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1.  Pollinator convergence and the nature of species' boundaries in sympatric Sardinian Ophrys (Orchidaceae) 
Annals of Botany  2008;104(3):497-506.
Background and Aims
In the sexually deceptive Ophrys genus, species isolation is generally considered ethological and occurs via different, specific pollinators, but there are cases in which Ophrys species can share a common pollinator and differ in pollen placement on the body of the insect. In that condition, species are expected to be reproductively isolated through a pre-mating mechanical barrier. Here, the relative contribution of pre- vs. post-mating barriers to gene flow among two Ophrys species that share a common pollinator and can occur in sympatry is studied.
Methods
A natural hybrid zone on Sardinia between O. iricolor and O. incubacea, sharing Andrena morio as pollinator, was investigated by analysing floral traits involved in pollinator attraction as odour extracts both for non-active and active compounds and for labellum morphology. The genetic architecture of the hybrid zone was also estimated with amplified fragment length polymorphism (AFLP) markers, and pollination fitness and seed set of both parental species and their hybrids in the sympatric zone were estimated by controlled crosses.
Key Results
Although hybrids were intermediate between parental species in labellum morphology and non-active odour compounds, both parental species and hybrids produced a similar odour bouquet for active compounds. However, hybrids produced significantly lower fruit and seed set than parental species, and the genetic architecture of the hybrid zone suggests that they were mostly first-generation hybrids.
Conclusions
The two parental species hybridize in sympatry as a consequence of pollinator overlap and weak mechanical isolation, but post-zygotic barriers reduce hybrid frequency and fitness, and prevent extensive introgression. These results highlight a significant contribution of late post-mating barriers, such as chromosomal divergence, for maintaining reproductive isolation, in an orchid group for which pre-mating barriers are often considered predominant.
doi:10.1093/aob/mcn219
PMCID: PMC2720645  PMID: 19001428
AFLP markers; floral scent variation; hybrid zone; hybrid fitness; Ophrys iricolor; Ophrys incubacea; reproductive isolation; sexual deception
2.  Ecology and genetic diversity of the dense-flowered orchid, Neotinea maculata, at the centre and edge of its range 
Annals of Botany  2008;104(3):507-516.
Background and Aims
Species may occur over a wide geographical range within which populations can display large variation in reproductive success and genetic diversity. Neotinea maculata is a rare orchid of conservation concern at the edge of its range in Ireland, where it occurs in small populations. However, it is relatively common throughout the Mediterranean region. Here, factors that affect rarity of N. maculata in Ireland are investigated by comparing Irish populations with those found in Italy, where it is more common.
Methods
Vegetation communities, breeding system and genetic diversity were compared using three amplified fragment length polymorphism (AFLP) primer pairs in populations in Ireland and Italy. Vegetation was quantified using quadrats taken along transects in study populations, and hand pollination experiments were performed to assess reliance of N. maculata on pollinators in both Irish and Italian populations.
Key Results
Neotinea maculata occupies different vegetation communities in Italian and Irish populations. Breeding system experiments show that N. maculata is 100 % autogamous, and there are no differences in fruit and seed production in selfed, outcrossed and unmanipulated plants. AFLP markers revealed that Irish and Italian populations have similar genetic diversity and are distinct from each other.
Conclusions
Neotinea maculata does not suffer any negative effects of autogamous reproduction; it self-pollinates and sets seed readily in the absence of pollinators. It occupies a variety of habitats in both Ireland and Italy; however, Irish populations are small and rare and should be conserved. This could be due to climatic factors and the absence of suitable soil mycorrhizas to allow recruitment from seed.
doi:10.1093/aob/mcn200
PMCID: PMC2720646  PMID: 18940852
Neotinea maculata; AFLP; autogamy; conservation; genetic diversity; Lusitanian species; pollination
3.  Oeceoclades maculata, an alien tropical orchid in a Caribbean rainforest 
Annals of Botany  2008;104(3):557-563.
Background and Aims
Undisturbed forest habitat can be relatively impenetrable to invasive, non-native species. Orchids are not commonly regarded as invasive, but some species have become invasive and these generally depend on habitat disturbance. One of the most aggressive orchids is Oeceoclades maculata, a terrestrial species with remarkable ecological amplitude. Originally from tropical Africa, it is now widespread in the neotropics. By associating its local distribution with land-use history and habitat characteristics, it was determined whether O. maculata is dependent on habitat disturbance. It was also investigated whether this exotic orchid occupies the same habitat space as two sympatric native species.
Methods
Six 10 m × 500 m transects were censused in June 2007 on the 16-ha Luquillo Forest Dynamics Plot, located in the Luquillo Mountains, Puerto Rico. The plot had been mapped for historical land use, topography and soil type.
Key Results
Oeceoclades maculata was the most abundant of three orchid species surveyed and was found in all four historical cover classes. In cover class 3 (50–80 % forest cover in 1936), 192 of 343 plants were found at a density of 0·48 plants per 5 × 5 m subplot. Over 93 % of the 1200 subplots surveyed were composed of Zarzal or Cristal soil types, and O. maculata was nearly evenly distributed in both. The orchid was most common on relatively flat terrain. The distribution and abundance of two sympatric orchid species were negatively associated with that of the invasive species.
Conclusions
Oeceoclades maculata does penetrate ‘old growth’ forest but is most abundant in areas with moderate levels of past disturbance. Soil type makes little difference, but slope of terrain can be important. The negative association between O. maculata and native species may reflect differences in habitat requirements or a negative interaction perhaps at the mycorrhizal level.
doi:10.1093/aob/mcn191
PMCID: PMC2720658  PMID: 18840872
Oeceoclades maculata; Wullschlaegelia calcarata; Prescottia stachyodes; Orchidaceae; land-use history; tropical forest disturbance; terrestrial orchids; invasive species; Luquillo Experimental Forest; Puerto Rico; forest recovery; Caribbean
4.  Reproductive biology of Acrolophia cochlearis (Orchidaceae): estimating rates of cross-pollination in epidendroid orchids 
Annals of Botany  2008;104(3):573-581.
