Defining nutritional constraints on carbon cycling in boreal forests – towards a less `phytocentric' perspective

Growing interest in possible global climate change has underlined the need for better information concerning the way in which carbon partitioning between ecosystem components is influenced by constraints on nutrient availability. Micro-organisms play a fundamental role in the cycling of carbon and nutrients in all ecosystems but the role of fungi in particular is pivotal in boreal forest ecosystems. Traditional models of nutrient cycling are based on methods and concepts developed in agricultural systems where microorganisms are considered primarily as nutrient processors providing plants with inorganic nutrients. The filamentous nature of fungi, their ability to translocate carbon and nutrients between different substrates and the capacity of ectomycorrhizal fungi to utilise organic nutrients have all been largely ignored. In this article, a new model is suggested which emphasises competition for organic nutrients between decomposer organisms and plants, with the plants depending on their associated mycorrhizal fungi for nutrient acquisition. Antagonistic interactions involving nutrient transfer between decomposer and mycorrhizal fungi are proposed as important pathways in nutrient cycling. Due to the nutrient conservative features of decomposer fungi, inorganic nutrients are considered less important for plant nutrition. The implications of the new nutrient cycling model on the carbon balance of boreal forests are discussed.     

Recent advances in unraveling the mystery of combined nutrient stress in plants

Efficiently regulating growth to adapt to varying resource availability is crucial for organisms, including plants. In particular, the acquisition of essential nutrients is vital for plant development, as a shortage of just one nutrient can significantly decrease crop yield. However, plants constantly experience fluctuations in the presence of multiple essential mineral nutrients, leading to combined nutrient stress conditions. Unfortunately, our understanding of how plants perceive and respond to these multiple stresses remains limited. Unlocking this mystery could provide valuable insights and help enhance plant nutrition strategies. This review focuses specifically on the regulation of phosphorous homeostasis in plants, with a primary emphasis on recent studies that have shed light on the intricate interactions between phosphorous and other essential elements, such as nitrogen, iron, and zinc, as well as non-essential elements like aluminum and sodium. By summarizing and consolidating these findings, this review aims to contribute to a better understanding of how plants respond to and cope with combined nutrient stress.     

Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals

Plant nutrients, with the exception of nitrogen, are ultimately derived from weathering of primary minerals. Traditional theories about the role of ectomycorrhizal fungi in plant nutrition have emphasized quantitative effects on uptake and transport of dissolved nutrients. Qualitative effects of the symbiosis on the ability of plants to access organic nitrogen and phosphorus sources have also become increasingly apparent. Recent research suggests that ectomycorrhizal fungi mobilize other essential plant nutrients directly from minerals through excretion of organic acids. This enables ectomycorrhizal plants to utilize essential nutrients from insoluble mineral sources and affects nutrient cycling in forest systems.     

Testing experimentally the effect of soil resource mobility on plant competition

Aims The volume of soil beyond a plant's roots from which that plant is able to acquire a particular nutrient depends upon the mobility of that nutrient in the soil. For this reason it has been hypothesized that the strength of competitive interactions between plants vary with soil nutrient mobility. We aimed to provide an experimental test of this hypothesis.Methods We devised two experimental systems to investigate specifically the effect of nutrient transport rates upon intraspecific competition. In the first, the exchange of rhizosphere water and dissolved nutrients between two connected pots, each containing one plant, was manipulated by alternately raising and lowering the pots. In the second experiment, the roots systems of two competing plants were separated by partitions of differing porosity, thereby varying the plants' access to water and nutrients in the other plant′s rhizosphere. In this second experiment, we also applied varying amounts of nutrients to test whether higher nutrient input would reduce competition when competition for light is avoided, and applied different water levels to affect nutrient concentrations without changing nutrient supply.Important findings In both experiments, lower mobility reduced competitive effects on plant biomass and on relative growth rate (RGR), as hypothesized. In the second experiment, however, competition was more intense under high nutrient input, suggesting that low nutrient supply rates reduced the strength of the superior competitor. Competitive effects on RGR were only evident under the low water level, suggesting that under lower nutrient concentrations, competitive effects might be less pronounced. Taken together, our results provide the first direct experimental evidence that a reduction in nutrient mobility can reduce the intensity of competition between plants.     

