Challenges in imaging and predictive modeling of rhizosphere processes

Background

Plant-soil interaction is central to human food production and ecosystem function. Thus, it is essential to not only understand, but also to develop predictive mathematical models which can be used to assess how climate and soil management practices will affect these interactions.

Scope

In this paper we review the current developments in structural and chemical imaging of rhizosphere processes within the context of multiscale mathematical image based modeling. We outline areas that need more research and areas which would benefit from more detailed understanding.

Conclusions

We conclude that the combination of structural and chemical imaging with modeling is an incredibly powerful tool which is fundamental for understanding how plant roots interact with soil. We emphasize the need for more researchers to be attracted to this area that is so fertile for future discoveries. Finally, model building must go hand in hand with experiments. In particular, there is a real need to integrate rhizosphere structural and chemical imaging with modeling for better understanding of the rhizosphere processes leading to models which explicitly account for pore scale processes.

     

Back to the basics: The need for ecophysiological insights to enhance our understanding of microbial behaviour in the rhizosphere

Background and Scope

Microorganisms exhibit an astonishing diversity and wide genetic variability even within species, in particular with respect to their metabolic pathways and host-interactive capabilities. The mosaic genomes that encode these capacities are accountable for the abilities of environmental microbes to survive and thrive in highly complex systems such as soil and the rhizosphere. Whereas credits are to be given to traditional microbiology studies, e.g. with rhizobia and their interaction with the plant, an explosive enhancement of our understanding of the plant-microorganism interactive system has been recently achieved by the broad application of the molecular toolbox, in particular high-throughput sequencing (HTS) technologies. The latter have allowed to access thousands to millions of microbial phylotypes and functions at relatively low cost and effort. While such techniques have improved the accessibility of the taxonomic and functional diversity of rhizosphere and soil microbial communities, detailed insights into organismal ecology and physiology (reflecting the behaviour of populations of cells) within the community in the natural environment are still required.

Conclusions

In this review, we first examine the current ‘state-of-the-art’ of rhizosphere ecology studies and what HTS strategies have added to our understanding of the system. We posit that our capacity to develop and test refined ecological hypotheses is hindered if we solely depend on deep-sequencing methods. Plant-soil-microorganism systems represent one of the most intriguing ‘playgrounds’ for assessments of ecological theories, since they offer a myriad of ways to investigate ecological interactions (i.e. intra- and inter-specifically), physiological and behavioural traits. In addition, the evolutionary processes that lead to innovation in the microbiota are likely prominent in the rhizosphere. Thus, there is a perceived need to shift our attention from the HTS studies, that extensively map the local microbiota in an overall fashion, to studies focusing on as-yet-unaddressed fundamental questions about the plant-soil microbiota system. Such a paradigm shift will certainly assist us in the unravelling of the building blocks of rhizosphere (and soil) microbial communities, as well as form a basis for targeted manipulation of these in their natural settings.     

Environmental Risk Management Decision-Making in a Societal Context

Recent studies point to the need for improved understanding of environmental management frameworks designed to combine qualitative public and quantitative technical inputs in decision-making processes. Flux in public perception and concern about risks imply frameworks must be iterative in nature and incorporate a variety of assessment triggers in the form of decision points. A conceptual model is proposed here to explain the de facto operation of standard risk analytic frameworks within the broader sociopolitical milieu of public policy. The model is presented as a decision flow diagram that emphasizes setting environmental management goals based on societal input and the formulation of decision criteria for selecting management actions to achieve those goals. Prospective and retrospective decision control points operate to select management options that, respectively, avoid or reduce actual or predicted effects. Feedback loops that modify risk management outcomes are identified. Technical and scientific inputs (i.e., risk analysis) are assigned an essential information role within the framework and are responsible for informing the management process with the results of appropriately conducted and reviewed investigations. The proposed model is intended primarily to indicate how environmental risk management decision-making and associated technical assessments may be influenced by social pressures. It is hoped this understanding will lead to analytical transparency and better public communication of the environmental implications of policy options.     

