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1.  Differences in salinity tolerance of genetically distinct Phragmites australis clones 
AoB Plants  2013;5:plt019.
The common reed (Phragmites australis) is a clonal wetland grass with high genetic variability. Clone-specific differences are reflected in morphological and physiological traits, and hence in the ability to cope with environmental stress. The responses to progressively increasing salinity of fifteen distinct Phragmites australis clones reveal genotype-related strategies of salt avoidance and exclusion. The salinity-induced inhibition in shoot elongation rate and photosynthesis varies widely between clones. The differences can be partially attributed to their geographic range, but not correlated to ploidy level. Thus, the genetic background is a major factor influencing the salinity tolerance of distinct Phragmites australis clones.
Different clones of the wetland grass Phragmites australis differ in their morphology and physiology, and hence in their ability to cope with environmental stress. We analysed the responses of 15 P. australis clones with distinct ploidy levels (PLs) (4n, 6n, 8n, 10n, 12n) and geographic origins (Romania, Russia, Japan, Czech Republic, Australia) to step-wise increased salinity (8, 16, 24, 32, 40, 56 and 72 ppt). Shoot elongation rate, photosynthesis and plant part-specific ion accumulation were studied in order to assess if traits associated with salinity tolerance can be related to the genetic background and the geographic origin of the clones. Salt stress affected all clones, but at different rates. The maximum height was reduced from 1860 mm in control plants to 660 mm at 40 ppt salinity. The shoot elongation rate of salt-exposed plants varied significantly between clones until 40 ppt salinity. The light-saturated photosynthesis rate (Pmax) was stimulated by a salinity of 8 ppt, but decreased significantly at higher salinities. The stomatal conductance (gs) and the transpiration rate (E) decreased with increasing salinity. Only three clones survived at 72 ppt salinity, although their rates of photosynthesis were strongly inhibited. The roots and basal leaves of the salt-exposed plants accumulated high concentrations of water-extractable Na+ (1646 and 1004 µmol g−1 dry mass (DM), respectively) and Cl− (1876 and 1400 µmol g−1 DM, respectively). The concentrations of water-extractable Mg2+ and Ca2+ were reduced in salt-exposed plants compared with controls. The variation of all the measured parameters was higher among clones than among PLs. We conclude that the salinity tolerance of distinct P. australis clones varies widely and can be partially attributed to their longitudinal geographic origin, but not to PL. Further investigation will help in improving the understanding of this species' salt tolerance mechanisms and their connection to genetic factors.
PMCID: PMC4104622
Common reed; ecophysiology; geographic range; ion concentration; ploidy level; salt-stress tolerance
2.  Exploring the borders of European Phragmites within a cosmopolitan genus 
AoB Plants  2012;2012:pls020.
European Phragmites australis is one of four main cp-DNA haplotype clusters present worldwide. The European gene pool extends from North America to Far East Asia and South Africa. Extensive gene flow occurs only within the temperate region of Europe.
Background and aims
Two Phragmites australis taxa are recognized in Europe: P. australis ssp. altissimus, also known as Phragmites isiaca, in the Mediterranean region and P. australis in the temperate region. Another taxonomic group in the Mediterranean is Phragmites frutescens. European genotypes are diverse genetically, cytologically and morphologically, and are related to African, Asiatic and American genotypes. We investigated chloroplast DNA (cpDNA) diversity in Europe and defined the current borders of the European gene pool.
We analysed chloroplast variation with parsimony and genetic distance methods, and compared it with that of nuclear amplified fragment length polymorphism and microsatellites. We also investigated the phenological pattern of 188 genotypes collected worldwide in a common garden in Denmark. We assumed that non-flowering genotypes could indicate climatic, geographic and/or reproductive barriers to dispersal and would have been recorded in the genetic pattern as groups genetically isolated from, or within, the European pool.
Principal results
The European P. australis gene pool extends from North America to the Far East and South Africa. However, African and North American genotypes are differentiating from the European genotypes. Mediterranean P. australis is genetically different from temperate P. australis and shares several similarities with Phragmites mauritianus in Africa and Phragmites karka in Asia. Phragmites frutescens shares the cpDNA sequences with both these tropical species. Two DNA bands can distinguish Mediterranean P. australis from P. frutescens and P. mauritianus and from temperate P. australis, and reveal possible hybrids among these species in the Mediterranean region. Phenological data confirmed possible gene flow within the temperate region of Europe, whereas the Mediterranean genotypes did not set inflorescences in Denmark, suggesting reproductive barriers between temperate and Mediterranean P. australis.
European P. australis appears as one of four main Phragmites groups known in the world. Further research is needed to understand the implications of long-distance dispersal at the population level.
PMCID: PMC3435523  PMID: 22962631
3.  Jack-and-Master Trait Responses to Elevated CO2 and N: A Comparison of Native and Introduced Phragmites australis 
PLoS ONE  2012;7(10):e42794.
Global change is predicted to promote plant invasions world-wide, reducing biodiversity and ecosystem function. Phenotypic plasticity may influence the ability of introduced plant species to invade and dominate extant communities. However, interpreting differences in plasticity can be confounded by phylogenetic differences in morphology and physiology. Here we present a novel case investigating the role of fitness trait values and phenotypic plasticity to global change factors between conspecific lineages of Phragmites australis. We hypothesized that due to observed differences in the competitive success of North American-native and Eurasian-introduced P. australis genotypes, Eurasian-introduced P. australis would exhibit greater fitness in response to global change factors. Plasticity and plant performance to ambient and predicted levels of carbon dioxide and nitrogen pollution were investigated to understand how invasion pressure may change in North America under a realistic global change scenario. We found that the introduced Eurasian genotype expressed greater mean trait values in nearly every ecophysiological trait measured – aboveground and belowground – to elevated CO2 and nitrogen, outperforming the native North American conspecific by a factor of two to three under every global change scenario. This response is consistent with “jack and master” phenotypic plasticity. We suggest that differences in plant nitrogen productivity, specific leaf area, belowground biomass allocation, and inherently higher relative growth rate are the plant traits that may enhance invasion of Eurasian Phragmites in North America. Given the high degree of genotypic variability within this species, and our limited number of genotypes, our results must be interpreted cautiously. Our study is the first to demonstrate the potential importance of jack-and-master phenotypic plasticity in plant invasions when facing imminent global change conditions. We suggest that jack-and-master invasive genotypes and/or species similar to introduced P. australis will have an increased ecological fitness, facilitating their invasion in both stressful and resource rich environments.