Background and Aims
Pollen fates strongly influence mating success in plants but are difficult to quantify. By promoting foraging constancy in pollinators, floral rewards such as nectar may enhance the overall efficiency of pollen transfer. However, this can also lead to high levels of geitonogamy. Pollen fates were studied in Acrolophia cochlearis, a member of a terrestrial epidendroid orchid genus that includes both rewarding and deceptive species.
Methods
Pollinator observations were conducted. Pollen transfer efficiency (PTE), the proportion of removed pollinia deposited on stigmas, was measured in a large population at regular intervals throughout the 5-month flowering season. The level of cross-pollination in two populations was estimated from the percentage of seeds with embryos in naturally pollinated fruits.
Key Results
Acrolophia cochlearis (and a congener A. micrantha) produce minute but concentrated nectar rewards. Observations showed that A. cochlearis is pollinated exclusively by a solitary bee species, Colletes claripes. Although both sexes visited flowers, only males carried pollinaria. Overall levels of pollination and PTE of the rewarding A. cochlearis were much higher than in a deceptive congener, A. capensis. Seeds resulting from self-fertilization had a significantly lower probability of containing viable embryos than did those from cross-fertilization. This dichotomy in fruit quality was used to estimate that cross-pollination occurred in approx. 66 % of A. cochlearis flowers in a large dense population and approx. 10 % in a small sparse population. Traits of A. cochlearis that limit geitonogamy include pollinarium reconfiguration that exceeds the visit time of pollinators and rapid flower senescence following visitation.
Conclusions
Presence of a nectar reward in Acrolophia cochlearis results in high levels of PTE. It is estimated that approx. 33–90 % of fruits in natural populations arise from self-pollination in this species.
doi:10.1093/aob/mcn218
PMCID: PMC2720661  PMID: 19001427
Reward; deception; pollen transfer efficiency; pollen tracking; geitonogamy; Acrolophia cochlearis; epidendroid orchid; Cape floral region
5.  A key role for floral scent in a wasp-pollination system in Eucomis (Hyacinthaceae) 
Annals of Botany  2008;103(5):715-725.
Background and Aims
Floral scent may play a key role as a selective attractant in plants with specialized pollination systems, particularly in cases where floral morphology does not function as a filter of flower visitors. The pollination systems of two African Eucomis species (E. autumnalis and E. comosa) were investigated and a test was made of the importance of scent and visual cues as floral attractants.
Methods and Key Results
Visitor observations showed that E. autumnalis and E. comosa are visited primarily by pompilid wasps belonging to the genus Hemipepsis. These wasps carry considerably more Eucomis pollen and are more active on flowers than other visiting insects. Furthermore, experiments involving virgin flowers showed that these insects are capable of depositing pollen on the stigmas of E. autumnalis, and, in the case of E. comosa, pollen deposited during a single visit is sufficient to result in seed set. Experimental hand-pollinations showed that both species are genetically self-incompatible and thus reliant on pollinators for seed set. Choice experiments conducted in the field and laboratory with E. autumnalis demonstrated that pompilid wasps are attracted to flowers primarily by scent and not visual cues. Measurement of spectral reflectance by flower petals showed that flowers are cryptically coloured and are similar to the background vegetation. Analysis of headspace scent samples using coupled gas chromatography–mass spectrometry revealed that E. autumnalis and E. comosa scents are dominated by aromatic and monoterpene compounds. One hundred and four volatile compounds were identified in the floral scent of E. autumnalis and 83 in the floral scent of E. comosa, of which 57 were common to the scents of both species.
Conclusions
This study showed that E. autumnalis and E. comosa are specialized for pollination by pompilid wasps in the genus Hemipepsis and achieve specialization through cryptic colouring and the use of scent as a selective floral attractant.
doi:10.1093/aob/mcn261
PMCID: PMC2707869  PMID: 19116433
Eucomis; Pompilidae; wasp pollination; breeding system; pollination syndrome; pollinator shift; floral volatile; floral filter
6.  Rapid loss of genetic variation in a founding population of Primula elatior (Primulaceae) after colonization 
Annals of Botany  2008;103(5):777-783.
Background and Aims
Land-use changes and associated extinction/colonization dynamics can have a large impact on population genetic diversity of plant species. The aim of this study was to investigate genetic diversity in a founding population of the self-incompatible forest herb Primula elatior and to elucidate the processes that affect genetic diversity shortly after colonization.
Methods
AFLP markers were used to analyse genetic diversity across three age classes and spatial genetic structure within a founding population of P. elatior in a recently established stand in central Belgium. Parentage analyses were used to assess the amount of gene flow from outside the population and to investigate the contribution of mother plants to future generations.
Results
The genetic diversity of second and third generation plants was significantly reduced compared with that of first generation plants. Significant spatial genetic structure was observed. Parentage analyses showed that <20 % of the youngest individuals originated from parents outside the study population and that >50 % of first and second generation plants did not contribute to seedling recruitment.
Conclusions
These results suggest that a small effective population size and genetic drift can lead to rapid decline of genetic diversity of offspring in founding populations shortly after colonization. This multigenerational study also highlights that considerable amounts of gene flow seem to be required to counterbalance genetic drift and to sustain high levels of genetic diversity after colonization in recently established stands.
doi:10.1093/aob/mcn253
PMCID: PMC2707865  PMID: 19106180
AFLP; colonization; forest regeneration; genetic diversity; genetic drift; parentage analysis; spatial genetic structure
7.  Adaptive phenotypic plasticity of Pseudoroegneria spicata: response of stomatal density, leaf area and biomass to changes in water supply and increased temperature 
Annals of Botany  2008;103(5):769-775.