Phylofloristics: an example from the Lesser Antilles

Aims The last decade has seen many plant ecologists integrating phylogenetic analysis into ecology to explain patterns of species co-occurrence and compositional similarity across assemblages. Despite the advances in this area, there are still some challenges that need to be addressed. One challenge is that most of the phylogenetic studies of plant assemblages have focused only on a small proportion of all of the vascular plants that co-occur (e.g. woody plants), while much of the remaining co-occurring flora has been ignored.Methods Here we introduce an analytical approach that we term phylofloristics that analyzes the compositional similarity of floras in relation to spatial and environmental gradients to understand their assembly. As an illustration, we assembled a large phylogenetic tree for the flora of the Lesser Antilles and evaluated the patterns of floristic and phylofloristic similarity among the island-specific floras. We analyzed the relationship of these similarities with spatial and environmental distance and compared the results for non-endemic and endemic lineages.Important findings The results show a major influence of environmental heterogeneity on the assembly of island floras and far less evidence for the importance of dispersal limitation of lineages and species. This study highlights the importance of incorporating broader taxonomic sampling to improve our understanding of assembly processes in ecology. We expect future phylofloristic studies will improve the approach we have taken by generating more refined phylogenetic trees and by incorporating phylogeographic information.     

Arsenic transformations in the soil-rhizosphere-plant system: fundamentals and potential application to phytoremediation

This paper reviews major processes that potentially affect the fate of arsenic in the rhizosphere of plants. Rhizosphere interactions are deemed to play a key role in controlling bioavailability to crop plants and for a better understanding and improvement of phytoremediation technologies. Substantial progress has been made towards an understanding of As transformation processes in soils. However, virtually no information is available that directly addresses the fate of As in the rhizosphere. We are proposing a conceptual model of the fate of As in the soil-rhizosphere-plant system by integrating the state-of-the art knowledge available in the contributing disciplines. Using this model and recent studies on hyperaccumulation of As, we discuss research needs and the potential application of rhizosphere processes to the development of phytoremediation technologies for As-polluted soils.     

Contemplating the future: Acting now on long‐term monitoring to answer 2050's questions

In 2050, which aspects of ecosystem change will we regret not having measured? Long‐term monitoring plays a crucial part in managing Australia's natural environment because time is a key factor underpinning changes in ecosystems. It is critical to start measuring key attributes of ecosystems – and the human and natural process affecting them – now, so that we can track the trajectory of change over time. This will facilitate informed choices about how to manage ecological changes (including interventions where they are required) and promote better understanding by 2050 of how particular ecosystems have been shaped over time. There will be considerable value in building on existing long‐term monitoring programmes because this can add significantly to the temporal depth of information. The economic and social processes driving change in ecosystems are not identical in all ecosystems, so much of what is monitored (and the means by which it is monitored) will most likely target specific ecosystems or groups of ecosystems. To best understand the effects of ecosystem‐specific threats and drivers, monitoring also will need to address the economic and social factors underpinning ecosystem‐specific change. Therefore, robust assessments of the state of Australia's environment will be best achieved by reporting on the ecological performance of a representative sample of ecosystems over time. Political, policy and financial support to implement appropriate ecosystem‐specific monitoring is a perennial problem. We suggest that the value of ecological monitoring will be demonstrable, when plot‐based monitoring data make a unique and crucial contribution to Australia's ability to produce environmental accounts, environmental reports (e.g. the State of the Environment, State of the Forests) and to fulfilling reporting obligations under international agreements, such as the Convention on Biological Diversity. This paper suggests what must be done to meet Australia's ecological information needs by 2050.     

Corporate environmental performance,environmental information disclosure,and financial performance: Evidence from China

As pollution emitters and energy users, firms are important causes of environmental problems, making it increasingly vital for them to strengthen their environmental management and information disclosure policies. However, firms doubt whether it pays to be green and whether it is worthwhile to disclose their environmental information, and there are hot debates on these questions in the literature. This paper analyzes the relationships among corporate environmental performance, environmental information disclosure, and financial performance in China, which witnessed rapid growth at the price of environmental degradation. With 950 observations from 475 Chinese listed companies between 2013 and 2014, we find a U-shaped nonlinear relationship between corporate environmental performance and environmental disclosure, an insignificant relationship between environmental performance and financial performance, and a negative relationship between environmental disclosure and financial performance, which is different from most findings in developed countries. The aforementioned results imply that Chinese firms have few motivations to disclose environmental information or improve environmental performance; therefore, mandatory disclosure of environmental information is necessary, and proper environmental policy should be made to punish environmental violations and encourage better environmental performance.     