PMCID: PMC3485286  PMID: 23118844
4.  Interactive effects of elevated temperature and CO2 on two phylogeographically distinct clones of common reed (Phragmites australis) 
AoB Plants  2013;5:pls051.
One European and one Mediterranean Phragmites australis genotype (DK clone and ALG clone, respectively) showed distinct aboveground growth and physiology in response to different treatment combinations of elevated CO2 and temperature according to their genetic background. The DK clone was the most responsive clone.
The aboveground growth, physiological and biochemical parameters of two clones of the cosmopolitan wetland grass Phragmites australis, grown at four treatment combinations of temperature and CO2, were investigated to elucidate whether their climate response differed due to inherent differences in their ecological adaptation. The two phylogeographically distinct P. australis clones (DK clone, European genetic background; ALG clone, Mediterranean genetic background) were grown for 151 days in phytotrons at 19/12 °C (day/night temperature) and 390 ppm CO2, and at elevated temperature (+5 °C) and CO2 (700 ppm) with treatment factors alone or in combination. The ALG clone had 2–4 times higher aboveground biomass, higher light-saturated rates of photosynthesis (Pmax), maximum electron transport rates (ETRmax) and Rubisco activity, and higher photosynthetic nitrogen-use efficiency than the DK clone. The DK clone, however, produced more shoots, leaves and side-shoots, and had 9–51 % higher specific leaf area and 15–39 % higher leaf nitrogen concentration than the ALG clone. Although elevated atmospheric CO2 alone barely affected the aboveground growth of the two P. australis clones, simultaneously elevated temperature and CO2 stimulated growth and aboveground biomass. Overall, elevated CO2 stimulated photosynthesis, but the clones responded differently to a concomitant increase in CO2 and temperature, depending on the phylogeographic background of the plant. The DK clone showed overall stronger responses, and can be considered the more plastic of the two clones with respect to CO2 and temperature. Thus, the DK clone may be better adapted to climate change than the ALG clone, at least in the short term.
PMCID: PMC4104621
Algeria; climate change; Denmark; Mediterranean Phragmites; RERAF phytotron; temperate Phragmites
5.  Physiological ecology and functional traits of North American native and Eurasian introduced Phragmites australis lineages 
AoB Plants  2013;5:plt048.
Biological invasion pose serious threats to biodiversity and ecosystem services worldwide. While the effects of invasive species are well-documents, less is known about which specific plant traits convey “invasiveness” because most studies compare closely related, but different species which can confound results. A review of the literature by Mozdzer and other scientists compared genetic lineages of the same species, those native to North American and a lineage introduced from Europe to address this complex issue. The authors found that the ability to change both physiologically and morphologically were the key to success of the introduced genetic lineage under current and predicted global change conditions.
Physiological ecology and plant functional traits are often used to explain plant invasion. To gain a better understanding of how traits influence invasion, studies usually compare the invasive plant to a native congener, but there are few conspecific examples in the literature. In North America, the presence of native and introduced genetic lineages of the common reed, Phragmites australis, presents a unique example to evaluate how traits influence plant invasion. We reviewed the literature on functional traits of P. australis lineages in North America, specifically contrasting lineages present on the Atlantic Coast. We focused on differences in physiology between the lineage introduced from Eurasia and the lineage native to North America, specifically seeking to identify the causes underlying the recent expansion of the introduced lineage. Our goals were to better understand which traits may confer invasiveness, provide predictions of how these lineages may respond to interspecific competition or imminent global change, and provide guidance for future research. We reviewed published studies and articles in press, and conducted personal communications with appropriate researchers and managers to develop a comparative dataset. We compared the native and introduced lineages and focused on plant physiological ecology and functional traits. Under both stressful and favourable conditions, our review showed that introduced P. australis consistently exhibited greater ramet density, height and biomass, higher and more plastic relative growth rate, nitrogen productivity and specific leaf area, higher mass specific nitrogen uptake rates, as well as greater phenotypic plasticity compared with the native lineage. We suggest that ecophysiological and other plant functional traits elucidate potential mechanisms for the introduced lineage's invasiveness under current and predicted global change conditions. However, our review identified a disconnect between field surveys, experiments, natural competition and plant ecophysiology that must be addressed in future field studies. Given the likelihood of hybridization between lineages, a better understanding of plant traits in native, non-native and hybrid lineages is needed to manage current invasions and to predict the outcome of interactions among novel genotypes. Comparative physiology and other plant functional traits may provide additional tools to predict the trajectory of current and potential future invasions.
PMCID: PMC4104623
Conspecific; global change; invasive; nitrogen; nitrogen productivity; phenotypic plasticity; relative growth rate; specific leaf area; wetland.
6.  Hybridization of common reed in North America? The answer is blowing in the wind 
AoB Plants  2012;2012:pls022.
Hybridization of Phragmites has occurred in the Gulf Coast and likely is occurring elsewhere in North America. However, detection failure may be due to limited genetic tools. Additionally, nomenclature confusion necessitates a revision of the current classification system.
Background and aims
We review evidence for hybridization of Phragmites australis in North America and the implications for the persistence of native P. australis ssp. americanus populations in North America. We also highlight the need for an updated classification system, which takes P. australis intraspecific variation and hybridization into account.
We reviewed available published, in press and in preparation literature to assess the likelihood of hybridization and interbreeding in genotypes of P. australis present in North America.
Principal results
Experimental results demonstrate that hybridization among introduced and native haplotypes is possible within the genus Phragmites, yet evidence that hybridization has occurred naturally is only starting to emerge. The lag in identifying hybridization in Phragmites in North America may be related to under-sampling in some parts of North America and to a lack of molecular tools that provide the capability to recognize hybrids.