Background and Aims
Changes in rainfall and temperature brought about through climate change may affect plant species distribution and community composition of grasslands. The primary objective of this study was to test how manipulation of water and temperature would influence the plasticity of stomatal density and leaf area of bluebunch wheatgrass, Pseudoroegneria spicata. It was hypothesized that: (1) an increased water supply will increase biomass and leaf area and decrease stomatal density, while a reduced water supply will cause the opposite effect; (2) an increase in temperature will reduce biomass and leaf area and increase stomatal density; and (3) the combinations of water and temperature treatments can be aligned along a stress gradient and that stomatal density will be highest at high stress.
Methods
The three water supply treatments were (1) ambient, (2) increased approx. 30 % more than ambient through weekly watering and (3) decreased approx. 30 % less than ambient by rain shades. The two temperature treatments were (1) ambient and (2) increased approx. 1–3 °C by using open-top chambers. At the end of the second experimental growing season, above-ground biomass was harvested, oven-dried and weighed, tillers from bluebunch wheatgrass plants sampled, and the abaxial stomatal density and leaf area of tillers were measured.
Key Results
The first hypothesis was partially supported – reducing water supply increased stomatal density, but increasing water supply reduced leaf area. The second hypothesis was rejected. Finally, the third hypothesis could not be fully supported – rather than a linear response there appears to be a parabolic stomatal density response to stress.
Conclusions
Overall, the abaxial stomatal density and leaf area of bluebunch wheatgrass were plastic in their response to water and temperature manipulations. Although bluebunch wheatgrass has the potential to adapt to changing climate, the grass is limited in its ability to respond to a combination of reduced water and increased temperature.
doi:10.1093/aob/mcn252
PMCID: PMC2707864  PMID: 19088084
Bluebunch wheatgrass; Pseudoroegneria spicata; biomass; climate change; grassland; open top chamber; rain shade; stomata
8.  Correlations between leaf toughness and phenolics among species in contrasting environments of Australia and New Caledonia 
Annals of Botany  2008;103(5):757-767.
Background and Aims
Plants are likely to invest in multiple defences, given the variety of sources of biotic and abiotic damage to which they are exposed. However, little is known about syndromes of defence across plant species and how these differ in contrasting environments. Here an investigation is made into the association between carbon-based chemical and mechanical defences, predicting that species that invest heavily in mechanical defence of leaves will invest less in chemical defence.
Methods
A combination of published and unpublished data is used to test whether species with tougher leaves have lower concentrations of phenolics, using 125 species from four regions of Australia and the Pacific island of New Caledonia, in evergreen vegetation ranging from temperate shrubland and woodland to tropical shrubland and rainforest. Foliar toughness was measured as work-to-shear and specific work-to-shear (work-to-shear per unit leaf thickness). Phenolics were measured as ‘total phenolics’ and by protein precipitation (an estimate of tannin activity) per leaf dry mass.
Key Results
Contrary to prediction, phenolic concentrations were not negatively correlated with either measure of leaf toughness when examined across all species, within regions or within any plant community. Instead, measures of toughness (particularly work-to-shear) and phenolics were often positively correlated in shrubland and rainforest (but not dry forest) in New Caledonia, with a similar trend suggested for shrubland in south-western Australia. The common feature of these sites was low concentrations of soil nutrients, with evidence of P limitation.
Conclusions
Positive correlations between toughness and phenolics in vegetation on infertile soils suggest that additive investment in carbon-based mechanical and chemical defences is advantageous and cost-effective in these nutrient-deficient environments where carbohydrate may be in surplus.
doi:10.1093/aob/mcn246
PMCID: PMC2707862  PMID: 19098067
Antiherbivore defence; leaf toughness; mechanical defence; chemical defence; phenolics; trade-offs
9.  Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses 
Annals of Botany  2008;103(4):609-623.
Background
Environmental conditions, such as water supply, temperature and salinity, strongly affect plant growth and development. Extremes of these conditions (abiotic stresses) adversely affect many different mechanisms associated with plant responses and adaptation to stress: photosynthetic mechanisms, e.g. stomatal control of CO2 diffusion, photosystem II repair, ribulose bisphosphate carboxylase/oxygenase (Rubisco) activity and scavenging of reactive oxygen species (ROS), are susceptible to damage, and photosynthetic efficiency can be greatly decreased. Responses and adaptations require differential gene expression, which is regulated by specific transcription factors (TFs).
Scope
The role and regulation of several TFs involved in abiotic stress response pathways are considered, with emphasis on new findings regarding expression of genes related to both stomatal and non-stomatal limitations to CO2 photosynthetic assimilation.
Conclusions
Many TFs, belonging to different families (e.g. MYB, bZIP and DREB), have been related to abiotic stress responses; however, only a few are known to regulate the expression of photosynthesis-related genes in response to stress. Several TFs belonging to the MYB family play an important role in both stomatal and non-stomatal responses by regulation of stomatal numbers and sizes, and metabolic components, respectively. To obtain more insight into this area of potentially large agronomic impact, it is essential to identify and functionally characterize new TFs that mediate the stress responses regulating the expression of genes associated with photosynthesis and related metabolism.
doi:10.1093/aob/mcn227
PMCID: PMC2707349  PMID: 19010801
Transcription factors; photosynthesis; stomata; abiotic stress; abiotic stress signalling; cold; drought; salt; ABA; MYB; AP2/EREBP
10.  Transfer of genetic material between the chloroplast and nucleus: how is it related to stress in plants? 
Annals of Botany  2008;103(4):625-633.
Background
The presence of chloroplast-related DNA sequences in the nuclear genome is generally regarded as a relic of the process by which genes have been transferred from the chloroplast to the nucleus. The remaining chloroplast encoded genes are not identical across the plant kingdom indicating an ongoing transfer of genes from the organelle to the nucleus.