The big ecological questions inhibiting effective environmental management in Australia

The need to improve environmental management in Australia is urgent because human health, well‐being and social stability all depend ultimately on maintenance of life‐supporting ecological processes. Ecological science can inform this effort, but when issues are socially and economically complex the inclination is to wait for science to provide answers before acting. Increasingly, managers and policy‐makers will be called on to use the present state of scientific knowledge to supply reasonable inferences for action based on imperfect knowledge. Hence, one challenge is to use existing ecological knowledge more effectively; a second is to tackle the critical unanswered ecological questions. This paper identifies areas of environmental management that are profoundly hindered by an inability of science to answer basic questions, in contrast to those areas where knowledge is not the major barrier to policy development and management. Of the 22 big questions identified herein, more than half are directly related to climate change. Several of the questions concern our limited understanding of the dynamics of marine systems. There is enough information already available to develop effective policy and management to address several significant ecological issues. We urge ecologists to make better use of existing knowledge in dialogue with policy‐makers and land managers. Because the challenges are enormous, ecologists will increasingly be engaging a wide range of other disciplines to help identify pathways towards a sustainable future.     

Predicting Ecological Roles in the Rhizosphere Using Metabolome and Transportome Modeling

The ability to obtain complete genome sequences from bacteria in environmental samples, such as soil samples from the rhizosphere, has highlighted the microbial diversity and complexity of environmental communities. However, new algorithms to analyze genome sequence information in the context of community structure are needed to enhance our understanding of the specific ecological roles of these organisms in soil environments. We present a machine learning approach using sequenced Pseudomonad genomes coupled with outputs of metabolic and transportomic computational models for identifying the most predictive molecular mechanisms indicative of a Pseudomonad’s ecological role in the rhizosphere: a biofilm, biocontrol agent, promoter of plant growth, or plant pathogen. Computational predictions of ecological niche were highly accurate overall with models trained on transportomic model output being the most accurate (Leave One Out Validation F-scores between 0.82 and 0.89). The strongest predictive molecular mechanism features for rhizosphere ecological niche overlap with many previously reported analyses of Pseudomonad interactions in the rhizosphere, suggesting that this approach successfully informs a system-scale level understanding of how Pseudomonads sense and interact with their environments. The observation that an organism’s transportome is highly predictive of its ecological niche is a novel discovery and may have implications in our understanding microbial ecology. The framework developed here can be generalized to the analysis of any bacteria across a wide range of environments and ecological niches making this approach a powerful tool for providing insights into functional predictions from bacterial genomic data.     

Searching and mining visually observed phenotypes of maize mutants

There are thousands of maize mutants, which are invaluable resources for plant research. Geneticists use them to study underlying mechanisms of biochemistry, cell biology, cell development, and cell physiology. To streamline the understanding of such complex processes, researchers need the most current versions of genetic and physical maps, tools with the ability to recognize novel phenotypes or classify known phenotypes, and an intimate knowledge of the biochemical processes generating physiological and phenotypic effects. They must also know how all of these factors change and differ among species, diverse alleles, germplasms, and environmental conditions. While there are robust databases, such as MaizeGDB, for some of these types of raw data, other crucial components are missing. Moreover, the management of visually observed mutant phenotypes is still in its infant stage, let alone the complex query methods that can draw upon high-level and aggregated information to answer the questions of geneticists. In this paper, we address the scientific challenge and propose to develop a robust framework for managing the knowledge of visually observed phenotypes, mining the correlation of visual characteristics with genetic maps, and discovering the knowledge relating to cross-species conservation of visual and genetic patterns. The ultimate goal of this research is to allow a geneticist to submit phenotypic and genomic information on a mutant to a knowledge base and ask, "What genes or environmental factors cause this visually observed phenotype?".     

