Plant root exudation under drought Williams, Alex; de Vries, Franciska T.
New phytologist,
03/2020, Letnik:
225, Številka:
5
Journal Article
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Root exudates are a pathway for plant–microbial communication and play a key role in ecosystem response to environmental change. Here, we collate recent evidence that shows that plants of different ...growth strategies differ in their root exudation, that root exudates can select for beneficial soil microbial communities, and that drought affects the quantity and quality of root exudation. We use this evidence to argue for a central involvement of root exudates in plant and microbial response to drought and propose a framework for understanding how root exudates influence ecosystem form and function during and after drought. Specifically, we propose that fast-growing plants modify their root exudates to recruit beneficial microbes that facilitate their regrowth after drought, with cascading impacts on their abundance and ecosystem functioning. We identify outstanding questions and methodological challenges that need to be addressed to advance and solidify our comprehension of the importance of root exudates in ecosystem response to drought.
Interactions between aboveground and belowground biota have the potential to modify ecosystem responses to climate change, yet little is known about how drought influences plant–soil feedbacks with ...respect to microbial mediation of plant community dynamics.
We tested the hypothesis that drought modifies plant–soil feedback with consequences for plant competition. We measured net pairwise plant–soil feedbacks for two grassland plant species grown in monoculture and competition in soils that had or had not been subjected to a previous drought; these were then exposed to a subsequent drought. To investigate the mechanisms involved, we assessed treatment responses of soil microbial communities and nutrient availability.
We found that previous drought had a legacy effect on bacterial and fungal community composition that decreased plant growth in conspecific soils and had knock-on effects for plant competitive interactions. Moreover, plant and microbial responses to subsequent drought were dependent on a legacy effect of the previous drought on plant–soil interactions.
We show that drought has lasting effects on belowground communities with consequences for plant–soil feedbacks and plant–plant interactions. This suggests that drought, which is predicted to increase in frequency with climate change, may change soil functioning and plant community composition via the modification of plant–soil feedbacks.
Root-associated microbes can improve plant growth, and they offer the potential to increase crop resilience to future drought. Although our understanding of the complex feedbacks between plant and ...microbial responses to drought is advancing, most of our knowledge comes from non-crop plants in controlled experiments. We propose that future research efforts should attempt to quantify relationships between plant and microbial traits, explicitly focus on food crops, and include longer-term experiments under field conditions. Overall, we highlight the need for improved mechanistic understanding of the complex feedbacks between plants and microbes during, and particularly after, drought. This requires integrating ecology with plant, microbiome, and molecular approaches and is central to making crop production more resilient to our future climate.
Root exudates play an important role in ecosystem response to climate change, but the functional consequences of drought-induced changes in the quality of root exudates are unknown. Here, we ...addressed this knowledge gap in a unique experimental approach.
We subjected two common grassland species that differ widely in their growth strategies and root systems, the grass Holcus lanatus and the forb Rumex acetosa, to 2 wk of drought. We collected root exudates and soils at the end of the drought and after 2 wk of recovery and readded all root exudates to all soils in a fully reciprocal set-up to measure root-exudate-induced respiration.
We found that soil treatment was unimportant for determining root-exudate-induced respiration. By contrast, root exudates collected from plants that had experienced drought clearly triggered more soil respiration than exudates from undroughted plants. Importantly, this increased respiration compensated for the lower rates of root exudation in droughted plants.
Our findings reveal a novel mechanism through which drought can continue to affect ecosystem carbon cycling, and a potential plant strategy to facilitate regrowth through stimulating microbial activity. These findings have important implications for understanding plant and ecosystem response to drought.
Summary
Feedback between plants and soil microbial communities can be a powerful driver of vegetation dynamics. Plants elicit changes in the soil microbiome that either promote or suppress ...conspecifics at the same location, thereby regulating population density‐dependence and species co‐existence. Such effects are often attributed to the accumulation of host‐specific antagonistic or beneficial microbiota in the rhizosphere. However, the identity and host‐specificity of the microbial taxa involved are rarely empirically assessed. Here we review the evidence for host‐specificity in plant‐associated microbes and propose that specific plant–soil feedbacks can also be driven by generalists. We outline the potential mechanisms by which generalist microbial pathogens, mutualists and decomposers can generate differential effects on plant hosts and synthesize existing evidence to predict these effects as a function of plant investments into defence, microbial mutualists and dispersal. Importantly, the capacity of generalist microbiota to drive plant–soil feedbacks depends not only on the traits of individual plants but also on the phylogenetic and functional diversity of plant communities. Identifying factors that promote specialization or generalism in plant–microbial interactions and thereby modulate the impact of microbiota on plant performance will advance our understanding of the mechanisms underlying plant–soil feedback and the ways it contributes to plant co‐existence.