Scope
This review focuses on the active processes by which the nuclear genome might be acquiring or removing DNA sequences from the chloroplast genome. Present knowledge of the contribution to the nuclear genome of DNA originating from the chloroplast will be reviewed. In particular, the possible effects of stressful environments on the transfer of genetic material between the chloroplast and nucleus will be considered. The significance of this research and suggestions for the future research directions to identify drivers, such as stress, of the nuclear incorporation of plastid sequences are discussed.
Conclusions
The transfer to the nuclear genome of most of the protein-encoding functions for chloroplast-located proteins facilitates the control of gene expression. The continual transfer of fragments, including complete functional genes, from the chloroplast to the nucleus has been observed. However, the mechanisms by which the loss of functions and physical DNA elimination from the chloroplast genome following the transfer of those functions to the nucleus remains obscure. The frequency of polymorphism across chloroplast-related DNA fragments within a species will indicate the rate at which these DNA fragments are incorporated and removed from the chromosomes.
doi:10.1093/aob/mcn173
PMCID: PMC2707348  PMID: 18801916
Stress; DNA transfer; organelles and nucleus; genome integration
11.  Crassulacean acid metabolism and fitness under water deficit stress: if not for carbon gain, what is facultative CAM good for? 
Annals of Botany  2008;103(4):645-653.
Background
In obligate Crassulacean acid metabolism (CAM), up to 99 % of CO2 assimilation occurs during the night, therefore supporting the hypothesis that CAM is adaptive because it allows CO2 fixation during the part of the day with lower evaporative demand, making life in water-limited environments possible. By comparison, in facultative CAM (inducible CAM, C3-CAM) and CAM-cycling plants drought-induced dark CO2 fixation may only be, with few exceptions, a small proportion of C3 CO2 assimilation in watered plants and occur during a few days. From the viewpoint of survival the adaptive advantages, i.e. increased fitness, of facultative CAM and CAM-cycling are not obvious. Therefore, it is hypothesized that, if it is to increase fitness, CAM must aid in reproduction.
Scope
An examination of published reports of 23 facultative CAM and CAM-cycling species finds that, in 19 species, drought-induced dark CO2 fixation represents on average 11 % of C3 CO2 assimilation of watered plants. Evidence is discussed on the impact of the operation of CAM in facultative and CAM-cycling plants on their survival – carbon balance, water conservation, water absorption, photo-protection of the photosynthetic apparatus – and reproductive effort. It is concluded that in some species, but not all, facultative and cycling CAM contribute, rather than to increase carbon balance, to increase water-use efficiency, water absorption, prevention of photoinhibition and reproductive output.
doi:10.1093/aob/mcn145
PMCID: PMC2707347  PMID: 18708641
Facultative CAM; CAM-cycling; water; crassulacean acid metabolism; deficit
12.  Indirect suppression of photosynthesis on individual leaves by arthropod herbivory 
Annals of Botany  2008;103(4):655-663.
Background
Herbivory reduces leaf area, disrupts the function of leaves, and ultimately alters yield and productivity. Herbivore damage to foliage typically is assessed in the field by measuring the amount of leaf tissue removed and disrupted. This approach assumes the remaining tissues are unaltered, and plant photosynthesis and water balance function normally. However, recent application of thermal and fluorescent imaging technologies revealed that alterations to photosynthesis and transpiration propagate into remaining undamaged leaf tissue.
Scope and Conclusions
This review briefly examines the indirect effects of herbivory on photosynthesis, measured by gas exchange or chlorophyll fluorescence, and identifies four mechanisms contributing to the indirect suppression of photosynthesis in remaining leaf tissues: severed vasculature, altered sink demand, defence-induced autotoxicity, and defence-induced down-regulation of photosynthesis. We review the chlorophyll fluorescence and thermal imaging techniques used to gather layers of spatial data and discuss methods for compiling these layers to achieve greater insight into mechanisms contributing to the indirect suppression of photosynthesis. We also elaborate on a few herbivore-induced gene-regulating mechanisms which modulate photosynthesis and discuss the difficult nature of measuring spatial heterogeneity when combining fluorescence imaging and gas exchange technology. Although few studies have characterized herbivore-induced indirect effects on photosynthesis at the leaf level, an emerging literature suggests that the loss of photosynthetic capacity following herbivory may be greater than direct loss of photosynthetic tissues. Depending on the damage guild, ignoring the indirect suppression of photosynthesis by arthropods and other organisms may lead to an underestimate of their physiological and ecological impacts.
doi:10.1093/aob/mcn127
PMCID: PMC2707346  PMID: 18660492
Chlorophyll fluorescence imaging; thermography; plant–insect interactions; spatial patterns; autotoxicity; induced defences; jasmonates
13.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell 
Annals of Botany  2008;103(4):551-560.
Background
Plants are often subjected to periods of soil and atmospheric water deficits during their life cycle as well as, in many areas of the globe, to high soil salinity. Understanding how plants respond to drought, salt and co-occurring stresses can play a major role in stabilizing crop performance under drought and saline conditions and in the protection of natural vegetation. Photosynthesis, together with cell growth, is among the primary processes to be affected by water or salt stress.
Scope
The effects of drought and salt stresses on photosynthesis are either direct (as the diffusion limitations through the stomata and the mesophyll and the alterations in photosynthetic metabolism) or secondary, such as the oxidative stress arising from the superimposition of multiple stresses. The carbon balance of a plant during a period of salt/water stress and recovery may depend as much on the velocity and degree of photosynthetic recovery, as it depends on the degree and velocity of photosynthesis decline during water depletion. Current knowledge about physiological limitations to photosynthetic recovery after different intensities of water and salt stress is still scarce. From the large amount of data available on transcript-profiling studies in plants subjected to drought and salt it is becoming apparent that plants perceive and respond to these stresses by quickly altering gene expression in parallel with physiological and biochemical alterations; this occurs even under mild to moderate stress conditions. From a recent comprehensive study that compared salt and drought stress it is apparent that both stresses led to down-regulation of some photosynthetic genes, with most of the changes being small (ratio threshold lower than 1) possibly reflecting the mild stress imposed. When compared with drought, salt stress affected more genes and more intensely, possibly reflecting the combined effects of dehydration and osmotic stress in salt-stressed plants.
doi:10.1093/aob/mcn125
PMCID: PMC2707345  PMID: 18662937
Photosynthesis; stress; drought; salt; stomatal; mesophyll and biochemical limitations; gene expression; signalling
14.  The crucial role of plant mitochondria in orchestrating drought tolerance 
Annals of Botany  2008;103(4):581-597.