Our understanding of the gene flow within and between species in the genus Phragmites is moving at a fast pace, especially on the east and Gulf coasts of North America. More attention should also be focused on the Great Lakes region, the southwestern and the west coast of the USA, where sympatry has created opportunities for hybridization. Where hybridizations have been detected, there are currently no published data on how hybridization affects plant vigour, morphology, invasiveness or conservation of the genetic integrity of the North American native subspecies. We conclude that the detection of more hybridization is highly likely and that there is a need to develop new markers for the different Phragmites species and lineages to fill current knowledge gaps. Finally, we suggest that the classification system for P. australis should be updated and published to help clarify the nomenclature.
PMCID: PMC3444738  PMID: 22993684
7.  Moving from a regional to a continental perspective of Phragmites australis invasion in North America 
AoB Plants  2012;2012:pls040.
Here we describe the results of a regional comparison of introduced Phragmites australis and two other P. australis lineages found in North America. The regional similarities and differences in introduced P. australis invasion highlight the importance of continental-scale studies for decoding plant invasions.
We use a regional comparison of Phragmites australis (common reed) subsp. americanus, P. australis subsp. berlandieri and introduced P. australis (possibly five sublineages) in the Chesapeake Bay, the St Lawrence River, Utah and the Gulf Coast to inform a North American perspective on P. australis invasion patterns, drivers, impacts and research needs.
Findings and research needs
Our regional assessments reveal substantial diversity within and between the three main lineages of P. australis in terms of mode of reproduction and the types of environment occupied. For introduced P. australis, the timing of introduction also differed between the regions. Nevertheless, a common finding in these regions reinforces the notion that introduced P. australis is opportunistic and thrives in disturbed habitats. Thus, we expect to see substantial expansion of introduced P. australis with increasing anthropogenic disturbances in each of these regions. Although there have been some studies documenting the negative impacts of introduced P. australis, it also plays a beneficial role in some regions, and in some cases, the purported negative impacts are unproven. There is also a broader need to clarify the genetic and ecological relationships between the different introduced sublineages observed in North America, and their relative competitive ability and potential for admixture. This may be done through regional studies that use similar methodologies and share results to uncover common patterns and processes. To our knowledge, such studies have not been performed on P. australis in spite of the broad attention given to this species. Such research could advance theoretical knowledge on biological invasion by helping to determine the extent to which the patterns observed can be generalized or are sublineage specific or region specific.
Given what appears to be sometimes idiosyncratic invasion patterns when interpreted in isolation in the regions that we analysed, it may be time to consider initiatives on a continental (if not intercontinental) scale to tackle unresolved issues about P. australis.
PMCID: PMC3676263  PMID: 23755351
8.  Preadaptation and post-introduction evolution facilitate the invasion of Phragmites australis in North America 
Ecology and Evolution  2014;4(24):4567-4577.
Compared with non-invasive species, invasive plant species may benefit from certain advantageous traits, for example, higher photosynthesis capacity and resource/energy-use efficiency. These traits can be preadapted prior to introduction, but can also be acquired through evolution following introduction to the new range. Disentangling the origins of these advantageous traits is a fundamental and emerging question in invasion ecology. We conducted a multiple comparative experiment under identical environmental condition with the invasive haplotype M lineage of the wetland grass Phragmites australis and compared the ecophysiological traits of this invasive haplotype M in North America with those of the European ancestor and the conspecific North American native haplotype E lineage, P. australis ssp. americanus. The invasive haplotype M differed significantly from the native North American conspecific haplotype E in several ecophysiological and morphological traits, and the European haplotype M had a more efficient photosynthetic apparatus than the native North American P. australis ssp. americanus. Within the haplotype M lineage, the introduced North American P. australis exhibited different biomass allocation patterns and resource/energy-use strategies compared to its European ancestor group. A discriminant analysis of principal components separated the haplotype M and the haplotype E lineages completely along the first canonical axis, highly related to photosynthetic gas-exchange parameters, photosynthetic energy-use efficiency and payback time. The second canonical axis, highly related to photosynthetic nitrogen use efficiency and construction costs, significantly separated the introduced P. australis in North America from its European ancestor. Synthesis. We conclude that the European P. australis lineage was preadapted to be invasive prior to its introduction, and that the invasion in North America is further stimulated by rapid post-introduction evolution in several advantageous traits. The multicomparison approach used in this study could be an effective approach for distinguishing preadaptation and post-introduction evolution of invasive species. Further research is needed to link the observed changes in invasive traits to the genetic variation and the interaction with the environment.
PMCID: PMC4278810  PMID: 25558352
Biomass allocation; common reed; common-environment experiment; discriminant analysis; ecophysiological trade-off; functional traits; invasion ecology; leaf construction cost; photosynthesis; standardized major axis (SMA)
9.  Expression of major photosynthetic and salt-resistance genes in invasive reed lineages grown under elevated CO2 and temperature 
Ecology and Evolution  2014;4(21):4161-4172.
It is important to investigate the molecular causes of the variation in ecologically important traits to fully understand phenotypic responses to climate change. In the Mississippi River Delta, two distinct, sympatric invasive lineages of common reed (Phragmites australis) are known to differ in several ecophysiological characteristics and are expected to become more salt resistant due to increasing atmospheric CO2 and temperature. We investigated whether different patterns of gene expression can explain their ecophysiological differences and increased vigor under future climatic conditions. We compared the transcript abundance of photosynthetic genes of the Calvin cycle (Rubisco small subunit, RbcS; Phosphoglycerate kinase, PGK; Phosphoribulokinase, PRK), genes related with salt transport (Na+/H+ antiporter, PhaNHA) and oxidative stress response genes (Manganese Superoxide dismutase, MnSOD; Glutathione peroxidase, GPX), and the total aboveground biomass production between two genotypes representing the two lineages. The two genotypes (Delta-type, Mediterranean lineage, and EU-type, Eurasian lineage) were grown under an ambient and a future climate scenario with simultaneously elevated CO2 and temperature, and under two different soil salinities (0‰ or 20‰). We found neither differences in the aboveground biomass production nor the transcript abundances of the two genotypes, but soil salinity significantly affected all the investigated parameters, often interacting with the climatic conditions. At 20‰ salinity, most genes were higher expressed in the future than in the ambient climatic conditions. Higher transcription of the genes suggests higher abundance of the protein they code for, and consequently increased photosynthate production, improved stress responses, and salt exclusion. Therefore, the higher expression of these genes most likely contributed to the significantly ameliorated salinity impact on the aboveground biomass production of both P. australis genotypes under elevated temperature and CO2. Although transcript abundances did not explain differences between the lineages, they correlated with the increased vigor of both lineages under anticipated future climatic conditions.