Soil microbial communities are intricately linked to ecosystem functioning because they play important roles in carbon and nitrogen cycling. Still, we know little about how soil microbial communities ...will be affected by disturbances expected with climate change. This is a significant gap in understanding, as the stability of microbial communities, defined as a community's ability to resist and recover from disturbances, likely has consequences for ecosystem function. Here, we propose a framework for predicting a community's response to climate change, based on specific functional traits present in the community, the relative dominance of r- and K-strategists, and the soil environment. We hypothesize that the relative abundance of r- and K-strategists will inform about a community's resistance and resilience to climate change associated disturbances. We also propose that other factors specific to soils, such as moisture content and the presence of plants, may enhance a community's resilience. For example, recent evidence suggests microbial grazers, resource availability, and plant roots each impact on microbial community stability. We explore these hypotheses by offering three vignettes of published data that we re-analyzed. Our results show that community measures of the relative abundance of r- and K-strategists, as well as environmental properties like resource availability and the abundance and diversity of higher trophic levels, can contribute to explaining the response of microbial community composition to climate change-related disturbances. However, further investigation and experimental validation is necessary to directly test these hypotheses across a wide range of soil ecosystems.
The controls on aboveground community composition and diversity have been extensively studied, but our understanding of the drivers of belowground microbial communities is relatively lacking, despite ...their importance for ecosystem functioning. In this study, we fitted statistical models to explain landscape‐scale variation in soil microbial community composition using data from 180 sites covering a broad range of grassland types, soil and climatic conditions in England. We found that variation in soil microbial communities was explained by abiotic factors like climate, pH and soil properties. Biotic factors, namely community‐weighted means (CWM) of plant functional traits, also explained variation in soil microbial communities. In particular, more bacterial‐dominated microbial communities were associated with exploitative plant traits versus fungal‐dominated communities with resource‐conservative traits, showing that plant functional traits and soil microbial communities are closely related at the landscape scale.
Background and Aims Root traits are increasingly used to predict how plants modify soil processes. Here, we assessed how drought-induced changes in root systems of four common grassland species ...affected C and N availability in soil. We hypothesized that drought would promote resource-conservative root traits such as high root tissue density (RTD) and low specific root length (SRL), and that these changes would result in higher soil N availability through decreased root N uptake, but lower C availability through reduced root exudation. Methods We subjected individual plants to drought under controlled conditions, and compared the response of their root biomass, root traits, and soil C and N availability, to control individuals. Results Drought affected most root traits through reducing root biomass. Only SRL and RTD displayed plasticity; drought reduced SRL, and increased RTD in small plants but decreased RTD in larger plants. Reduced root biomass and a shift towards more resource-conservative root traits increased soil inorganic N availability but did not directly affect soil C availability. Conclusions These findings identify mechanisms through which drought-induced changes in root systems affect soil C and N availability, and contribute to our understanding of how root traits modify soil processes in a changing world.
1. Healthy soils that contain an active microbiome and food web are critical to sustainably produce food for a growing global human population. Many studies have focussed on the role of microbial ...species diversity and the presence of key functional groups as important controls on the many functions that a sustainable food system relies on. 2. Here, we synthesise recent ecological empirical evidence and theory to propose that the interactions between organisms in the soil food web are the critical determinant of soil function. 3. We propose the Rhizosphere Interactions for Sustainable Agriculture Model, in which crop roots recruit small, modular, highly connected soil rhizosphere networks from large, static, relatively unconnected and diverse bulk soil networks. We argue that conventional agricultural management disrupts the connections between rhizosphere and bulk soil networks. 4. Synthesis. We identify future research directions for optimising ecological connections between roots and rhizosphere microbial and faunal networks, and between rhizosphere networks and bulk soil networks in agricultural production systems. Knowledge on these connections can be applied in agricultural systems to sustainability produce food for a growing global population.
Plant root exudation is a crucial means through which plants communicate with soil microbes and influence rhizosphere processes. Exudation can also underlie ecosystem response to changing ...environmental conditions. Different plant species vary in their root exudate quantity and quality, but our understanding of the plant characteristics that drive these differences is fragmentary. We hypothesised that root exudates would be under phylogenetic control and fit within an exploitative root nutrient uptake strategy, specifically that high rates of root exudation would link to root traits indicative of exploitative growth.
We collected root exudates from plants grown in field soil, as well as leachates of the entire plant–soil system, to assess both the quantity and quality of root exudates, and their interaction with the soil metabolome, across 18 common grassland species.
We found that exudation varied with plant functional group and that differences were trait dependent. Particularly, root diameter, root tissue density and root nitrogen content explained much of the variation in exudate metabolome, along with plant phylogeny. Specific root exudation rate was highest in forbs and was negatively correlated with root tissue density, a trait indicative of conservative resource‐use strategy, and positively correlated with root diameter, which is associated with microbial collaboration and resource uptake ‘outsourcing’.
Synthesis. We provide novel insight into species‐specific differences in root exudates and identify root functional traits that might underlie these differences. Our results show that root exudation fits, although not entirely, within current models of the root economic space, with strong positive relationships to outsourcing traits like high root diameter. Determining the role of root exudates as a key facet of the resource‐outsourcing strategy necessitates further research into the fundamental controls on root exudation quantity and quality, particularly during environmental change.
Our study shows that root exudates fit into the root economic spectrum and are associated with resource‐outsourcing traits: exudation rates increase with root diameter, decrease with root tissue density and operate under plant phylogenetic control. Metabolite composition of exudates is species specific, with some phylogenetic association. It is likely that quantity and composition operate together in conjunction with root trait syndromes to inform a rhizosphere microbial function consistent with the growth strategy of the plant. Greater consideration and characterisation of root exudates remain key to fully unravelling plant–microbe relationships and their role in plant environmental adaptation and survival.
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