Background
Around the world, the frequency and intensity of droughts is increasing as a result of global climate change, with important consequences for the growth and survival of agricultural and native plant species. Understanding how plants respond to water stress is thus crucial for predicting the impacts of climate change on the crop productivity and ecosystem functioning. In contrast to the large number of studies assessing drought impacts on photosynthesis, relatively little attention has been devoted to understanding how mitochondrial respiratory metabolism is altered under water stress conditions.
Scope
This review provides an overview of the impacts of water stress on mitochondrial respiration (R), combining studies at the whole-plant, individual organ, cellular and organelle levels. To establish whether there are clear patterns in the response of in vivo R to water stress, a wide range of root, leaf and whole-plant studies are reviewed. It is shown that water stress almost always inhibits R in actively growing roots and whole plants. However, in fully expanded, mature leaves the response is more variable, with water stress reducing R in near two-thirds of reported studies, with most of the remainder showing no change. Only a few studies reported increases in leaf R under severe water stress conditions. The mechanisms responsible for these variable responses are discussed. Importantly, the fact is highlighted that irrespective of whether drought increases or decreases respiration, overall the changes in R are minor compared with the large decreases in photosynthetic carbon gain in response to drought. Based on recent work highlighting the link between chloroplast and mitochondrial functions in leaves, we propose a model by which mitochondrial R enables survival and rapid recovery of productivity under water stress conditions. Finally, the effects of water stress on mitochondrial function, protein abundance and overall metabolism are reviewed.
doi:10.1093/aob/mcn094
PMCID: PMC2707344  PMID: 18552366
Respiration; photosynthesis; water stress; drought; desiccation tolerance; mitochondria; chloroplast; metabolic shuttle; alternative pathway; organelle cross-talk; oxidative stress; photorespiration
15.  C4 photosynthesis and water stress 
Annals of Botany  2008;103(4):635-644.
Background
In contrast to C3 photosynthesis, the response of C4 photosynthesis to water stress has been less-well studied in spite of the significant contribution of C4 plants to the global carbon budget and food security. The key feature of C4 photosynthesis is the operation of a CO2-concentrating mechanism in the leaves, which serves to saturate photosynthesis and suppress photorespiration in normal air. This article reviews the current state of understanding about the response of C4 photosynthesis to water stress, including the interaction with elevated CO2 concentration. Major gaps in our knowledge in this area are identified and further required research is suggested.
Scope
Evidence indicates that C4 photosynthesis is highly sensitive to water stress. With declining leaf water status, CO2 assimilation rate and stomatal conductance decrease rapidly and photosynthesis goes through three successive phases. The initial, mainly stomatal phase, may or may not be detected as a decline in assimilation rates depending on environmental conditions. This is because the CO2-concentrating mechanism is capable of saturating C4 photosynthesis under relatively low intercellular CO2 concentrations. In addition, photorespired CO2 is likely to be refixed before escaping the bundle sheath. This is followed by a mixed stomatal and non-stomatal phase and, finally, a mainly non-stomatal phase. The main non-stomatal factors include reduced activity of photosynthetic enzymes; inhibition of nitrate assimilation, induction of early senescence, and changes to the leaf anatomy and ultrastructure. Results from the literature about CO2 enrichment indicate that when C4 plants experience drought in their natural environment, elevated CO2 concentration alleviates the effect of water stress on plant productivity indirectly via improved soil moisture and plant water status as a result of decreased stomatal conductance and reduced leaf transpiration.
Conclusions
It is suggested that there is a limited capacity for photorespiration or the Mehler reaction to act as significant alternative electron sinks under water stress in C4 photosynthesis. This may explain why C4 photosynthesis is equally or even more sensitive to water stress than its C3 counterpart in spite of the greater capacity and water use efficiency of the C4 photosynthetic pathway.
doi:10.1093/aob/mcn093
PMCID: PMC2707343  PMID: 18552367
C3 and C4 photosynthesis; stomatal and non-stomatal limitation; high CO2; water stress
16.  Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding 
Annals of Botany  2008;103(4):599-607.
Background
Photosynthetic electron transport is performed by a chain of redox components that are electrochemically connected in series. Its efficiency depends on the balanced action of the photosystems and on the interaction with the dark reaction. Plants are sessile and cannot escape from environmental conditions such as fluctuating illumination, limitation of CO2 fixation by low temperatures, salinity, or low nutrient or water availability, which disturb the homeostasis of the photosynthetic process. Photosynthetic organisms, therefore, have developed various molecular acclimation mechanisms that maintain or restore photosynthetic efficiency under adverse conditions and counteract abiotic stresses. Recent studies indicate that redox signals from photosynthetic electron transport and reactive oxygen species (ROS) or ROS-scavenging molecules play a central role in the regulation of acclimation and stress responses.
Scope
The underlying signalling network of photosynthetic redox control is largely unknown, but it is already apparent that gene regulation by redox signals is of major importance for plants. Signalling cascades controlling the expression of chloroplast and nuclear genes have been identified and dissection of the different pathways is advancing. Because of the direction of information flow, photosynthetic redox signals can be defined as a distinct class of retrograde signals in addition to signals from organellar gene expression or pigment biosynthesis. They represent a vital signal of mature chloroplasts that report their present functional state to the nucleus. Here we describe possible problems in the elucidation of redox signalling networks and discuss some aspects of plant cell biology that are important for developing suitable experimental approaches.