The Multifunctional Role of Ectomycorrhizal Associations in Forest Ecosystem Processes

Belowground biological interactions that occur among plant roots, microorganisms and animals are dynamic and substantially influence ecosystem processes. Among these interactions, the ectomycorrhizal (ECM) symbiosis is remarkable but unfortunately these associations have mainly been considered within the rather narrow perspective of their effects on the uptake of dissolved mineral nutrients by individual plants. More recent research has placed emphasis on a wider, multifunctional perspective, including the effects of ectomycorrhizal symbiosis on plant and microbial communities, and on ecosystem processes. This includes mobilization of N and P from organic polymers, release of nutrients from mineral particles or rock surfaces via weathering, effects on carbon cycling, interactions with mycoheterotrophic plants, mediation of plant responses to stress factors such as drought, soil acidification, toxic metals, and plant pathogens, rehabilitation and regeneration of degraded forest ecosystems, as well as a range of possible interactions with groups of other soil microorganisms. Ectomycorrhizas are almost invariably characterized by a Hartig net composed of highly branched hyphae which entirely surround the outer root cortical cells. The Hartig net is the place of massive bidirectional exchanges of nutrients between the host and the fungus. Through these branched hyphae ectomycorrhizal fungi connect their plant hosts to the heterogeneously distributed nutrients required for their growth, enabling the flow of energy-rich compounds required for nutrient mobilization whilst simultaneously providing conduits for the translocation of mobilized products back to their hosts. In addition to increasing the nutrient absorptive surface area of their host plant root systems, the extraradical mycelium of ectomycorrhizal fungi provides a direct pathway for translocation of photosynthetically derived carbon from their hosts to microsites in the soil and a large surface area for interaction with other soil micro-organisms. The detailed functioning and regulation of these mycorrhizosphere processes is still poorly understood and needs detailed molecular approach to study these mycorrhizosphere processes but recent progress in ectomycorrhizal associations is reviewed and potential benefits of improved understanding of mycorrhizosphere interactions are discussed.     

Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control

A great deal of information is available in the literature on the effects of nutrition on disease development in plants and crops. However, much of this information is contradictory and although it is widely recognised that nutrition can influence disease in crops, limited progress has been made in the manipulation of crop nutrition to enhance disease control. Achieving this aim requires a sound understanding of the effects of fertilisation on nutrient levels and availability in crop tissues, and in turn, how the nutrient status of such tissues influences pathogen infection, colonisation and sporulation. Some of these details are known for a number of crop plants under controlled conditions, but very little of this type of information is available for crops under field conditions. This review focuses on nitrogen, sulphur, phosphorus, potassium and silicon, examines the availability of these nutrients in plant tissues to support pathogen growth and development, and reviews the effects of the different nutrients on disease development. The review also examines the potential for manipulating crop nutrition to enhance disease control in conventional and organic cropping systems.     

植物与土壤微生物在调控生态系统养分循环中的作用

陆地生态系统的地上、地下是相互联系的。植物与土壤微生物作为陆地生态系统中的重要组成部分, 它们之间的相互作用是生态系统地上、地下结合的重要纽带。该文首先介绍了植物在养分循环中对营养元素的吸收、积累和归还等作用, 阐述了土壤微生物对养分有效性及土壤质量具有重要的作用。其次, 重点综述了植物与土壤微生物之间相互依存、相互竞争的关系。植物通过其凋落物与分泌物为土壤微生物提供营养, 土壤微生物作为分解者提供植物可吸收的营养元素, 比如共生体菌根真菌即可使植物根与土壤真菌达到互惠。然而, 植物的养分吸收与微生物的养分固持同时存在, 因而两者之间存在对养分的竞争。通过植物多样性对土壤微生物多样性的影响分析, 以及土壤微生物直接或间接作用于植物多样性和生产力的分析, 探讨了植物物种多样性与土壤微生物多样性之间的内在联系。针对当前植物与土壤微生物对养分循环的调控机制的争论, 提出植物凋落物是调节植物与土壤微生物养分循环的良好媒介, 植物与土壤微生物的共同作用对维持整个生态系统的稳定性具有重要意义。也指出了目前在陆地生态系统地上、地下研究中存在的不足和亟待解决的问题。     

Emerging trends in nitrogen and phosphorus signalling in photosynthetic eukaryotes

Phosphorus (P) and nitrogen (N) are the major nutrients that constrain plant and algal growth in nature. Recent advances in understanding nutrient signalling mechanisms of these organisms have revealed molecular attributes to optimise N and P acquisition. This has illuminated the importance of interplay between N and P regulatory networks, highlighting a need to study synergistic interactions rather than single-nutrient effects. Emerging insights of nutrient signalling in polyphyletic model plants and algae hint that, although core P-starvation signalling components are conserved, distinct mechanisms for P (and N) sensing have arisen. Here, the N and P signalling mechanisms of diverse photosynthetic eukaryotes are examined, drawing parallels and differences between taxa. Future directions to understand their molecular basis, evolution, and ecology are proposed.     

