contain what are probably the oldest depictions of Luffa aegyptiaca in Mediterranean lands. Sponge gourds are depicted often, in 11 of the mosaics at eight localities, and the images include both mature fruits, which are useful for cleaning and washing, and immature fruits, which are edible. Only one mosaic has images positively identifiable as of bottle gourds, and these were round–pyriform and probably used as vessels.
PMCID: PMC4111391  PMID: 24948671
Byzantine mosaics; crop archaeology; crop history; crop domestication; Citrullus lanatus; Cucumis melo; cucurbit history; Cucurbitaceae; Lagenaria siceraria; Luffa aegyptiaca; Luffa cylindrica; snake melon; sponge gourd
21.  Plant Cuttings 
Annals of Botany  2014;114(2):iv-vii.
PMCID: PMC4111392
22.  ContentSnapshots 
Annals of Botany  2014;114(2):i-iv.
PMCID: PMC4111393
23.  Reticulate evolution in North American black-fruited hawthorns (Crataegus section Douglasia; Rosaceae): evidence from nuclear ITS2 and plastid sequences 
Annals of Botany  2014;114(2):253-269.
Background and Aims
The taxonomic complexity of Crataegus (hawthorn; Rosaceae, Maleae), especially in North America, has been attributed by some to hybridization in combination with gametophytic apomixis and polyploidization, whereas others have considered the roles of hybridization and apomixis to be minimal. Study of the chemical composition and therapeutic value of hawthorn extracts requires reproducible differentiation of entities that may be difficult to distinguish by morphology alone. This study sought to address this by using the nuclear ribosomal spacer region ITS2 as a supplementary DNA barcode; however, a lack of success prompted an investigation to discover why this locus gave unsatisfactory results.
ITS2 was extensively cloned so as to document inter- and intraindividual variation in this locus, using hawthorns of western North America where the genus Crataegus is represented by only two widely divergent groups, the red-fruited section Coccineae and the black-fruited section Douglasia. Additional sequence data from selected loci on the plastid genome were obtained to enhance further the interpretation of the ITS2 results.
Key Results
In the ITS2 gene tree, ribotypes from western North American hawthorns are found in two clades. Ribotypes from diploid members of section Douglasia occur in one clade (with representatives of the east-Asian section Sanguineae). The other clade comprises those from diploid and polyploid members of section Coccineae. Both clades contribute ribotypes to polyploid Douglasia. Data from four plastid-derived intergenic spacers demonstrate the maternal parentage of these allopolyploids.
Repeated hybridization between species of section Douglasia and western North American members of section Coccineae involving the fertilization of unreduced female gametes explains the observed distribution of ribotypes and accounts for the phenetic intermediacy of many members of section Douglasia.
PMCID: PMC4111394  PMID: 24984714
Reticulate evolution; nrITS; cpDNA; Crataegus; Douglasia; Coccineae; Rosaceae; hawthorn; gametophytic apomixis; allopolyploid; autopolyploid; concerted evolution; hybrids; taxonomy
24.  Plant functional types in Earth system models: past experiences and future directions for application of dynamic vegetation models in high-latitude ecosystems 
Annals of Botany  2014;114(1):1-16.
Earth system models describe the physical, chemical and biological processes that govern our global climate. While it is difficult to single out one component as being more important than another in these sophisticated models, terrestrial vegetation is a critical player in the biogeochemical and biophysical dynamics of the Earth system. There is much debate, however, as to how plant diversity and function should be represented in these models.
Plant functional types (PFTs) have been adopted by modellers to represent broad groupings of plant species that share similar characteristics (e.g. growth form) and roles (e.g. photosynthetic pathway) in ecosystem function. In this review, the PFT concept is traced from its origin in the early 1800s to its current use in regional and global dynamic vegetation models (DVMs). Special attention is given to the representation and parameterization of PFTs and to validation and benchmarking of predicted patterns of vegetation distribution in high-latitude ecosystems. These ecosystems are sensitive to changing climate and thus provide a useful test case for model-based simulations of past, current and future distribution of vegetation.
Models that incorporate the PFT concept predict many of the emerging patterns of vegetation change in tundra and boreal forests, given known processes of tree mortality, treeline migration and shrub expansion. However, representation of above- and especially below-ground traits for specific PFTs continues to be problematic. Potential solutions include developing trait databases and replacing fixed parameters for PFTs with formulations based on trait co-variance and empirical trait–environment relationships. Surprisingly, despite being important to land–atmosphere interactions of carbon, water and energy, PFTs such as moss and lichen are largely absent from DVMs. Close collaboration among those involved in modelling with the disciplines of taxonomy, biogeography, ecology and remote sensing will be required if we are to overcome these and other shortcomings.
PMCID: PMC4071098  PMID: 24793697
Plant functional types; PFT; Earth system model; ESM; Arctic tundra; biogeography; dynamic vegetation models; global change; plant traits; high-latitude ecosystem
25.  Why Africa matters: evolution of Old World Salvia (Lamiaceae) in Africa 
Annals of Botany  2014;114(1):61-83.
Background and Aims
Salvia is the largest genus in Lamiaceae and it has recently been found to be non-monophyletic. Molecular data on Old World Salvia are largely lacking. In this study, we present data concerning Salvia in Africa. The focus is on the colonization of the continent, character evolution and the switch of pollination systems in the genus.
Maximum likelihood and Bayesian inference were used for phylogenetic reconstruction. Analyses were based on two nuclear markers [internal transcribed spacer (ITS) and external transcribed spacer (ETS)] and one plastid marker (rpl32-trnL). Sequence data were generated for 41 of the 62 African taxa (66 %). Mesquite was used to reconstruct ancestral character states for distribution, life form, calyx shape, stamen type and pollination syndrome.
Key Results
Salvia in Africa is non-monophyletic. Each of the five major regions in Africa, except Madagascar, was colonized at least twice, and floristic links between North African, south-west Asian and European species are strongly supported. The large radiation in Sub-Saharan Africa (23 species) can be traced back to dispersal from North Africa via East Africa to the Cape Region. Adaptation to bird pollination in southern Africa and Madagascar reflects parallel evolution.
The phenotypic diversity in African Salvia is associated with repeated introductions to the continent. Many important evolutionary processes, such as colonization, adaptation, parallelism and character transformation, are reflected in this comparatively small group. The data presented in this study can help to understand the evolution of Salvia sensu lato and other large genera.
PMCID: PMC4071099  PMID: 24966353
Salvia; Lamiaceae; Canary Islands; character evolution; ITS; ETS; Madagascar; ornithophily; pollination; rpl32-trnL; Sub-Saharan Africa

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