PMCID: PMC4242567  PMID: 25505541
Common reed; Delta-type; EU-type; Mississippi River Delta; Phragmites australis; US Gulf Coast
10.  Vegetation Types Alter Soil Respiration and Its Temperature Sensitivity at the Field Scale in an Estuary Wetland 
PLoS ONE  2014;9(3):e91182.
Vegetation type plays an important role in regulating the temporal and spatial variation of soil respiration. Therefore, vegetation patchiness may cause high uncertainties in the estimates of soil respiration for scaling field measurements to ecosystem level. Few studies provide insights regarding the influence of vegetation types on soil respiration and its temperature sensitivity in an estuary wetland. In order to enhance the understanding of this issue, we focused on the growing season and investigated how the soil respiration and its temperature sensitivity are affected by the different vegetation (Phragmites australis, Suaeda salsa and bare soil) in the Yellow River Estuary. During the growing season, there were significant linear relationships between soil respiration rates and shoot and root biomass, respectively. On the diurnal timescale, daytime soil respiration was more dependent on net photosynthesis. A positive correlation between soil respiration and net photosynthesis at the Phragmites australis site was found. There were exponential correlations between soil respiration and soil temperature, and the fitted Q10 values varied among different vegetation types (1.81, 2.15 and 3.43 for Phragmites australis, Suaeda salsa and bare soil sites, respectively). During the growing season, the mean soil respiration was consistently higher at the Phragmites australis site (1.11 µmol CO2 m−2 s−1), followed by the Suaeda salsa site (0.77 µmol CO2 m−2 s−1) and the bare soil site (0.41 µmol CO2 m−2 s−1). The mean monthly soil respiration was positively correlated with shoot and root biomass, total C, and total N among the three vegetation patches. Our results suggest that vegetation patchiness at a field scale might have a large impact on ecosystem-scale soil respiration. Therefore, it is necessary to consider the differences in vegetation types when using models to evaluate soil respiration in an estuary wetland.
PMCID: PMC3946705  PMID: 24608636
11.  Belowground advantages in construction cost facilitate a cryptic plant invasion 
AoB Plants  2014;6:plu020.
Energetic costs of tissue construction were compared in two subspecies of Phragmites australis, the common reed – namely the primary native and introduced lineages in North America. Caplan et al. report that the introduced lineage has lower construction costs than the native under all environmental conditions assessed, driven mainly by its lower cost rhizomes. These results highlight the fact that belowground energetics, which are seldom investigated, can influence the performance advantages that drive many plant invasions. The authors also demonstrate that tissue construction costs in organs not typically assessed can shift with global change, suggesting that they may have increasingly important implications into the future.
The energetic cost of plant organ construction is a functional trait that is useful for understanding carbon investment during growth (e.g. the resource acquisition vs. tissue longevity tradeoff), as well as in response to global change factors like elevated CO2 and N. Despite the enormous importance of roots and rhizomes in acquiring soil resources and responding to global change, construction costs have been studied almost exclusively in leaves. We sought to determine how construction costs of aboveground and belowground organs differed between native and introduced lineages of a geographically widely dispersed wetland plant species (Phragmites australis) under varying levels of CO2 and N. We grew plants under ambient and elevated atmospheric CO2, as well as under two levels of soil nitrogen. We determined construction costs for leaves, stems, rhizomes and roots, as well as for whole plants. Across all treatment conditions, the introduced lineage of Phragmites had a 4.3 % lower mean rhizome construction cost than the native. Whole-plant construction costs were also smaller for the introduced lineage, with the largest difference in sample means (3.3 %) occurring under ambient conditions. In having lower rhizome and plant-scale construction costs, the introduced lineage can recoup its investment in tissue construction more quickly, enabling it to generate additional biomass with the same energetic investment. Our results suggest that introduced Phragmites has had an advantageous tissue investment strategy under historic CO2 and N levels, which has facilitated key rhizome processes, such as clonal spread. We recommend that construction costs for multiple organ types be included in future studies of plant carbon economy, especially those investigating global change.
PMCID: PMC4060782  PMID: 24938305
Carbon dioxide; common reed; construction cost; eutrophication; intraspecific; invasion ecology; Phragmites; plant functional traits; rhizomes; wetlands.
12.  Genetic Variation of Stomatal Traits and Carbon Isotope Discrimination in Two Hybrid Poplar Families (Populus deltoides ‘S9-2’ × P. nigra ‘Ghoy’ and P. deltoides ‘S9-2’ × P. trichocarpa ‘V24’) 
Annals of Botany  2008;102(3):399-407.
Background and Aims
Stomata play an important role in both the CO2 assimilation and water relations of trees. Therefore, stomatal traits have been suggested as criteria for selection of clones or genotypes which are more productive and have larger water-use efficiency (WUE) than others. However, the relationships between plant growth, WUE and stomatal traits are still unclear depending on plant material (genus, species, families, genotypes) and, more precisely, on the strength of the relationships between the plants. In this study, the correlations between these three traits categories, i.e. plant growth, WUE and stomatal traits, were compared in two related poplar families.
Stomatal traits (stomatal density, length and ratio adaxial : abaxial stomatal densities) of a selection of F1 genotypes and the parents of two hybrid poplar families Populus deltoides ‘S9-2’ × P. nigra ‘Ghoy’ (D × N family, 50 F1) and P. deltoides ‘S9-2’ × P. trichocarpa ‘V24’ (D × T family, 50 F1) were measured, together with stem height and circumference. Carbon isotope discrimination (Δ) was determined and used as an indicator of leaf-level intrinsic WUE.