Interactions between resources and abiotic conditions control plant performance on subarctic coastal dunes

Both abiotic conditions and resource levels affect the performance of plants on coastal dune systems. On the foredune, environmental factors are particularly limiting for plant growth and these vary along a short topographical gradient, from the foot to the ridge. On subarctic coastal dunes in northeastern Canada, this topographical gradient is paralleled by a plant sequence that typically involves Honckenya peploides, Elymus mollis, and Lathyrus japonicus. In this study, field nutrient additions were carried out to evaluate the importance of N and/or P limitation on foredune plant performance. Also, glasshouse experiments were done to determine the significance of interactions between substrate resources (i.e., nutrients and water), and between substrate resources (i.e., nutrients) and an abiotic condition (i.e., salt spray) on the growth of a dune species. Field nutrient additions did not result in any significant increase in plant biomass, although nutrients were accumulated in the rhizomes of all three species present on the foredune and in the aboveground tissues of Elymus. Glasshouse experiments on Elymus showed that nutrient addition could increase plant biomass. However, water availability and salt spray interfered with nutrient use by the plants. I suggest that such interactions between resources and abiotic conditions may significantly affect plant performance and plant sequence on the foredune of coastal dune systems.     

Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium

Different symbiotic mycorrhizal associations between plantsand fungi occur, almost ubiquitously, in a wide range of terrestrialecosystems. Historically, these have mainly been consideredwithin the rather narrow perspective of their effects on theuptake of dissolved mineral nutrients by individual plants.More recent research has placed emphasis on a wider, multifunctionalperspective, including the effects of mycorrhizal symbiosison plant and microbial communities, and on ecosystem processes.This includes mobilization of N and P from organic polymers,release of nutrients from mineral particles or rock surfacesvia weathering, effects on carbon cycling, interactions withmyco-heterotrophic plants, mediation of plant responses to stressfactors such as drought, soil acidification, toxic metals, andplant pathogens, as well as a range of possible interactionswith groups of other soil micro-organisms. Mycorrhizal fungiconnect their plant hosts to the heterogeneously distributednutrients required for their growth, enabling the flow of energy-richcompounds required for nutrient mobilization whilst simultaneouslyproviding conduits for the translocation of mobilized productsback to their hosts. In addition to increasing the nutrientabsorptive surface area of their host plant root systems, theextraradical mycelium of mycorrhizal fungi provides a directpathway for translocation of photosynthetically derived carbonto microsites in the soil and a large surface area for interactionwith other micro-organisms. The detailed functioning and regulationof these mycorrhizosphere processes is still poorly understoodbut recent progress is reviewed and potential benefits of improvedunderstanding of mycorrhizosphere interactions are discussed. Key words: Arbuscular mycorrhiza, biotic interactions, carbon flow, ectomycorrhiza, ericoid mycorrhiza, mycelium, nutrient uptake, symbiosis, weathering Received 22 January 2008; Revised 7 February 2008 Accepted 7 February 2008     

Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula

Legumes form tripartite interactions with arbuscular mycorrhizal fungi and rhizobia, and both root symbionts exchange nutrients against carbon from their host. The carbon costs of these interactions are substantial, but our current understanding of how the host controls its carbon allocation to individual root symbionts is limited. We examined nutrient uptake and carbon allocation in tripartite interactions of Medicago truncatula under different nutrient supply conditions, and when the fungal partner had access to nitrogen, and followed the gene expression of several plant transporters of the Sucrose Uptake Transporter (SUT) and Sugars Will Eventually be Exported Transporter (SWEET) family. Tripartite interactions led to synergistic growth responses and stimulated the phosphate and nitrogen uptake of the plant. Plant nutrient demand but also fungal access to nutrients played an important role for the carbon transport to different root symbionts, and the plant allocated more carbon to rhizobia under nitrogen demand, but more carbon to the fungal partner when nitrogen was available. These changes in carbon allocation were consistent with changes in the SUT and SWEET expression. Our study provides important insights into how the host plant controls its carbon allocation under different nutrient supply conditions and changes its carbon allocation to different root symbionts to maximize its symbiotic benefits.     

