Unravelling plant responses to rising atmospheric CO2 concentration (CO2) has largely focussed on plastic functional attributes to single generation CO2 exposure. Quantifying the consequences of ...long‐term, decadal multigenerational exposure to elevated CO2 and the genetic changes that may underpin evolutionary mechanisms with CO2 as a driver remain largely unexplored. Here, we investigated both plastic and evolutionary plant responses to elevated CO2 by applying multi‐omic technologies using populations of Plantago lanceolata L., grown in naturally high CO2 for many generations in a CO2 spring. Seed from populations at the CO2 spring and an adjacent control site (ambient CO2) were grown in a common environment for one generation, and then offspring were grown in ambient or elevated CO2 growth chambers. Low overall genetic differentiation between the CO2 spring and control site populations was found, with evidence of weak selection in exons. We identified evolutionary divergence in the DNA methylation profiles of populations derived from the spring relative to the control population, providing the first evidence that plant methylomes may respond to elevated CO2 over multiple generations. In contrast, growth at elevated CO2 for a single generation induced limited methylome remodelling (an order of magnitude fewer differential methylation events than observed between populations), although some of this appeared to be stably transgenerationally inherited. In all, 59 regions of the genome were identified where transcripts exhibiting differential expression (associated with single generation or long‐term natural exposure to elevated CO2) co‐located with sites of differential methylation or with single nucleotide polymorphisms exhibiting significant inter‐population divergence. This included genes in pathways known to respond to elevated CO2, such as nitrogen use efficiency and stomatal patterning. This study provides the first indication that DNA methylation may contribute to plant adaptation to future atmospheric CO2 and identifies several areas of the genome that are targets for future study.
The response of plants to multigenerational elevated atmospheric CO2 exposure is poorly understood, and vitally needed to predict the consequences of climate change. Plants growing in naturally elevated CO2 spring sites provide a resource to investigate the plastic and evolutionary response to elevated CO2. Combining genomic, methylomic and transcriptomic datasets derived from a crossed factored experiment, we provide critical novel insight into the mechanisms coordinating the multigenerational response, highlighting the potential roles for both DNA methylation and genetic variation in facilitating plant adaptation.
There is a limited understanding of the importance of abiotic factors in regulating biodiversity and structure of many functionally important soil microbial communities. In this paper we present a ...molecular characterisation of archaeal and bacterial communities, exposed to long-term change in soil abiotic environment at natural CO2 springs (mofettes), using T-RFLP profiling and examination of 16S rRNA clone libraries. Our results show major shifts in archaeal and bacterial communities towards anaerobic and methanogenic taxa dominating in CO2 rich hypoxic soils with a significant increase in abundance of Methanomicrobia and predominantly anaerobic Chloroflexi and Firmicutes. O2 concentration in soil was consistently shown to be the strongest predictor of the compositional changes across both the archaeal and bacterial communities. However, soil pH and total N, were most important in separating the archaeal communities in transition and control zones, but not the bacterial communities. We conclude that geological CO2 induced hypoxia in mofette systems can cause major shifts in community composition of soil microbes that can generate significant implications for ecosystem functioning (e.g. nutrient cycling and CH4 production). Our data indicate that mofettes offer a good model system for studying the response of natural microbial communities to long-term environmental changes, which is urgently needed to address the bias towards macro-organisms in soil biodiversity research.
•Mofettes (natural CO2 springs) provide long-term stable changes in abiotic factors.•Soil archaeal and bacterial community composition is affected by CO2 and hypoxia.•O2 is the strongest predictor influencing location specific community composition.•Hypoxic soils have higher abundance of methanogenic and anaerobic microbes.
Long-term exposure to elevated CO₂ concentration will affect the traits of wild plants in association with other environmental factors. We investigated multiple effects of atmospheric CO₂ ...concentration, irradiance, and soil N availability on the leaf photosynthetic traits of a herbaceous species, Polygonum sachalinense, growing around natural CO₂ springs in northern Japan. Atmospheric CO₂ concentration and its interaction with irradiance and soil N availability affected several leaf traits. Leaf mass per unit area increased and N per mass decreased with increasing CO₂ and irradiance. Leaf N per area increased with increasing soil N availability at higher CO₂ concentrations. The photosynthetic rate under growth CO₂ conditions increased with increasing irradiance and CO₂, and with increasing soil N at higher CO₂ concentrations. The maximal velocity of ribulose 1,5-bisphosphate carboxylation (V cmax) was affected by the interaction of CO₂ and soil N, suggesting that down-regulation of photosynthesis at elevated CO₂ was more evident at lower soil N availability. The ratio of the maximum rate of electron transport to V cmax (J max/V cmax) increased with increasing CO₂, suggesting that the plants used N efficiently for photosynthesis at high CO₂ concentrations by changes in N partitioning. To what extent elevated CO₂ influenced plant traits depended on other environmental factors. As wild plants are subject to a wide range of light and nutrient availability, our results highlight the importance of these environmental factors when the effects of elevated CO₂ on plants are evaluated.