Key Results
Leaves of hybrids and parents were amphistomatous, except for the P. trichocarpa parent. Both families displayed high values of heritability for stomatal traits and Δ. In the progeny, the relationship between stem circumference and Δ was weak for the D × N family, while abaxial and total stomatal density were positively associated with stem dimensions for the D × T family only.
Genetic variation in stomatal traits and Δ was large within as well as between the different poplar species and their hybrids, but there were no direct relationships between stomatal traits and plant growth or Δ. As already noticed in various poplar hybrids, the absence of, or the weak, relationship between Δ and plant growth allows the possibility of selecting poplar genotypes combining high productivity and high WUE. In this study, stomatal traits are of limited value as criteria for selection of genotypes with good growth and large WUE.
PMCID: PMC2701808  PMID: 18587131
Adaxial and abaxial stomatal density; stomatal length; heritability; water-use efficiency (WUE); F1 hybrids; breeding; Populus deltoides; Populus nigra; Populus trichocarpa
13.  Population Dynamics of Diploid and Hexaploid Populations of a Perennial Herb 
Annals of Botany  2007;100(6):1259-1270.
Background and Aims
Despite the recent enormous increase in the number of studies on polyploid species, no studies to date have explored the population dynamics of these taxa. It is thus not known whether the commonly reported differences in single life-history traits between taxa of different ploidy levels result in differences in population dynamics.
This study explores differences in single life-history traits and in the complete life cycle between populations of different ploidy levels and compares these differences with differences observed between different habitat types and years. Diploid and hexaploid populations of a perennial herb, Aster amellus, are used as the study system. Transition matrix models were used to describe the dynamics of the populations, and population growth rates, elasticity values and life-table response experiments were used to compare the dynamics between populations and years.
Key Results
The results indicate that between-year variation in population dynamics is much larger than variation between different ploidy levels and different habitat conditions. Significant differences exist, however, in the structure of the transition matrices, indicating that the dynamics of the different ploidy levels are different. Strong differences in probability of extinction of local populations were also found, with hexaploid populations having higher probability than diploid populations, indicating strong potential differences in persistence of these populations.
This is the first study on complete population dynamics of plants of different ploidy levels. This knowledge will help to understand the ability of new ploidy levels to spread into new areas and persist there, and the interactions of different ploidy levels in secondary contact zones. This knowledge will also contribute to understanding of interactions of different ploidy levels with other plant species or other interacting organisms such as pollinators or herbivores.
PMCID: PMC2759246  PMID: 17881342
Asteraceae; co-existence; contact zone; evolution; growth rate; LTRE; matrix model; permutation test; polyploidy; seed production
14.  Direct and indirect selection on flowering time, water-use efficiency (WUE, δ 13C), and WUE plasticity to drought in Arabidopsis thaliana 
Ecology and Evolution  2014;4(23):4505-4521.
Flowering time and water-use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time, WUE, and WUE plasticity to drought in Arabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) Is WUE plasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions of A. thaliana grown in well-watered and season-ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment. WUE and flowering time were consistently positively genetically correlated. WUE was correlated with WUE plasticity, but the direction changed between treatments. Selection generally favored early flowering and low WUE, with drought favoring earlier flowering significantly more than well-watered conditions. Selection for lower WUE was marginally stronger under drought. There were no net fitness costs of WUE plasticity. WUE plasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation between WUE and flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions of A. thaliana. WUE plasticity may be favored over completely fixed development in environments with periodic drought.
PMCID: PMC4264900  PMID: 25512847
Arabidopsis thaliana; drought; flowering time; plasticity; selection; water-use efficiency
15.  Soil As Levels and Bioaccumulation in Suaeda salsa and Phragmites australis Wetlands of the Yellow River Estuary, China 
BioMed Research International  2015;2015:301898.
Little information is available on As contamination dynamics in the soil-plant systems of wetlands. Total arsenic (As) in soil and plant samples from Suaeda salsa and Phragmites australis wetlands was measured in the Yellow River Estuary (YRE) in summer and autumn of 2007 to investigate the seasonal changes in As concentrations in different wetlands. The results showed that soil As levels greatly exceeded the global and regional background values. As levels in soil and the roots and stems of both types of plants were much higher in summer than in autumn, whereas leaf As showed higher level in autumn. Soil sulfur was the main factor influencing As levels in Suaeda salsa wetlands, whereas soil porosity was the most important factor for Phragmites australis wetlands. The contamination factor (CF) showed moderately to considerably polluted levels of As in both wetland soils. Plant roots and leaves of Suaeda salsa had higher As concentrations and biological concentration factors (BCFs) than stems, while the leaves and stems of Phragmites australis showed higher As levels and BCFs than roots. Compared to Phragmites australis, Suaeda salsa generally showed higher translocation factor (TF), while TF values for both plant species were higher in summer than in autumn.
PMCID: PMC4317578
16.  Photosynthesis of co-existing Phragmites haplotypes in their non-native range: are characteristics determined by adaptations derived from their native origin? 
AoB Plants  2013;5:plt016.
Several Phragmites lineages differing in origin and phenotype co-exist in the Gulf Coast of North America. We collected rhizomes of four lineages and propagated them in a common environment to compare photosynthetic characteristics. We observed substantial differences among and within lineages. As the lineages originating in Africa and in the Mediterranean region had higher photosynthetic capacity than the lineages originating in Eurasia, and showed typical ecophysiological traits of plants adapted to warm and arid climates, we concluded that the differences observed are due to adaptations acquired in the native ranges. The four lineages can therefore be regarded as ecotypes.