Conclusions
The photosynthetic function of chloroplasts represents an important sensor that integrates various abiotic changes in the environment into corresponding molecular signals, which, in turn, regulate cellular activities to counterbalance the environmental changes or stresses.
doi:10.1093/aob/mcn081
PMCID: PMC2707342  PMID: 18492734
Photosynthesis; redox signals; gene expression; regulatory network; retrograde signalling; cross-talk; plastids; higher plants
17.  Evaluating the microtubule cytoskeleton and its interacting proteins in monocots by mining the rice genome 
Annals of Botany  2008;103(3):387-402.
Background
Microtubules (MTs) are assembled by heterodimers of α- and β-tubulins, which provide tracks for directional transport and frameworks for the spindle apparatus and the phragmoplast. MT nucleation and dynamics are regulated by components such as the γ-tubulin complex which are conserved among eukaryotes, and other components which are unique to plants. Following remarkable progress made in the model plant Arabidopsis thaliana toward revealing key components regulating MT activities, the completed rice (Oryza sativa) genome has prompted a survey of the MT cytoskeleton in this important crop as a model for monocots.
Scope
The rice genome contains three α-tubulin genes, eight β-tubulin genes and a single γ-tubulin gene. A functional γ-tubulin ring complex is expected to form in rice as genes encoding all components of the complex are present. Among proteins that interact with MTs, compared with A. thaliana, rice has more genes encoding some members such as the MAP65/Ase1p/PRC1 family, but fewer for the motor kinesins, the end-binding protein EB1 and the mitotic kinase Aurora. Although most known MT-interacting factors have apparent orthologues in rice, no orthologues of arabidopsis RIC1 and MAP18 have been identified in rice. Among all proteins surveyed here, only a few have had their functions characterized by genetic means in rice. Elucidating functions of proteins of the rice MT cytoskeleton, aided by recent technical advances made in this model monocot, will greatly advance our knowledge of how monocots employ their MTs to regulate their growth and form.
doi:10.1093/aob/mcn248
PMCID: PMC2707338  PMID: 19106179
Cytoskeleton; kinesins; microtubules (MTs); microtubule-associated proteins (MAPs); motors; rice; Oryza sativa
18.  Field methods for sampling and storing nectar from flowers with low nectar volumes 
Annals of Botany  2008;103(3):533-542.
Background and Aims
Although several methods of sampling and storing floral nectar are available, little information exists on sampling and storing nectar from flowers with low nectar volumes. Methods for sampling and storing nectar from the flowers of species with low floral nectar volumes (<1 µL) were investigated using the flowers of Eucalyptus species.
Methods
Sampling with microcapillary tubes, blotting up with filter paper, washing and rinsing were compared to determine masses of sugars recovered and differences in sugar ratios. Storage methods included room temperature, refrigeration and freezing treatments; the addition of antimicrobial agents benzyl alcohol or methanol to some of these treatments was also evaluated. Nectar samples were analysed using high-performance liquid chromatography and the masses of sucrose, glucose and fructose in each sample were determined.
Key Results
Masses of sugars varied significantly among sampling treatments, but the highest yielding methods, rinsing and washing, were not significantly different. A washing time of 1 min was as effective as one of 20 min. Storage trials showed that the sugar concentration measurements of nectar solutions changed rapidly, with the best results achieved for refrigeration with no additive (sucrose and fructose were stable for at least 2 weeks). Sugar ratios, however, remained relatively stable in most treatments and did not change significantly across 4 weeks for the methanol plus refrigerator and freezing treatments, and 2 weeks for the refrigeration treatment with no additive.
Conclusions
Washing is recommended for nectar collection from flowers with low nectar volumes in the field (with the understanding that one wash underestimates the amounts of sugars present in a flower), as is immediate analysis of sugar mass. In view of the great variation in results depending on nectar collection and storage methods, caution should be exercised in their choice, and their accuracy should be evaluated. The use of pulsed amperometric detection, more specific than refractive index detection, may improve the accuracy of nectar sugar analysis.
doi:10.1093/aob/mcn241
PMCID: PMC2707336  PMID: 19074446
Eucalyptus; flower with small nectar volume; nectar collection; nectar sampling; nectar storage; sugar ratio
19.  A proposed mechanism for physical dormancy break in seeds of Ipomoea lacunosa (Convolvulaceae) 
Annals of Botany  2008;103(3):433-445.
Background and Aims
The water-impermeable seeds of Ipomoea lacunosa undergo sensitivity cycling to dormancy breaking treatment, and slits are formed around bulges adjacent to the micropyle during dormancy break, i.e. the water gap opens. The primary aim of this research was to identify the mechanism of slit formation in seeds of this species.
Methods
Sensitive seeds were incubated at various combinations of relative humidity (RH) and temperature after blocking the hilar area in different places. Increase in seed mass was measured before and after incubation. Scanning electron microscopy (SEM) and staining of insensitive and sensitive seeds were carried out to characterize these states morphologically and anatomically. Water absorption was monitored at 35 and 25 °C at 100 % RH.
Key Results
There was a significant relationship between incubation temperature and RH with percentage seed dormancy break. Sensitive seeds absorbed water vapour, but insensitive seeds did not. Different amounts of water were absorbed by seeds with different blocking treatments. There was a significant relationship between dormancy break and the amount of water absorbed during incubation.
Conclusions
Water vapour seals openings that allow it to escape from seeds and causes pressure to develop below the bulge, thereby causing slits to form. A model for the mechanism of formation of slits (physical dormancy break) is proposed.
doi:10.1093/aob/mcn240
PMCID: PMC2707335  PMID: 19098068
Convolvulaceae; Ipomoea lacunosa; dormancy-breaking mechanism; physical dormancy; seeds; sensitivity cycling; water vapour
20.  Mycorrhization and phosphorus nutrition affect water relations and CAM induction by drought in seedlings of Clusia minor 
Annals of Botany  2008;103(3):525-532.