Ecosystem dynamics based on plankton functional types for global ocean biogeochemistry models

Ecosystem processes are important determinants of the biogeochemistry of the ocean, and they can be profoundly affected by changes in climate. Ocean models currently express ecosystem processes through empirically derived parameterizations that tightly link key geochemical tracers to ocean physics. The explicit inclusion of ecosystem processes in models will permit ecological changes to be taken into account, and will allow us to address several important questions, including the causes of observed glacial–interglacial changes in atmospheric trace gases and aerosols, and how the oceanic uptake of CO₂ is likely to change in the future. There is an urgent need to assess our mechanistic understanding of the environmental factors that exert control over marine ecosystems, and to represent their natural complexity based on theoretical understanding. We present a prototype design for a Dynamic Green Ocean Model (DGOM) based on the identification of (a) key plankton functional types that need to be simulated explicitly to capture important biogeochemical processes in the ocean; (b) key processes controlling the growth and mortality of these functional types and hence their interactions; and (c) sources of information necessary to parameterize each of these processes within a modeling framework. We also develop a strategy for model evaluation, based on simulation of both past and present mean state and variability, and identify potential sources of validation data for each. Finally, we present a DGOM-based strategy for addressing key questions in ocean biogeochemistry. This paper thus presents ongoing work in ocean biogeochemical modeling, which, it is hoped will motivate international collaborations to improve our understanding of the role of the ocean in the climate system.     

In silico tools for signal transduction research

Signal transduction is a fundamental process that takes place in all living organisms and understanding how this event occurs at the cellular level is of vital importance to virtually all fields of biomedicine. There are several major steps involved in deciphering the signalling pathways: (a) Which molecules are involved in signalling? (b) Who talks to whom?, ie making sense of the molecular interactions in a context-dependent way. (c) Where are the signalling events taking place?, eg when a resting cell becomes activated. The challenge lies in reconstructing signalling modules and networks evoked in a particular response to a single input as well as correlating the signalling response to different cellular inputs. There is also the need for interpretation of cross-talk between signalling modules in response to single and multiple inputs. To follow up these questions there are many good databases that provide an information system on regulatory networks. This review aims to find some of the bioinformatics tools and websites available to conduct signal transduction research and to discuss the representation of databases available for the processes of signalling. The databases considered here can provide a well-structured overview on the subject and a basis for advanced bioinformatics analysis to interpret the function of genomic sequences or to analyse signalling networks within a cell. However, the knowledge of most signalling pathways is incomplete and for this reason the existing databases will provide insight, but very rarely a more complete picture.     

The practice of prediction: What can ecologists learn from applied,ecology-related fields?

The pervasive influence of human induced global environmental change affects biodiversity across the globe, and there is great uncertainty as to how the biosphere will react on short and longer time scales. To adapt to what the future holds and to manage the impacts of global change, scientists need to predict the expected effects with some confidence and communicate these predictions to policy makers. However, recent reviews found that we currently lack a clear understanding of how predictable ecology is, with views seeing it as mostly unpredictable to potentially predictable, at least over short time frames. However, in applied, ecology-related fields predictions are more commonly formulated and reported, as well as evaluated in hindsight, potentially allowing one to define baselines of predictive proficiency in these fields. We searched the literature for representative case studies in these fields and collected information about modeling approaches, target variables of prediction, predictive proficiency achieved, as well as the availability of data to parameterize predictive models. We find that some fields such as epidemiology achieve high predictive proficiency, but even in the more predictive fields proficiency is evaluated in different ways. Both phenomenological and mechanistic approaches are used in most fields, but differences are often small, with no clear superiority of one approach over the other. Data availability is limiting in most fields, with long-term studies being rare and detailed data for parameterizing mechanistic models being in short supply. We suggest that ecologists adopt a more rigorous approach to report and assess predictive proficiency, and embrace the challenges of real world decision making to strengthen the practice of prediction in ecology.     