The Gulf Coast of North America (GC) is a ‘hot spot’ of Phragmites diversity as several lineages (defined according to the haplotypes of their chloroplast DNA) differing in origin, genetic traits and phenotype co-exist and interbreed in this area. We analysed differences in photosynthetic characteristics among and within four haplotypes to understand if differences in gas exchange can be attributed to adaptations acquired in their native ranges. We collected rhizomes of four GC haplotypes (I2, M1, M and AI; including the phenotypes ‘Land-type’, ‘Delta-type’, ‘EU-type’ and ‘Greeny-type’) and propagated them in a common controlled environment to compare photosynthesis–irradiance responses, CO2 responses, chlorophyll fluorescence, the activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), specific leaf area (SLA), pigment contents, stomatal density and guard cell length. The maximum light-saturated photosynthetic rate, Amax, in the haplotype I2 (Land-type) and haplotype M1 (Delta-type) (34.3–36.1 µmol CO2 m−2 s−1) was higher than that in the invasive Eurasian haplotype M (22.4 ± 2.3 µmol CO2 m−2 s−1). The Amax of haplotype AI (Greeny3-type) was 29.1 ± 4.0 µmol CO2 m−2 s−1 and did not differ from the Amax of the other haplotypes. The carboxylation rate (Vcmax) and electron transport rate (Jmax) followed the same pattern as Amax. The haplotypes also differed in SLA (17.0–24.3 m2 kg−1 dry mass) and pigment content, whereas stomatal density and guard cell length, Rubisco activity and chlorophyll fluorescence did not differ significantly among haplotypes. The high photosynthetic activity and gas-exchange capacity of the two haplotypes originating in tropical Africa and the Mediterranean area (haplotypes I2 and M1) are apparently adaptations derived from their native ranges. Hence, the haplotypes can be regarded as ecotypes. However, it remains unclear how these differences relate to plant competitiveness and fitness in the GC of North America environment.
PMCID: PMC4104645
Adaptations; Gulf Coast of North America; genotypes; haplotypes; invasion; photosynthesis; Phragmites
17.  Effects of External Iron Concentration upon Seedling Growth and Uptake of Fe and Phosphate by the Common Reed, Phragmites australis (Cav.) Trin ex. Steudel 
Annals of Botany  2003;92(6):801-806.
The objectives of this study were to determine whether, and to what degree, the aqueous iron concentration in the growing medium affects the growth of, and Fe uptake by, Phragmites australis, and whether the presence of iron in the growing environment affects the uptake of the essential element phosphate. The wetland macrophyte P. australis was grown under laboratory conditions in nutrient solution (0·31 mg L–1 phosphate) containing a range of iron concentrations (0–50 mg L–1 Fe). A threshold of iron concentration (1 mg L–1) was found, above which growth of P. australis was significantly inhibited. No direct causal relationship between iron content in aerial tissues and growth inhibition was found, which strongly suggests that iron toxicity cannot explain these results. Phosphate concentrations in aerial tissues were consistently sufficient for growth and development (2–3 % d. wt) despite significant variation in concentration of phosphate associated with roots. External Fe concentration had a significant effect on the growth of P. australis and on both Fe and phosphate concentrations associated with roots. However, neither direct toxicity nor phosphate deficiency could explain the reduction in growth above 1 mg L–1 external Fe concentration
PMCID: PMC4243622  PMID: 14565939
Iron plaque; iron uptake; nutrient deficiency; phosphate; Phragmites australis; wetlands
18.  Understanding Plant-Microbe Interactions for Phytoremediation of Petroleum-Polluted Soil 
PLoS ONE  2011;6(3):e17961.
Plant-microbe interactions are considered to be important processes determining the efficiency of phytoremediation of petroleum pollution, however relatively little is known about how these interactions are influenced by petroleum pollution. In this experimental study using a microcosm approach, we examined how plant ecophysiological traits, soil nutrients and microbial activities were influenced by petroleum pollution in Phragmites australis, a phytoremediating species. Generally, petroleum pollution reduced plant performance, especially at early stages of plant growth. Petroleum had negative effects on the net accumulation of inorganic nitrogen from its organic forms (net nitrogen mineralization (NNM)) most likely by decreasing the inorganic nitrogen available to the plants in petroleum-polluted soils. However, abundant dissolved organic nitrogen (DON) was found in petroleum-polluted soil. In order to overcome initial deficiency of inorganic nitrogen, plants by dint of high colonization of arbuscular mycorrhizal fungi might absorb some DON for their growth in petroleum-polluted soils. In addition, through using a real-time polymerase chain reaction method, we quantified hydrocarbon-degrading bacterial traits based on their catabolic genes (i.e. alkB (alkane monooxygenase), nah (naphthalene dioxygenase) and tol (xylene monooxygenase) genes). This enumeration of target genes suggests that different hydrocarbon-degrading bacteria experienced different dynamic changes during phytoremediation and a greater abundance of alkB was detected during vegetative growth stages. Because phytoremediation of different components of petroleum is performed by different hydrocarbon-degrading bacteria, plants’ ability of phytoremediating different components might therefore vary during the plant life cycle. Phytoremediation might be most effective during the vegetative growth stages as greater abundances of hydrocarbon-degrading bacteria containing alkB and tol genes were observed at these stages. The information provided by this study enhances our understanding of the effects of petroleum pollution on plant-microbe interactions and the roles of these interactions in the phytoremediation of petroleum-polluted soil.
PMCID: PMC3060916  PMID: 21437257
19.  Multivariate genetic analysis of plant responses to water deficit and high temperature revealed contrasting adaptive strategies 
Journal of Experimental Botany  2014;65(22):6457-6469.
Plants need to control transpiration and photosynthesis tightly in order to grow under drought and high temperature. Contrasting genetic-by-environment interactions are exploited by Arabidopsis thaliana to improve stress tolerance.
How genetic factors control plant performance under stressful environmental conditions is a central question in ecology and for crop breeding. A multivariate framework was developed to examine the genetic architecture of performance-related traits in response to interacting environmental stresses. Ecophysiological and life history traits were quantified in the Arabidopsis thaliana Ler×Cvi mapping population exposed to constant soil water deficit and high air temperature. The plasticity of the genetic variance–covariance matrix (G-matrix) was examined using mixed-effects models after regression into principal components. Quantitative trait locus (QTL) analysis was performed on the predictors of genotype effects and genotype by environment interactions (G×E). Three QTLs previously identified for flowering time had antagonistic G×E effects on carbon acquisition and the other traits (phenology, growth, leaf morphology, and transpiration). This resulted in a size-dependent response of water use efficiency (WUE) to high temperature but not soil water deficit, indicating that most of the plasticity of carbon acquisition and WUE to temperature is controlled by the loci that control variation of development, size, growth, and transpiration. A fourth QTL, MSAT2.22, controlled the response of carbon acquisition to specific combinations of watering and temperature irrespective of plant size and development, growth, and transpiration rate, which resulted in size-independent plasticity of WUE. These findings highlight how the strategies to optimize plant performance may differ in response to water deficit and high temperature (or their combination), and how different G×E effects could be targeted to improve plant tolerance to these stresses.