Background and Aims
Crassulacean acid metabolism (CAM) is currently viewed as an adaptation to water deficit. In plants of Clusia minor, which grow mostly on acidic, P-deficient soils, CAM is induced by water deficit. The symbiosis between plants and mycorrhizal fungi alleviates the symptoms of P deficiency and may influence drought resistance. Therefore, the effect of P supply, modified by three different experimental treatments, on the induction of CAM by drought in C. minor was investigated to test the hypothesis that P deficiency will produce greater CAM activity and, in addition, that treatment will modify drought tolerance.
Methods
Seedlings were grown in forest soil sterilized and inoculated with Scutellospora fulgida (SF treatment), sterilized and supplemented with P (Ph treatment) or non-sterilized and containing native mycorrhizae (Nat treatment). Leaf turgor potential (ψT) was determined psychrometrically, and CAM activity as nocturnal acid accumulation (ΔH+) by titration of dawn and dusk leaf sap.
Key Results
Plant mass and P content were higher in SF and Ph than in Nat seedlings. After 21 d of water deficit, ψT increased in SF, decreased in Ph and remained unchanged in Nat, and, after 7 and 14 d of water deficit, ΔH+ in Nat was three times higher than at the beginning of drought, whereas in SF and Ph ΔH+ was lower than on day 0.
Conclusions
P deficiency in Nat seedlings was ameliorated by inoculation or P addition. The SF and Nat seedlings showed greater tolerance of drought than Ph. P deficiency promoted the induction of CAM by drought in Nat seedlings, whereas P fertilization and mycorrhization did not. Nocturnal acid accumulation was highly and negatively correlated with plant P and N contents, indicating that P and N deficiencies are promoters of CAM in droughted plants of C. minor.
doi:10.1093/aob/mcn238
PMCID: PMC2707333  PMID: 19049985
Clusia minor; crassulacean acid metabolism; CAM; mycorrhiza; drought; phosphorus deficiency; nitrogen–water relations
21.  Food bodies in Cissus verticillata (Vitaceae): ontogenesis, structure and functional aspects 
Annals of Botany  2008;103(3):517-524.
Background and Aims
The distinction between pearl bodies (or pearl glands) and food bodies (FBs) is not clear; neither is our understanding of what these structures really represent. The present work examined the ontogenesis, structure, ultrastructure and histochemical aspects of the protuberances in Cissus verticillata, which have been described since the beginning of the 19th century as pearl glands or pearl bodies, in order to establish a relationship between their structure and function.
Methods
Segments of stems and leaves in different stages of development were collected and fixed for study under light microscopy as well as electron transmission and scanning microscopy. Samples of FBs were subjected to chemical analysis using thin-layer chromatography.
Key Results
The FBs in C. verticillata are globose and attached to the plant by a short peduncle. These structures are present along the entire stem during primary growth, and on the inflorescence axis and the abaxial face of the leaves. The FBs were observed to be of mixed origin, with the participation of both the epidermis and the underlying parenchymatic cells. The epidermis is uniseriate with a thin cuticle, and the cells have dense cytoplasm and a large nucleus. The internal parenchymatic cells have thin walls; in the young structures these cells have dense cytoplasm with a predominance of mitochondria and plastids. In the mature FBs, the parenchymatic cells accumulate oils and soluble sugars; dictyosomes and rough endoplasmic reticulum predominate in the cytoplasm; the vacuoles are ample. Removal of the FBs appears to stimulate the formation of new ones, at the same place.
Conclusions
The vegetative vigour of the plant seems to influence the number of FBs produced, with more vigorous branches having greater densities of FBs. The results allow the conclusion that the structures traditionally designated pearl glands or pearl bodies in C. verticillata constitute FBs that can recruit large numbers of ants.
doi:10.1093/aob/mcn237
PMCID: PMC2707332  PMID: 19049986
Ant–plant interactions; Cissus verticillata; food bodies; myrmecophily; pearl glands; pearl bodies; cell ultrastructure; Vitaceae
22.  Recognition of root exudates by seeds of broomrape (Orobanche and Phelipanche) species 
Annals of Botany  2008;103(3):423-431.
Background and Aims
The long co-existence of broomrapes and their hosts within the same environment has culminated in a strong adaptation and effective parasitism. As a first step of specialization in the parasitic process, seed receptors of parasitic plant species vary in their ability to recognize compounds released by their hosts. This work aims to investigate potential patterns for the reception requirements needed to activate germination within Orobanche and Phelipanche species.
Methods
Induction of the germination of seeds of nine Orobanche and Pheliphanche species by root exudates of 41 plant species was studied and subjected to biplot multivariate analysis.
Key Results
A high level of specialization in root exudate recognition was found in Orobanche densiflora, O. gracilis and O. hederae, which germinated almost exclusively in contact with root exudates from the plants they infect in nature. At the opposite extreme, Phelipanche aegyptiaca, P. ramosa and O. minor were highly generalist, germinating when in contact with the root exudates of most plant species. Orobanche crenata, O. cumana and O. foetida showed intermediate behaviour.
Conclusions
A universal germination stimulant for all broomrape species has not being identified to date. The synthetic stimulant GR24 is active against most of the weedy broomrape species, but fails with the non-weedy species tested in this study and with the very recent weedy species O. foetida. In addition, germination behaviour of broomrape species depends on the crop plant tested. Weedy broomrapes with a broad host spectrum respond better to the different exudates released by a wide range of crops and wild species than do non-weedy broomrapes, which have a narrow host spectrum and are more restricted to their host range. Root exudates of many plant species were active in stimulating germination of seeds of Orobanche and Phelipanche species for which they are not described as hosts, representing interesting examples of potential trap crops.
doi:10.1093/aob/mcn236
PMCID: PMC2707331  PMID: 19049987
Xenognosis; broomrape; root exudate; germination; Orobanche; Phelipanche
23.  Preformation and distribution of staminate and pistillate flowers in growth units of Nothofagus alpina and N. obliqua (Nothofagaceae) 
Annals of Botany  2008;103(3):411-421.