Rhizosphere: biophysics, biogeochemistry and ecological relevance

Life on Earth is sustained by a small volume of soil surrounding roots, called the rhizosphere. The soil is where most of the biodiversity on Earth exists, and the rhizosphere probably represents the most dynamic habitat on Earth; and certainly is the most important zone in terms of defining the quality and quantity of the Human terrestrial food resource. Despite its central importance to all life, we know very little about rhizosphere functioning, and have an extraordinary ignorance about how best we can manipulate it to our advantage. A major issue in research on rhizosphere processes is the intimate connection between the biology, physics and chemistry of the system which exhibits astonishing spatial and temporal heterogeneities. This review considers the unique biophysical and biogeochemical properties of the rhizosphere and draws some connections between them. Particular emphasis is put on how underlying processes affect rhizosphere ecology, to generate highly heterogeneous microenvironments. Rhizosphere ecology is driven by a combination of the physical architecture of the soil matrix, coupled with the spatial and temporal distribution of rhizodeposits, protons, gases, and the role of roots as sinks for water and nutrients. Consequences for plant growth and whole-system ecology are considered. The first sections address the physical architecture and soil strength of the rhizosphere, drawing their relationship with key functions such as the movement and storage of elements and water as well as the ability of roots to explore the soil and the definition of diverse habitats for soil microorganisms. The distribution of water and its accessibility in the rhizosphere is considered in detail, with a special emphasis on spatial and temporal dynamics and heterogeneities. The physical architecture and water content play a key role in determining the biogeochemical ambience of the rhizosphere, via their effect on partial pressures of O₂ and CO₂, and thereby on redox potential and pH of the rhizosphere, respectively. We address the various mechanisms by which roots and associated microorganisms alter these major drivers of soil biogeochemistry. Finally, we consider the distribution of nutrients, their accessibility in the rhizosphere, and their functional relevance for plant and microbial ecology. Gradients of nutrients in the rhizosphere, and their spatial patterns or temporal dynamics are discussed in the light of current knowledge of rhizosphere biophysics and biogeochemistry. Priorities for future research are identified as well as new methodological developments which might help to advance a comprehensive understanding of the co-occurring processes in the rhizosphere.     

How a growing organismal perspective is adding new depth to integrative studies of morphological evolution

Over the past half century, the field of Evolutionary Developmental Biology, or Evo‐devo, has integrated diverse fields of biology into a more synthetic understanding of morphological diversity. This has resulted in numerous insights into how development can evolve and reciprocally influence morphological evolution, as well as generated several novel theoretical areas. Although comparative by default, there remains a great gap in our understanding of adaptive morphological diversification and how developmental mechanisms influence the shape and pattern of phenotypic variation. Herein we highlight areas of research that are in the process of filling this void, and areas, if investigated more fully, that will add new insights into the diversification of morphology. At the centre of our discussion is an explicit awareness of organismal biology. Here we discuss an organismal framework that is supported by three distinct pillars. First, there is a need for Evo‐devo to adopt a high‐resolution phylogenetic approach in the study of morphological variation and its developmental underpinnings. Secondly, we propose that to understand the dynamic nature of morphological evolution, investigators need to give more explicit attention to the processes that generate evolutionarily relevant variation at the population level. Finally, we emphasize the need to address more thoroughly the processes that structure variation at micro‐ and macroevolutionary scales including modularity, morphological integration, constraint, and plasticity. We illustrate the power of these three pillars using numerous examples from both invertebrates and vertebrates to emphasize that many of these approaches are already present within the field, but have yet to be formally integrated into many research programs. We feel that the most exciting new insights will come where the traditional experimental approaches to Evo‐devo are integrated more thoroughly with the principles of this organismal framework.     

Movement of protistan trophic groups in soil–plant continuums

Protists, functionally divided into consumers, phototrophs, and parasites act as integral components and vital regulators of microbiomes in soil–plant continuums. However, the drivers of community structure, assembly mechanisms, co-occurrence patterns, and the associations with human pathogens and different protistan trophic groups remain unknown. Here, we characterized the phyllosphere and soil protistan communities associated with three vegetables under different fertilization treatments (none and organic fertilization) at five growth stages. In this study, consumers were the most diverse soil protist group, had the role of inter-kingdom connector, and were the primary biomarker for rhizosphere soils which were subjected to decreasing deterministic processes during plant growth. In contrast, phototrophs had the greatest niche breadth and formed soil protistan hubs, and were the primary biomarkers for both bulk soils and the phyllosphere. Parasites had minimal input to microbial co-occurrence networks. Organic fertilization increased the relative abundance (RA) of pathogenic protists and the number of pathogen–consumer connections in rhizosphere soils but decreased protistan richness and the number of internal protistan links. This study advances our understanding of the ecological roles and potential links between human pathogens and protistan trophic groups associated with soil–plant continuums, which is fundamental to the regulation of soil–plant microbiomes and maintenance of environmental and human health.     