PMCID: PMC4246181  PMID: 25246443
Antagonistic pleiotropy; Arabidopsis thaliana; genotype by environment interactions; G-matrix; mixed-effects model; photosynthesis; QTL; water use efficiency.
20.  Interactions among Plant Species and Microorganisms in Salt Marsh Sediments 
The interactions among Spartina patens and sediment microbial populations and the interactions among Phragmites australis and sediment microbial populations were studied at monotypic sites in Piermont Marsh, a salt marsh of the Hudson River north of New York, N.Y., at key times during the growing season. Arbuscular mycorrhizal fungi (AMF) effectively colonized S. patens but not P. australis, and there were seasonal increases and decreases that coincided with plant growth and senescence (17 and 6% of the S. patens root length were colonized, respectively). In sediment samples from the Spartina site, the microbial community and specific bacterial populations were at least twice as large in terms of number and biomass as the microbial community and specific bacterial populations in sediment samples from the Phragmites site, and peak values occurred during reproduction. Members of the domain Bacteria, especially members of the α-, γ-, and δ-subdivisions of the Proteobacteria, were the most abundant organisms at both sites throughout the growing season. The populations were generally more dynamic in samples from the Spartina site than in samples from the Phragmites site. No differences between the two sites and no differences during the growing season were observed when restriction fragment length polymorphism analyses of nifH amplicons were performed in an attempt to detect shifts in the diversity of nitrogen-fixing bacteria. Differences were observed only in the patterns generated by PCR or reverse transcription-PCR for samples from the Spartina site, suggesting that there were differences in the overall and active populations of nitrogen-fixing bacteria. Regression analyses indicated that there was a positive interaction between members of the δ-subdivision of the Proteobacteria and root biomass but not between members of the δ-subdivision of the Proteobacteria and macroorganic matter at both sites. In samples from the Spartina site, there were indications that there were bacterium-fungus interactions since populations of members of the α-subdivision of the Proteobacteria were negatively associated with AMF colonization and populations of members of the γ-subdivision of the Proteobacteria were positively associated with AMF colonization.
PMCID: PMC123761  PMID: 11872463
21.  Hurricane Activity and the Large-Scale Pattern of Spread of an Invasive Plant Species 
PLoS ONE  2014;9(5):e98478.
Disturbances are a primary facilitator of the growth and spread of invasive species. However, the effects of large-scale disturbances, such as hurricanes and tropical storms, on the broad geographic patterns of invasive species growth and spread have not been investigated. We used historical aerial imagery to determine the growth rate of invasive Phragmites australis patches in wetlands along the Atlantic and Gulf Coasts of the United States. These were relatively undisturbed wetlands where P. australis had room for unrestricted growth. Over the past several decades, invasive P. australis stands expanded in size by 6–35% per year. Based on tropical storm and hurricane activity over that same time period, we found that the frequency of hurricane-force winds explained 81% of the variation in P. australis growth over this broad geographic range. The expansion of P. australis stands was strongly and positively correlated with hurricane frequency. In light of the many climatic models that predict an increase in the frequency and intensity of hurricanes over the next century, these results suggest a strong link between climate change and species invasion and a challenging future ahead for the management of invasive species.
PMCID: PMC4039472  PMID: 24878928
22.  Effects of Spartina alterniflora invasion on the communities of methanogens and sulfate-reducing bacteria in estuarine marsh sediments 
The effect of plant invasion on the microorganisms of soil sediments is very important for estuary ecology. The community structures of methanogens and sulfate-reducing bacteria (SRB) as a function of Spartina alterniflora invasion in Phragmites australis-vegetated sediments of the Dongtan wetland in the Yangtze River estuary, China, were investigated using 454 pyrosequencing and quantitative real-time PCR (qPCR) of the methyl coenzyme M reductase A (mcrA) and dissimilatory sulfite-reductase (dsrB) genes. Sediment samples were collected from two replicate locations, and each location included three sampling stands each covered by monocultures of P. australis, S. alterniflora and both plants (transition stands), respectively. qPCR analysis revealed higher copy numbers of mcrA genes in sediments from S. alterniflora stands than P. australis stands (5- and 7.5-fold more in the spring and summer, respectively), which is consistent with the higher methane flux rates measured in the S. alterniflora stands (up to 8.01 ± 5.61 mg m−2 h−1). Similar trends were observed for SRB, and they were up to two orders of magnitude higher than the methanogens. Diversity indices indicated a lower diversity of methanogens in the S. alterniflora stands than the P. australis stands. In contrast, insignificant variations were observed in the diversity of SRB with the invasion. Although Methanomicrobiales and Methanococcales, the hydrogenotrophic methanogens, dominated in the salt marsh, Methanomicrobiales displayed a slight increase with the invasion and growth of S. alterniflora, whereas the later responded differently. Methanosarcina, the metabolically diverse methanogens, did not vary with the invasion of, but Methanosaeta, the exclusive acetate utilizers, appeared to increase with S. alterniflora invasion. In SRB, sequences closely related to the families Desulfobacteraceae and Desulfobulbaceae dominated in the salt marsh, although they displayed minimal changes with the S. alterniflora invasion. Approximately 11.3 ± 5.1% of the dsrB gene sequences formed a novel cluster that was reduced upon the invasion. The results showed that in the sediments of tidal salt marsh where S. alterniflora displaced P. australis, the abundances of methanogens and SRB increased, but the community composition of methanogens appeared to be influenced more than did the SRB.
PMCID: PMC3750361  PMID: 23986751
dissimilatory sulfite reductase B (dsrB); methyl coenzyme M reductase A (mcrA); spartina alterniflora; phragmites australis; estuarine marsh
23.  Phragmites australis root secreted phytotoxin undergoes photo-degradation to execute severe phytotoxicity 
Plant Signaling & Behavior  2009;4(6):506-513.
