The ongoing climate change is characterized by increased temperatures and altered precipitation patterns. In addition, there has been an increase in both the frequency and intensity of extreme climatic events such as drought. Episodes of drought induce a series of interconnected effects, all of which have the potential to alter the carbon balance of forest ecosystems profoundly at different scales of plant organization and ecosystem functioning. During recent years, considerable progress has been made in the understanding of how aboveground parts of trees respond to drought and how these responses affect carbon assimilation. In contrast, processes of belowground parts are relatively underrepresented in research on climate change. In this review, we describe current knowledge about responses of tree roots to drought. Tree roots are capable of responding to drought through a variety of strategies that enable them to avoid and tolerate stress. Responses include root biomass adjustments, anatomical alterations, and physiological acclimations. The molecular mechanisms underlying these responses are characterized to some extent, and involve stress signaling and the induction of numerous genes, leading to the activation of tolerance pathways. In addition, mycorrhizas seem to play important protective roles. The current knowledge compiled in this review supports the view that tree roots are well equipped to withstand drought situations and maintain morphological and physiological functions as long as possible. Further, the reviewed literature demonstrates the important role of tree roots in the functioning of forest ecosystems and highlights the need for more research in this emerging field.
The impact of climate change on the soil microbiome potentially alters the biogeochemical cycle of terrestrial ecosystems. In semi-arid environments, water availability is a major constraint on biogeochemical cycles due to the combination of high summer temperatures and low rainfall. Here, we explored how 10 years of irrigation of a water-limited pine forest in the central European Alps altered the soil microbiome and associated ecosystem functioning. A decade of irrigation stimulated tree growth, resulting in higher crown cover, larger yearly increments of tree biomass, increased litter fall and greater root biomass. Greater amounts of plant-derived inputs associated with increased primary production in the irrigated forest stands stimulated soil microbial activity coupled with pronounced shifts in the microbiome from largely oligotrophic to more copiotrophic lifestyles. Microbial groups benefitting from increased resource availabilities (litter, rhizodeposits) thrived under irrigation, leading to enhanced soil organic matter mineralization and carbon respired from irrigated soils. This unique long-term study provides new insights into the impact of precipitation changes on the soil microbiome and associated ecosystem functioning in a water-limited pine forest ecosystem and improves our understanding of the persistency of long-term soil carbon stocks in a changing climate.
Scots pines (Pinus sylvestris L.) in the inner-Alpine dry valleys of Switzerland have suffered from increased mortality during the past decades, which has been caused by longer and more frequent dry periods. In addition, a proceeding replacement of Scots pines by pubescent oaks (Quercus pubescens Willd.) has been observed. In 2003, an irrigation experiment was performed to track changes by reducing drought pressure on the natural pine forest. After nine years of irrigation, we observed major adaptations in the vegetation and shifts in Scots pine fine root abundance and structure. Irrigation permitted new plant species to assemble and promote canopy closure with a subsequent loss of herb and moss coverage. Fine root dry weight increased under irrigation and fine roots had a tendency to elongate. Structural composition of fine roots remained unaffected by irrigation, expressing preserved proportions of cellulose, lignin and phenolic substances. A shift to a more negative δ13C signal in the fine root C indicates an increased photosynthetic activity in irrigated pine trees. Using radiocarbon (14C) measurement, a reduced mean age of the fine roots in irrigated plots was revealed. The reason for this is either an increase in newly produced fine roots, supported by the increase in fine root biomass, or a reduced lifespan of fine roots which corresponds to an enhanced turnover rate. Overall, the responses belowground to irrigation are less conspicuous than the more rapid adaptations aboveground. Lagged and conservative adaptations of tree roots with decadal lifespans are challenging to detect, hence demanding for long-term surveys. Investigations concerning fine root turnover rate and degradation processes under a changing climate are crucial for a complete understanding of C cycling.