Predicting global change impacts on plant species’ distributions: Future challenges

Given the rate of projected environmental change for the 21st century, urgent adaptation and mitigation measures are required to slow down the on-going erosion of biodiversity. Even though increasing evidence shows that recent human-induced environmental changes have already triggered species’ range shifts, changes in phenology and species’ extinctions, accurate projections of species’ responses to future environmental changes are more difficult to ascertain. This is problematic, since there is a growing awareness of the need to adopt proactive conservation planning measures using forecasts of species’ responses to future environmental changes.

There is a substantial body of literature describing and assessing the impacts of various scenarios of climate and land-use change on species’ distributions. Model predictions include a wide range of assumptions and limitations that are widely acknowledged but compromise their use for developing reliable adaptation and mitigation strategies for biodiversity. Indeed, amongst the most used models, few, if any, explicitly deal with migration processes, the dynamics of population at the “trailing edge” of shifting populations, species’ interactions and the interaction between the effects of climate and land-use.

In this review, we propose two main avenues to progress the understanding and prediction of the different processes occurring on the leading and trailing edge of the species’ distribution in response to any global change phenomena. Deliberately focusing on plant species, we first explore the different ways to incorporate species’ migration in the existing modelling approaches, given data and knowledge limitations and the dual effects of climate and land-use factors. Secondly, we explore the mechanisms and processes happening at the trailing edge of a shifting species’ distribution and how to implement them into a modelling approach. We finally conclude this review with clear guidelines on how such modelling improvements will benefit conservation strategies in a changing world.     

Communicating about ocean health: theoretical and practical considerations

As anthropogenic stressors threaten the health of marine ecosystems, there is a need to better understand how the public processes and responds to information about ocean health. Recent studies of public perceptions about ocean issues report high concern but limited knowledge, prompting calls for information campaigns to mobilize public support for ocean restoration policy. Drawing on the literature from communication, psychology and related social science disciplines, we consider a set of social-cognitive challenges that researchers and advocates are likely to encounter when communicating with the public about ocean health and emerging marine diseases—namely, the psychological distance at which ocean issues are construed, the unfamiliarity of aquatic systems to many members of the public and the potential for marine health issues to be interpreted through politicized schemas that encourage motivated reasoning over the dispassionate consideration of scientific evidence. We offer theory-based strategies to help public outreach efforts address these challenges and present data from a recent experiment exploring the role of message framing (emphasizing the public health or environmental consequences of marine disease) in shaping public support for environmental policy.     

Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: A review

The aim of the present review is to define the various origins of root-mediated changes of pH in the rhizosphere, i.e., the volume of soil around roots that is influenced by root activities. Root-mediated pH changes are of major relevance in an ecological perspective as soil pH is a critical parameter that influences the bioavailability of many nutrients and toxic elements and the physiology of the roots and rhizosphere microorganisms. A major process that contributes root-induced pH changes in the rhizosphere is the release of charges carried by H⁺ or OH^– to compensate for an unbalanced cation–anion uptake at the soil–root interface. In addition to the ions taken up by the plant, all the ions crossing the plasma membrane of root cells (e.g., organic anions exuded by plant roots) should be taken into account, since they all need to be balanced by an exchange of charges, i.e., by a release of either H⁺ or OH^–. Although poorly documented, root exudation and respiration can contribute some proportion of rhizosphere pH decrease as a result of a build-up of the CO₂ concentration. This will form carbonic acid in the rhizosphere that may dissociate in neutral to alkaline soils, and result in some pH decrease. Ultimately, plant roots and associated microorganisms can also alter rhizosphere pH via redox-coupled reactions. These various processes involved in root-mediated pH changes in the rhizosphere also depend on environmental constraints, especially nutritional constraints to which plants can respond. This is briefly addressed, with a special emphasis on the response of plant roots to deficiencies of P and Fe and to Al toxicity. Finally, soil pH itself and pH buffering capacity also have a dramatic influence on root-mediated pH changes.