Background and Aims
The distribution and differentiation times of flowers in monoecious wind-pollinated plants are fundamental for the understanding of their mating patterns and evolution. Two closely related South American Nothofagus species were compared with regard to the differentiation times and positions of staminate and pistillate flowers along their parent growth units (GUs) by quantitative means.
Methods
Two samples of GUs that had extended in the 2004–2005 growing season were taken in 2005 and 2006 from trees in the Lanín National Park, Patagonia, Argentina. For the first sample, axillary buds of the parent GUs were dissected and the leaf, bud and flower primordia of these buds were identified. The second sample included all branches derived from the parent GUs in the 2005–2006 growing season.
Key Results
Both species developed flowering GUs with staminate and/or pistillate flowers; GUs with both flower types were the most common. The position of staminate flowers along GUs was similar between species and close to the proximal end of the GUs. Pistillate flowers were developed more distally along the GUs in N. alpina than in N. obliqua. In N. alpina, the nodes bearing staminate and pistillate flowers were separated by one to several nodes with axillary buds, something not observed in N. obliqua. Markovian models supported this between-species difference. Flowering GUs, including all of their leaves and flowers were entirely preformed in the winter buds.
Conclusions
Staminate and pistillate flowers of N. alpina and N. obliqua are differentiated at precise locations on GUs in the growing season preceding that of their antheses. The differences between N. alpina and N. obliqua (and other South American Nothofagus species) regarding flower distribution might relate to the time of anthesis of each flower type and, in turn, to the probabilities of self-pollination at the GU level.
doi:10.1093/aob/mcn235
PMCID: PMC2707330  PMID: 19033286
Branch; bud; growth unit; Markovian models; Nothofagus alpina; N. obliqua; Patagonian forests; pistillate flower; preformation; staminate flower
24.  The extreme halophyte Salicornia veneta is depleted of the extrinsic PsbQ and PsbP proteins of the oxygen-evolving complex without loss of functional activity 
Annals of Botany  2008;103(3):505-515.
Background and Aims
Photosystem II of oxygenic organisms is a multi-subunit protein complex made up of at least 20 subunits and requires Ca2+ and Cl− as essential co-factors. While most subunits form the catalytic core responsible for water oxidation, PsbO, PsbP and PsbQ form an extrinsic domain exposed to the luminal side of the membrane. In vitro studies have shown that these subunits have a role in modulating the function of Cl− and Ca2+, but their role(s) in vivo remains to be elucidated, as the relationships between ion concentrations and extrinsic polypeptides are not clear. With the aim of understanding these relationships, the photosynthetic apparatus of the extreme halophyte Salicornia veneta has been compared with that of spinach. Compared to glycophytes, halophytes have a different ionic composition, which could be expected to modulate the role of extrinsic polypeptides.
Methods
Structure and function of in vivo and in vitro PSII in S. veneta were investigated and compared to spinach. Light and electron microscopy, oxygen evolution, gel electrophoresis, immunoblotting, DNA sequencing, RT–PCR and time-resolved chlorophyll fluorescence were used.
Key Results
Thylakoids of S. veneta did not contain PsbQ protein and its mRNA was absent. When compared to spinach, PsbP was partly depleted (30 %), as was its mRNA. All other thylakoid subunits were present in similar amounts in both species. PSII electron transfer was not affected. Fluorescence was strongly quenched upon irradiation of plants with high light, and relaxed only after prolonged dark incubation. Quenching of fluorescence was not linked to degradation of D1 protein.
Conclusions
In S. veneta the PsbQ protein is not necessary for photosynthesis in vivo. As the amount of PsbP is sub-stoichiometric with other PSII subunits, this protein too is largely dispensable from a catalytic standpoint. One possibility is that PsbP acts as an assembly factor for PSII.
doi:10.1093/aob/mcn234
PMCID: PMC2707329  PMID: 19033288
Photosystem II; PsbQ; PsbP; halophytes; Salicornia veneta
25.  Regulation of tomato fruit ascorbate content is more highly dependent on fruit irradiance than leaf irradiance 
Annals of Botany  2008;103(3):495-504.
Background and Aims
The mechanisms involving light control of vitamin C content in fruits are not yet fully understood. The present study aimed to evaluate the impact of fruit and leaf shading on ascorbate (AsA) accumulation in tomato fruit and to determine how fruit sugar content (as an AsA precursor) affected AsA content.
Methods
Cherry tomato plants were grown in a glasshouse. The control treatment (normally irradiated fruits and irradiated leaves) was compared with the whole-plant shading treatment and with leaf or fruit shading treatments in fruits harvested at breaker stage. In a second experiment, the correlation between sugars and AsA was studied during ripening.
Key Results
Fruit shading was the most effective treatment in reducing fruit AsA content. Under normal conditions, AsA and sugar content were correlated and increased with the ripening stage. Reducing fruit irradiance strongly decreased the reduced AsA content (−74 %), without affecting sugars, so that sugar and reduced AsA were no longer correlated. Leaf shading delayed fruit ripening: it increased the accumulation of oxidized AsA in green fruits (+98 %), whereas it decreased the reduced AsA content in orange fruits (−19 %), suggesting that fruit AsA metabolism also depends on leaf irradiance.
Conclusions
Under fruit shading only, the absence of a correlation between sugars and reduced AsA content indicated that fruit AsA content was not limited by leaf photosynthesis or sugar substrate, but strongly depended on fruit irradiance. Leaf shading most probably affected fruit AsA content by delaying fruit ripening, and suggested a complex regulation of AsA metabolism which depends on both fruit and leaf irradiance and fruit ripening stage.
doi:10.1093/aob/mcn233
PMCID: PMC2707328  PMID: 19033285
Ascorbate; fruit quality; irradiance; shading; Solanum lycopersicon; sugars; tomato; vitamin C

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