Ring widths of five Mediterranean forest tree species (Arbutus unedo, Fraxinus ornus, Quercus cerris, Quercus ilex
and Quercus pubescens) growing close to a natural source of CO2 in Tuscany, Italy ...and at a nearby control site were
compared. At the CO2-enriched site, trees have been growing for decades under elevated CO2 concentrations.
They originated from parent trees that also grew under elevated CO2 in natural conditions, and they have been
continuously exposed to elevated CO2 throughout their growth. Tree-ring series from each of the species were
prepared. Assigning calendar dates to rings was difficult but possible, and ring-width series were built for all
species. The ring-width data were analysed using a two-sided t-test to assess if there was a difference between the
radial growth at the CO2-enriched site and the control site. The cumulative basal area at the same cambial age at
both sites was also compared using a Wilcoxon test. Radial growth of trees at the CO2-enriched site was not
significantly different from growth at the control site. For each species, year by year, radial growth at the CO2-enriched site was tested against the control site and significant differences were found in only a few years; these
differences were not synchronous with extreme climatic events. The expected increase in above-ground
productivity, as one of the ecosystem responses to increasing CO2 during drought stress, was not observed in this
Mediterranean woody plant community, despite being water-limited. Other resource limitations, such as low
nutrient availability (common in the Mediterranean region), may have counteracted the positive effect of elevated
CO2 under drought stress, or trees may have acclimated to the high CO2.
Annual variations in the water relations and stomatal response of Erica arborea, Myrtus communis and Juniperus communis occurring at a natural CO2 vent were analysed under Mediterranean field ...conditions. A distinct gradient of CO2concentration (CO2) exists between two sites near a natural CO2‐emitting vent, with higher CO2 (700 μmol mol−1) in the proximity of the CO2 spring. Plants at the CO2 spring site have been growing for generations at elevated CO2. At both sites, maximum leaf conductance was related to predawn shoot water potential. The effects of water deficits during the summer drought were severe. Leaf conductance and water potential recovered after major rainfalls in September to predrought values. Strong relationships between leaf conductance, predawn water potential, and leaf‐specific hydraulic resistance are consistent with the role of stomata in regulating plant water status. Considerable between‐species variation in sensitivity of water potentials and stomatal characters to elevated CO2 were observed. Common to all the shrubs were a reduction in leaf conductance and an increase in water potentials in response to elevated CO2. Elevated CO2 decreased the sensitivity of leaf conductance to vapour pressure deficit. Morphological characters (including stomatal density and degree of sclerophylly) showed site‐dependent variations, but degree and sign of such changes varied with the species and/or the season. Measurements of discrimination against 13C provided evidence for long‐term decreases of water use efficiency in CO2 spring plants. Analysis of C isotope composition suggested that a downward adjustment of photosynthetic capacity may have occurred under elevated CO2. Elevated CO2 effects on water relations and leaf morphology persisted in the long term, but the three shrubs growing in the same environment showed species‐specific responses.
Natural CO2 springs (mofettes) represent extreme ecosystems with severe exhalations of ambient temperature geological CO2, inducing long-term soil hypoxia. In this paper an overview of mofette ...research in the fields of microbial ecology and biodiversity in presented, with a focus on the studies describing the impact of the changed soil gas regime on communities of arbuscular mycorrhizal fungi, archaea and bacteria. Along with the fast development of new, highthroughput molecular techniques driving the field of molecular ecology, mofettes enable new insights into the importance of the abiotic environmental factors in regulating soil biodiversity, and the community structure of these functionally important microbial groups.