Our study organism, Phragmites australis (common reed), is a unique invader in that both native and introduced lineages are found coexisting in North America. This allows one to make direct assessments of physiological differences between these different subspecies and examine how this relates to invasiveness. Recent efforts to understand plant invasive behavior show that some invasive plants secrete a phytotoxin to ward-off encroachment by neighboring plants (allelopathy) and thus provide the invaders with a competitive edge in a given habitat. Here we show that a varying climatic factor like ultraviolet (UV) light leads to photo-degradation of secreted phytotoxin (gallic acid) in P. australis rhizosphere inducing higher mortality of susceptible seedlings. The photo-degraded product of gallic acid (hereafter GA), identified as mesoxalic acid (hereafter MOA), triggered a similar cell death cascade in susceptible seedlings as observed previously with GA. Further, we detected the biological concentrations of MOA in the natural stands of exotic and native P. australis. Our studies also show that the UV degradation of GA is facilitated at an alkaline pH, suggesting that the natural habitat of P. australis may facilitate the photo-degradation of GA. The study highlights the persistence of the photo-degraded phytotoxin in the P. australis's rhizosphere and its inhibitory effects against the native plants.
PMCID: PMC2688296  PMID: 19816146
ultraviolet; gallic acid; mesoxalic acid; novel weapons; invasive species; Phragmites australis
24.  Ancient Evolutionary Trade-Offs between Yeast Ploidy States 
PLoS Genetics  2013;9(3):e1003388.
The number of chromosome sets contained within the nucleus of eukaryotic organisms is a fundamental yet evolutionarily poorly characterized genetic variable of life. Here, we mapped the impact of ploidy on the mitotic fitness of baker's yeast and its never domesticated relative Saccharomyces paradoxus across wide swaths of their natural genotypic and phenotypic space. Surprisingly, environment-specific influences of ploidy on reproduction were found to be the rule rather than the exception. These ploidy–environment interactions were well conserved across the 2 billion generations separating the two species, suggesting that they are the products of strong selection. Previous hypotheses of generalizable advantages of haploidy or diploidy in ecological contexts imposing nutrient restriction, toxin exposure, and elevated mutational loads were rejected in favor of more fine-grained models of the interplay between ecology and ploidy. On a molecular level, cell size and mating type locus composition had equal, but limited, explanatory power, each explaining 12.5%–17% of ploidy–environment interactions. The mechanism of the cell size–based superior reproductive efficiency of haploids during Li+ exposure was traced to the Li+ exporter ENA. Removal of the Ena transporters, forcing dependence on the Nha1 extrusion system, completely altered the effects of ploidy on Li+ tolerance and evoked a strong diploid superiority, demonstrating how genetic variation at a single locus can completely reverse the relative merits of haploidy and diploidy. Taken together, our findings unmasked a dynamic interplay between ploidy and ecology that was of unpredicted evolutionary importance and had multiple molecular roots.
Author Summary
Organisms vary in the number of chromosome sets contained within the nucleus of each cell, but neither the reasons nor the consequences of this variation are well understood. We designed yeasts that differed in the number of chromosome sets but were otherwise identical and mapped the consequences of such ploidy variations during exposure to a large palette of environments. Contrary to commonly held assumptions, we found ploidy effects on the mitotic reproductive capacity of yeast to be the rule rather than the exception and to be highly evolutionarily conserved. Furthermore, our data rejected previously contemplated hypotheses of generalizable advantages of haploidy or diploidy when cells face nutrient starvation or are exposed to toxins or increased mutation rates. We also mapped the molecular processes mediating ploidy–environment interactions, showing that cell size and mating type locus composition had equal explanatory power. Finally we show that ploidy effects can be mechanistically very subtle, as a designed shift from one plasma membrane Li+ transporter to another completely altered the relative merits of having one or two chromosome sets when exposed to high Li+ concentrations. This complex and dynamic interplay between the number of chromosomes sets and the fluctuating environment must be taken into account when considering organismal form and behavior.
PMCID: PMC3605057  PMID: 23555297
25.  Ecosystem services of Phragmites in North America with emphasis on habitat functions 
AoB Plants  2013;5:plt008.
In North America, Phragmites australis (common reed) has generally been regarded as a weed to be controlled. This paper shows that Phragmites-dominated vegetation provides important non-habitat ecosystem services (e.g., carbon sequestration, water quality maintenance) in proportion to its biomass, and many habitat functions for other organisms that vary depending on characteristics of the vegetation and surrounding landscape. Phragmites has both detrimental and beneficial functions; therefore decision-makers must clarify their management goals and understand the local situation. Extensive dense Phragmites may be managed to optimize ecosystem services by partial removal of biomass for a bioenergy feedstock.
Phragmites australis (common reed) is widespread in North America, with native and non-native haplotypes. Many ecologists and wetland managers have considered P. australis a weed with little value to the native biota or human society. I document important ecosystem services of Phragmites including support for many common and rare species of plants and animals. This paper is based on an extensive review of the ecology and natural history literature, discussions with field workers, and observations in 13 US states and one Canadian province during the past 40 years. Phragmites sequesters nutrients, heavy metals and carbon, builds and stabilizes soils, and creates self-maintaining vegetation in urban and industrial areas where many plants do not thrive. These non-habitat ecosystem services are proportional to biomass and productivity. Phragmites was widely used by Native Americans for many purposes; the most important current direct use is for the treatment of wastes. Most of the knowledge of non-habitat ecosystem services is based on studies of P. australis haplotype M (an Old World haplotype). Phragmites also has habitat functions for many organisms. These functions depend on the characteristics of the landscape, habitat, Phragmites stand, species using Phragmites and life history element. The functions that Phragmites provides for many species are optimal at lower levels of Phragmites biomass and extent of stands. Old World Phragmites, contrary to many published statements, as well as North American native Phragmites, provide valuable ecosystem services including products for human use and habitat functions for other organisms. Phragmites stands may need management (e.g. thinning, fragmentation, containment or removal) to create or maintain suitable habitat for desired species of animals and plants.
PMCID: PMC4104640
Bio-energy; ecosystem services; habitat functions; invasive plants; management; methodology; non-native species; Phragmites

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