Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability

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.

Rhizosphere: biophysics, biogeochemistry and ecological relevance

Organic acids have been hypothesized to perform many functions in soil including root nutrient acquisition, mineral weathering, microbial chemotaxis and metal detoxification. However, their role in most of these processes remains unproven due to a lack of fundamental understanding about the reactions of organic acids in soil. This review highlights some of the knowledge gaps and misconceptions associated with the behavior of organic acids in soil with particular reference to low-molecular-weight organic acids (e.g., citrate, oxalate, malate) and plant nutrient acquisition. One major concern is that current methods for quantifying organic acids in soil may vastly underestimate soil solution concentrations and do not reveal the large spatial heterogeneity that may exist in their concentration (e.g., around roots or microbes). Another concern relates to the interaction of organic acids with the soil's solid phase and the lack of understanding about the relative importance of processes such as adsorption versus precipitation, and sorption versus desorption. Another major knowledge gap concerns the utilization of organic acids by the soil microbial community and the forms of organic acids that they are capable of degrading (e.g., metal-complexed organic acids, adsorbed organic acids etc). Without this knowledge it will be impossible to obtain accurate mathematical models of organic acid dynamics in soil and to understand their role and importance in ecosystem processes. Fundamental research on organic acids and their interaction with soil still needs to be done to fully elucidate their role in soil processes.

Organic acid behavior in soils - Misconceptions and knowledge gaps

Apart from the function of plant roots as organs for nutrient uptake, roots are 
also able to release a wide range of organic and inorganic compounds into the 
root environment. Soil-chemical changes related to the presence of these compounds and products of their microbial turnover are important factors affecting 
microbial populations, availability of nutrients, solubility of toxic elements in the 
rhizosphere, and thereby the ability of plants to cope with adverse soil-chemical 
conditions (1). Organic rhizodeposition includes lysates, liberated by autolysis 
of sloughed-off cells and tissues, as well as root exudates, released passively 
(diffusates) or actively (secretions) from intact root cells (Table 1; see also 
Chap. 2). In annual plant species, 30-60% of the photosynthetically fixed carbon 
is translocated to the roots, and a considerable proportion of this carbon (up to 
70%) can be released into the rhizosphere (2,3), as pointed out in Chaps. 4, 6, and 
12. This rhizodeposition is affected by multiple factors, such as light intensity, 
temperature, nutritional status of the plants, activity of retrieval mechanisms, various stress factors, mechanical impedance, sorption characteristics of the growth 
medium, and microbial activity in the rhizosphere. This chapter focuses on the 
release of water-soluble organic root exudates and highlights effects of the physiological status on root exudation and its significance for adaptations to adverse 
soil conditions and nutrient efficiency. Since the methods employed for collection 
and analysis of root exudates play an important role in the qualitative and quanti-Table 1 Root Exudates Detected in Higher PlantsClass of compoundsSugarsAmino acids and amidesAliphatic acidsAromatic acidsMiscellaneous phenolics 
Fatty acids 
Sterols 
EnzymesMicellaneousSingle componentsArabinose, glucose, fructose, galactose, maltose, raffinose, 
rhamnose, ribose, sucrose, xyloseAll 20 proteinogenic amino acids, aminobutyric acid, homoserine, cysrathionine, mugineic acid phytosiderophores 
(mugineic acid, deoxymugineic acid, hydroxymugineic 
acid, epi-hydroxymugineic acid, avenic acid, distichonic 
acid A)Formic, acetic, butyric, popionic, malic, citric, isocitric, oxalic, fumaric, malonic, succinic, maleic, tartaric, oxaloacetic, pyruvic, oxoglutaric, maleic, glycolic, shikimic, 
cis-aconitic, trans-aconitic, valerie, gluconicp-Hydroxybenzoic, caffeic, p-coumaric, ferulic, gallic, gentisic, protocatechuic, salicylic, sinapic, syringicFlavonols, ftavones, ftavanones, anthocyanins, isoftavonoids 
Linoleic, linolenic, oleic, palmitic, stearic 
Campestrol, cholesterol, sitosterol, stigmasterol 
Amylase, invertase, cellobiase, desoxyribonuclease, ribonu-clease, acid phosphatase, phytase, pyrophosphatase apyrase, peroxidase, proteaseVitamins, plant growth regulators (auxins, cytokinins, gibberellins), alkyl sulfides, ethanol, H+, K+ nitrate, phosphate, HC03-tative interpretation of measured exudate data, methodological aspects are also 
discussed in an introductory section.