丛枝菌根菌丝网络在植物互作中的作用机制研究进展

植物间的相互作用是生态学领域关注的重要方向之一,其对高效利用养分资源、提高生产力以及构建植物群落均具有重要意义。丛枝菌根真菌是重要的植物互惠共生微生物,其菌丝可以将邻近植物的根部连接起来,形成共同的菌丝网络(CMNs),这些网络对转移养分、水分以及调节植物群落具有重要作用。近期的研究表明,CMNs可以充当植物之间传递病害和蚜虫诱导信号的通道,并激活邻近植物(未受感染)的化学防御。本文围绕最新的CMNs在植物相互作用中的研究成果,总结了影响CMNs规模及其功能活性的主要因素,阐述了CMNs在植物间养分、水分转移及再分配中的作用,并对CMNs在地下化学信号交流、幼苗建植及群落构建的作用机制进行了系统回顾,最后展望了该研究领域中存在的问题,旨在为进一步理解CMNs在植物互作中的生态学功能提供参考。     

Impact of climate change on crop nutrient and water use efficiencies

Implicit in discussions of plant nutrition and climate change is the assumption that we know what to do relative to nutrient management here and now but that these strategies might not apply in a changed climate. We review existing knowledge on interactive influences of atmospheric carbon dioxide concentration, temperature and soil moisture on plant growth, development and yield as well as on plant water use efficiency (WUE) and physiological and uptake efficiencies of soil-immobile nutrients. Elevated atmospheric CO₂ will increase leaf and canopy photosynthesis, especially in C3 plants, with minor changes in dark respiration. Additional CO₂ will increase biomass without marked alteration in dry matter partitioning, reduce transpiration of most plants and improve WUE. However, spatiotemporal variation in these attributes will impact agronomic performance and crop water use in a site-specific manner. Nutrient acquisition is closely associated with overall biomass and strongly influenced by root surface area. When climate change alters soil factors to restrict root growth, nutrient stress will occur. Plant size may also change but nutrient concentration will remain relatively unchanged; therefore, nutrient removal will scale with growth. Changes in regional nutrient requirements will be most remarkable where we alter cropping systems to accommodate shifts in ecozones or alter farming systems to capture new uses from existing systems. For regions and systems where we currently do an adequate job managing nutrients, we stand a good chance of continued optimization under a changed climate. If we can and should do better, climate change will not help us.     

Heterogeneous distribution of soil nutrients increase intra-specific competition in the clonal plant Glechoma hederacea

Small-scale heterogeneity strongly affects plant fitness and many ecological processes, and it can significantly influence the growth of individual plants, populations and communities. Generally, clonal species achieve significantly more growth when essential resources are patchily distributed than when resources are uniformly distributed. In this study, we aim to determine the effect of spatial heterogeneity in soil resources on intraspecific competition in the clonal plant Glechoma hederacea. We report the outcomes of a greenhouse experiment where high and low densities of plants were exposed to patchy and uniform distribution of nutrients. Our results showed that patchy distribution of resources exacerbated intra-specific competition between clonal systems. We found a reduction of total mass of clonal systems growing at high-density, especially under patchy conditions. Patchy distribution of resources conduct to high concentration of resources located in small areas, and as consequence increase the competition interaction between plants. This study demonstrates that full understanding of plant–plant competitive interactions requires consideration of spatial heterogeneity in nutrient supply.     

Past, present and future of organic nutrients

Background

Slowing crop yield increases despite high fertiliser application rates, declining soil health and off-site pollution are testimony that many bioproduction systems require innovative nutrient supply strategies. One avenue is a greater contribution of organic compounds as nutrient sources for crops. That plants take up and metabolise organic molecules (‘organic nutrients’) has been discovered prior to more recent interest with scientific roots reaching far into the 19th century. Research on organic nutrients continued in the early decades of the 20th century, but after two world wars and yield increases achieved with mineral and synthetic fertilisers, a smooth continuation of the research was not to be expected, and we find major gaps in the transmission of methods and knowledge.

Scope

Addressing the antagonism of ‘organicists’ and ‘mineralists’ in plant nutrition, we illustrate how the focus of crop nutrition has shifted from organic to inorganic nutrients. We discuss reasons and provide evidence for a role of organic compounds as nutrients and signalling agents.

Conclusion

After decades of focussing on inorganic nutrients, perspectives have greatly widened again. As has occurred before in agricultural history, science has to validate agronomic practises. We argue that a framework that views plants as mixotrophs with an inherent ability to use organic nutrients, via direct uptake or aided by exoenzyme-mediated degradation, will transform nutrient management and crop breeding to complement inorganic and synthetic fertilisers with organic nutrients.     