Decomposition is a major flux of the carbon cycle in forest soils and understanding the involved processes is a key for budgeting carbon turnover. Decomposition is constrained by the presence of biological agents such as microorganisms and the underlying environmental conditions such as water availability. A metabarcoding approach of ribosomal markers was chosen to study the succession of bacterial and fungal decomposers on root litter. Litterbags containing pine roots were buried in a pine forest for two years and sequentially sampled. Decomposition and the associated communities were surveyed under ambient dry and long-term irrigation conditions. Early decomposition stages were characterized by the presence of fast-cycling microorganisms such as Bacteroidetes and Helotiales, which were then replaced by more specialized bacteria and litter-associated or parasitic groups such as Acidobacteria, white rots, and Pleosporales. This succession was likely driven by a decrease of easily degradable carbohydrates and a relative increase in persistent compounds such as lignin. We hypothesize that functional redundancy among the resident microbial taxa caused similar root decomposition rates in control and irrigated forest soils. These findings have important implications for drought-prone Alpine forests as frequent drought events reduce litter fall, but not litter decomposition, potentially resulting in lower carbon stocks.
Trait-based approaches are increasingly used to investigate plant strategies for resource acquisition, growth, or competition between individual organisms or across species. However, the characterization of responses to environmental stimuli by fine-root systems of trees at the trait level is rather limited, particularly regarding the timing and degree of plasticity of the traits involved. These aspects become especially relevant under current climate-driven shifts in environmental conditions. In the present study, we examined the responses of the fine roots of Scots pines to increased soil water availability from long-term irrigation starting in the year 2003. The Scots pine forest is situated in a water-limited region in the central European Alps where increased tree mortality has been observed over the last two decades. The fine-root traits investigated include root system traits, root dynamic traits, architectural traits, and morphological traits. A first survey of fine-root traits in 2005 using ingrowth cores did not reveal any trait-based responses resulting from the irrigation treatment over a three-year period. Fine-root biomass, as periodically recorded by coring the topsoil from 2003 to 2016, showed a significant increase compared to the non-irrigated controls between three and nine years after the start of treatment. Overall, a maximum biomass increase due to the irrigation treatment was recorded in 2016 with about 80% higher biomass compared to controls. The analysis of fine-root traits revealed that irrigation significantly increased biomass, length, and production, but did not alter morphological and architectural traits, such as diameter, frequency of tips, specific root length (SRL), and root tissue density (RTD). In contrast, clear significant differences were found for all traits except for length when comparing the two root sampling methods, namely, ingrowth cores and soil coring. However, there were no interactions between the irrigation treatment and the sampling methods used and, therefore, the methods used did not affect the documented patterns, just the actual measured trait values.
Fine roots support the water and nutrient demands of plants and supply carbon to soils. Quantifying turnover times of fine roots is crucial for modeling soil organic matter dynamics and constraining carbon cycle–climate feedbacks. Here we challenge widely used isotope-based estimates suggesting the turnover of fine roots of trees to be as slow as a decade. By recording annual growth rings of roots from woody plant species, we show that mean chronological ages of fine roots vary from <1 to 12 years in temperate, boreal and sub-arctic forests. Radiocarbon dating reveals the same roots to be constructed from 10 ± 1 year (mean ± 1 SE) older carbon. This dramatic difference provides evidence for a time lag between plant carbon assimilation and production of fine roots, most likely due to internal carbon storage. The high root turnover documented here implies greater carbon inputs into soils than previously thought which has wide-ranging implications for quantifying ecosystem carbon allocation.
The present study aimed to elucidate the influence of drought and elevated temperature on relative abundance and functioning of the ectomycorrhizal fungus Cenococcum geophilum on three oak species differing in adaptation to a warm and dry climate. The experiment QUERCO comprised three Quercus species (Q. robur, Q. petraea, Q. pubescens) grown for 3 years under four treatments: elevated air temperature, drought, a combination of the two, and control. Fine root samples were analysed for relative abundance and potential extracellular enzyme activities of ectomycorrhizae of C. geophilum, a fungal species known to be drought resistant. The relative abundance of C. geophilum on the roots of the oak species was significantly increased by temperature, decreased by drought, but unchanged in the combined treatment compared to the control. Although the extent of treatment effects differed among oak species, no significant influence of tree species on relative abundance of C. geophilum was detected. Exoenzyme activities of C. geophilum on Q. robur and Q. petraea (but not Q. pubescens) significantly increased in the combined treatment, but for all oak species were reduced under drought and air warming alone compared to the control. There was a significant negative correlation between abundance of C. geophilum and its leucine aminopeptidase activity. As this enzyme is not frequent among ectomycorrhizal fungi, this emphasises the functional importance of C. geophilum in the ectomycorrhizal community. Our results indicate that increased temperature and drought will influence the relative abundance and enzyme activity of C. geophilum. However, both the Quercus species and C. geophilum tolerated warming and strong drought.
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