The Release of Root Exudates as Affected by the Plant's Physiological Status

The main process by which dissolved organic matter (DOM) is retained in forest soils is likely to be sorption in the mineral horizons that adds to stabilized organic matter (OM) pools. The objectives of this study were to determine the extent of degradation of sorbed OM and to investigate changes in its composition during degradation. DOM of different origins was sorbed to a subsoil and incubated for 1 year. We quantified mineralized C by frequent CO2 measurements in the headspace of the incubation vessels and calculated mean residence times by a double exponential model. Mineralization of C of the corresponding DOM in solution was used as a control to estimate the extent of DOM stabilization by sorption. Changes in the composition of sorbed OM during the incubation were studied by spectroscopic (UV, fluorescence) and isotope (13C, 14C) measurements after hot-water extraction of OM. The fraction of sorbed organic C mineralized during the incubation was only one-third to one-sixth of that mineralized in solution. The mean residence time of the most stable OM sample was estimated to increase from 28 years in solution to 91 years after sorption. For highly degradable DOM samples, the portion of stable C calculated by a double exponential model nearly doubled upon sorption. With less degradable DOM the stability increased by only 20% after sorption. Therefore, the increase in stability due to sorption is large for labile DOM high in carbohydrates and relatively small for stable DOM high in aromatic and complex molecules. Nevertheless, in terms of stability the rank order of OM types after sorption was the same as in solution. Furthermore, the extent of sorption of recalcitrant compounds was much larger than sorption of labile compounds. Thus, sorptive stabilization of this stable DOM sample was four times larger than for the labile ones. We conclude that stabilization of OM by sorption depends on the intrinsic stability of organic compounds sorbed. We propose that the main stabilization processes are selective sorption of intrinsically stable compounds and strong chemical bonds to the mineral soil and/or a physical inaccessibility of OM to microorganisms. The UV, fluorescence and 13C measurements indicated that aromatic and complex compounds, probably derived from lignin, were preferentially stabilized by sorption of DOM. The 13C and 14C data showed that degradation of the indigenous OM in the mineral soil decreased after sorption of DOM. We estimated DOM sorption stabilizes about 24 Mg C ha−1 highlighting the importance of sorption for accumulation and preservation of OM in soil.

Stabilization of dissolved organic matter by sorption to the mineral soil

A system for microscale tensiometry and lysimetry

Capillary electrophoresis (CE) is suitable for the analysis of cations and anions, including organic acids, in soil solution. In the concentration range typical for soil solutions, the standard deviation of the linear calibration function is, with the exception of NH+4 and Na+ (≅ 12%), better than 6

Analysis of Small Volumes of Soil Solution by Capillary Electrophoresis

Characterization of phosphorus fractions in mountain soils of the Bavarian Alps by 31P NMR spectroscopy

Large amounts of soil organic matter can be extracted when using salt solutions or organic solvents, but these extracts do not represent the organic matter soluble under natural conditions. The objective of our study was to evaluate the usefulness of water at high-temperature and elevated pressure for soil organic matter extraction. Soil samples were extracted with water at different temperatures under high pressure (10 MPa), using an Accelerated Solvent Extractor (ASE). These extracts were compared to extracts obtained by conventional methods using distilled water, NaOH and Na4P2O7 solutions. Yields of ASE extracts were up to twenty-fold higher than those of conventional water extracts. UV spectra as well as 1H and 13C NMR spectra revealed high similarity between conventional water extracts and ASE extracts up to 150°C. At higher temperatures, ASE extracts were enriched in aromatic and depleted in O-alkyl-C structures, strongly resembling the NaOH and Na4P2O7 extracts.

Roland Blasek

Papers

A system for microscale tensiometry and lysimetry

Analysis of Small Volumes of Soil Solution by Capillary Electrophoresis

Characterization of phosphorus fractions in mountain soils of the Bavarian Alps by 31P NMR spectroscopy

Soil Organic Matter Extraction Using Water at High Temperature and Elevated Pressure (ASE) as Compared to Conventional Methods

Bodenkundliche Charakterisierung der Intensivmeßfläche Coulissenhieb