Earthworms,Collembola and residue management change wheat (<Emphasis Type="Italic">Triticum aestivum</Emphasis>) and herbivore pest performance (Aphidina: <Emphasis Type="Italic">Rhophalosiphum padi</Emphasis>)

Management practices of arable systems determine the distribution of soil organic matter thereby changing decomposer animal activity and their impact on nutrient mineralization, plant growth and plant-herbivore interactions. Decomposer-mediated changes in plant growth and insect pest performance were investigated in wheat-aphid model systems in the greenhouse. Three types of litter distribution were established: litter patch at the soil surface (simulating mulching), litter patch deeper in soil (simulating ploughing) and litter homogeneously mixed into soil (simulating disk cultivation). The litter was labelled with (15)N to follow the mineralization and uptake of nutrients by the plants. Earthworms (Aporrectodea caliginosa) and Collembola (Protaphorura armata) were included as representatives of major functional groups of decomposers. Wheat (Triticum aestivum) was planted and aphids (Rhophalosiphum padi) were introduced to leaves as one of the most important pests. Earthworms, Collembola and litter distribution affected plant growth, N acquisition and aphid development in an interactive way. Earthworms and Collembola increased biomass of seeds, shoots and roots of wheat. Increased plant growth by earthworms and Collembola was mainly due to increased transfer of N from soil (rather than litter) into plants. Despite increasing plant growth, earthworms reduced aphid reproduction. Aphid reproduction was not correlated closely with plant N concentrations, but rather with the concentration of litter N in wheat. Unexpectedly, both Collembola and earthworms predominantly affected the mobilization of N from soil organic matter, and by altering the distribution of litter earthworms reduced infestation of crops by aphids via reducing plant capture of litter N, in particular if the litter was concentrated deeper in soil. The results suggest that management practices stimulating a continuous moderate increase in nutrient mobilization from soil organic matter rather than nutrient flushes from decomposing fresh organic matter result in maximum plant growth with minimum plant pest infestation.     

Nitrogen transport in the ectomycorrhiza association: the Hebeloma cylindrosporum-Pinus pinaster model

The function of the ectomycorrhizal mutualism depends on the ability of the fungal symbionts to take up nutrients (particularly nitrogen) available in inorganic and/or organic form in the soil and to translocate them (or their metabolites) to the symbiotic roots. A better understanding of the molecular mechanisms underlying nutrient exchanges between fungus and plant at the symbiotic interface is necessary to fully understand the function of the mycorrhizal symbioses. The present review reports the characterization of several genes putatively involved in nitrogen uptake and transfer in the Hebeloma cylindrosporum-Pinus pinaster ectomycorrhizal association. Study of this model system will further clarify the symbiotic nutrient exchange which plays a major role in plant nutrition as well as in resistance of plants against pathogens, heavy metals, drought stress, etc. Ultimately, ecological balance is maintained and/or improved with the help of symbiotic associations, and therefore, warrant further understanding.     

Endophyte roles in nutrient acquisition,root system architecture development and oxidative stress tolerance

Plants associate with communities of microbes (bacteria and fungi) that play critical roles in plant development, nutrient acquisition and oxidative stress tolerance. The major share of plant microbiota is endophytes which inhabit plant tissues and help them in various capacities. In this article, we have reviewed what is presently known with regard to how endophytic microbes interact with plants to modulate root development, branching, root hair formation and their implications in overall plant development. Endophytic microbes link the interactions of plants, rhizospheric microbes and soil to promote nutrient solubilization and further vectoring these nutrients to the plant roots making the soil-plant-microbe continuum. Further, plant roots internalize microbes and oxidatively extract nutrients from microbes in the rhizophagy cycle. The oxidative interactions between endophytes and plants result in the acquisition of nutrients by plants and are also instrumental in oxidative stress tolerance of plants. It is evident that plants actively cultivate microbes internally, on surfaces and in soils to acquire nutrients, modulate development and improve health. Understanding this continuum could be of greater significance in connecting endophytes with the hidden half of the plant that can also be harnessed in applied terms to enhance nutrient acquisition through the development of favourable root system architecture for sustainable production under stress conditions.     

Long-distance transporters of inorganic nutrients in plants

In plants, long-distance transport of inorganic nutrients is important for mineral nutrition, ion homeostasis, nutrient recycling, and the detoxification of toxic or excess inorganic ions. Here, we review information on the transporters involved in the loading/unloading of inorganic nutrients to and from the vascular bundle. We also describe the methods used to obtain such information.