Variations in the water relations and stomatal response of Quercus ilex were analysed under field conditions by comparing trees at two locations in a Mediterranean environment during two consecutive ...summers (1993 and 1994). We used the heat‐pulse velocity technique to estimate transpirational water use of trees during a 5 month period from June to November 1994. At the end of sap flow measurements, the trees were harvested, and the foliage and sapwood area measured. A distinct environmental gradient exists between the two sites with higher atmospheric CO2 concentrations in the proximity of a natural CO2 spring. Trees at the spring site have been growing for generations in elevated atmospheric CO2 concentrations. At both sites, maximum leaf conductance was related to predawn shoot water potential. The effects of water deficits on water relations and whole‐plant transpiration during the summer drought were severe. Leaf conductance and water potential recovered after major rainfall in September to predrought values. Sap flow, leaf conductance and predawn water potential decreased in parallel with increases in hydraulic resistance, reaching a minimum in mid‐summer. These relationships are in agreement with the hypothesis of the stomatal control of transpiration to prevent desiccation damage but also to avoid ‘runaway embolism’. Trees at the CO2 spring underwent less reduction in hydraulic resistance for a given value of predawn water potential. The decrease in leaf conductance caused by elevated CO2 was limited and tended to be less at high than at low atmospheric vapour pressure deficit. Mean (and diurnal) sap flux were consistently higher in the control site trees than in the CO2 spring trees. The degree of reduction in water use between the two sites varied among the summer periods. The control site trees had consistently higher sap flow at corresponding values of either sapwood cross‐sectional area or foliage area. Larger trees displayed smaller differences than smaller trees, between the control and the CO2 spring trees. A strong association between foliage area and sapwood cross‐sectional area was found in both the control and the CO2 spring trees, the latter supporting a smaller foliage area at the corresponding sapwood stem cross‐sectional area. The specific leaf area (SLA) of the foliage was not influenced by site. The results are discussed in terms of the effects of elevated CO2 on plant water use at the organ and whole‐tree scale.
Ammonia oxidising bacteria (AOB) are important soil microorganisms that carry out the first step in nitrification, the oxidation of ammonia to nitrite. In this paper we investigated the impact of ...long-term elevated CO₂ on soil nitrification and soil AOB community composition. Soil samples were taken from Hakanoa natural CO₂ springs, Kamo, Northland, New Zealand. This site has been exposed to elevated CO₂ for several decades. Soils were collected from different points near to CO₂-emitting vents where the CO₂ concentration at canopy height had been characterised. Nitrification activity was measured using a short-term nitrification assay, and AOB community composition was characterised using polymerase chain reaction and denaturing gradient gel electrophoresis (DGGE). A principal component analysis of the DGGE banding pattern was carried out to identify the effect of CO₂ on AOB community composition. Soil nitrification activity was markedly decreased with increasing CO₂. The variation in DGGE banding patterns revealed differences in the composition of the soil AOB community that were related to CO₂ concentration. Principal component analysis showed that the changes in community composition and nitrifying activity were linked and that these changes were related to atmospheric CO₂ concentration.
Stomatal density (SD) and stomatal conductance (gs) can be affected by an increase of atmospheric CO2 concentration. This study was conducted on 17 species growing in a naturally enriched CO2 spring ...and belonging to three plant communities. Stomatal conductance, stomatal density and stomatal index (SI) of plants from the spring, which were assumed to have been exposed for generations to elevated CO2, and of plants of the same species collected in a nearby control site, were compared. Stomatal conductance was significantly lower in most of the species collected in the CO2 spring and this indicated that CO2 effects on gs are not of a transitory nature but persist in the long term and through plant generations. Such a decrease was, however, not associated with changes in the anatomy of leaves: SD was unaffected in the majority of species (the decrease was only significant in three out of the 17 species examined), and also SI values did not vary between the two sites with the exception of two species that showed increased SI in plants grown in the CO2‐enriched area. These results did not support the hypothesis that long‐term exposure to elevated CO2 may cause adaptive modification in stomatal number and in their distribution.
ABSTRACT
Seasonal changes in tissue water relations of Erica arborea L., Myrtus communis L. and Juniperus communis L., grown in a Mediterranean environment, were analysed under field conditions over ...a 12 month period by comparing plants grown in the proximity of a natural CO2 spring (about 700 μmol mol−1 atmospheric CO2 concentration, CO2) with plants in ambient conditions. Tissue water relations varied in response to changes in water availability, but the seasonal course of tissue water relations parameters was also related to ontogeny. Tissue water relations of these co‐occurring shrubs were not alike. Osmotic potentials and saturated mass/dry mass ratio were lowest during peak drought stress periods. Diurnal changes in osmotic potential at the point of turgor loss were least early in the season, maximal in mid‐season, and decreased again in autumn. Turgor potentials decreased as drought progressed and were highest in late fall and mid‐winter. Symplastic water fraction was highest in mid‐spring for E. arborea and M. communis and decreased during the summer, while the opposite was observed for J. communis. Common to all species, under elevated CO2, was an increase of turgor pressure, particularly during the summer months. Other parameters showed species‐specific responses to long‐term elevated CO2. In particular, exposure to elevated CO2 increased osmotic potentials in E. arborea under drought, while the opposite was the case for J. communis. Site differences in predawn to midday shifts were not strong in any of the species. Differences in tissue water relations suggest that the coexistence of these shrubs in the same environment with similar water availability are partially based on differential water relations strategies and water use patterns. Regardless of the mechanisms, growth of these shrubs in elevated CO2 may be either less, similarly or more affected by drought stress than plants in ambient CO2 depending on the species and season.
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