Role of mycorrhizas and root exudates in plant uptake of soil nutrients (calcium, iron, magnesium, and potassium): has the puzzle been completely solved?

Anthropogenic global change is driving an increase in the frequency and intensity of drought and flood events, along with associated imbalances and limitation of several soil nutrients. In the context of an increasing human population, these impacts represent a global-scale challenge for biodiversity conservation and sustainable crop production to ensure food security. Plants have evolved strategies to enhance uptake of soil nutrients under environmental stress conditions; for example, symbioses with fungi (mycorrhization) in the rhizosphere and the release of exudates from roots. Although crop cultivation is managed for the effects of limited availability of nitrogen (N) and phosphorus (P), there is increasing evidence for limitation of plant growth and fitness because of the low availability of other soil nutrients such as the metals potassium (K), calcium (Ca), magnesium (Mg), and iron (Fe), which may become increasingly limiting for plant productivity under global change. The roles of mycorrhizas and plant exudates on N and P uptake have been studied intensively; however, our understanding of the effects on metal nutrients is less clear and still inconsistent. Here, we review the literature on the role of mycorrhizas and root exudates in plant uptake of key nutrients (N, P, K, Ca, Mg, and Fe) in the context of potential nutrient deficiencies in crop and non-crop terrestrial ecosystems, and identify knowledge gaps for future research to improve nutrient-uptake capacity in food crop plants.

Soil carbon sequestration by root exudates.

Root exudates are well-known 'labile' sources of soil carbon that can prime microbial activity. Recent investigations suggest that the stability of labile carbon inputs in soil mostly depends upon the physical, chemical, and biological properties of the surroundings. Here, we propose that, in some ecosystems, such as forests and grasslands, root exudates can function as a source of soil organic carbon (SOC) that can be stabilized through various mechanisms leading to long-term sequestration. Increasing soil carbon sequestration is important for capturing atmospheric CO2 and combating climate change issues. Thus, there is an urgent need to preserve existing ecosystems and to adopt strategies such as afforestation, reforestation, and establishment of artificial grasslands to foster carbon sequestration through higher root exudate inputs in the soil.

Do Bryophyte Elemental Concentrations Explain Their Morphological Traits?

Differences in the elemental composition of plants, mainly C, N, and P, have been shown to be related to differences in their nutritional status, and their morphological and functional traits. The relationship between morphological traits and micronutrients and trace elements, however, has been much less studied. Additionally, in bryophytes, research devoted to investigating these relationships is still very scarce. Here, we analysed 80 samples from 29 aquatic and semi-aquatic (hygrophytic) moss species living in Mediterranean springs to investigate the relationship between moss nutrient concentrations and their micro- and macroscopic morphological traits and growth forms. We found that, across species, the elemental concentration of mosses was more tightly linked to macroscopic traits than to microscopic traits. Growth forms could also be successfully explained by the concentration of elements in mosses. Apart from macronutrients and their stoichiometric ratios (C:N, C:P, and N:P), micronutrients and trace elements were also important variables predicting moss morphological traits and growth forms. Additionally, our results showed that microscopic traits were well related to macroscopic traits. Overall, our results clearly indicate that the elemental composition of mosses can be used to infer their morphological traits, and that elements other than macronutrients should be taken into account to achieve a good representation of their morphological and, potentially, functional traits when comparing the elemental composition across species.

Resistance and resilience of soil prokaryotic communities in response to prolonged drought in a tropical forest.

Global climate changes such as prolonged duration and intensity of drought can lead to adverse ecological consequences in forests. Currently little is known about soil microbial community responses to such drought regimes in tropical forests. In this study, we examined the resistance and resilience of topsoil prokaryotic communities to a prolongation of the dry season in terms of diversity, community structure and co-occurrence patterns in a French Guianan tropical forest. Through excluding rainfall during and after the dry season, a simulated prolongation of the dry season by five months was compared to controls. Our results show that prokaryotic communities increasingly diverged from controls with the progression of rain exclusion. Furthermore, prolonged drought significantly affected microbial co-occurrence networks. However, both the composition and co-occurrence networks of soil prokaryotic communities immediately ceased to differ from controls when precipitation throughfall returned. This study thus suggests modest resistance but high resilience of microbial communities to a prolonged drought in tropical rainforest soils.

Fertile Crescent crop progenitors gained a competitive advantage from large seedlings.

Cereal domestication during the transition to agriculture resulted in widespread food production, but why only certain species were domesticated remains unknown. We tested whether seedlings of crop progenitors share functional traits that could give them a competitive advantage within anthropogenic environments, including higher germination, greater seedling survival, faster growth rates, and greater competitive ability.Fifteen wild grass species from the Fertile Crescent were grown individually under controlled conditions to evaluate differences in growth between cereal crop progenitors and other wild species that were never domesticated. Differences in germination, seedling survival, and competitive ability were measured by growing a subset of these species as monocultures and mixtures.Crop progenitors had greater germination success, germinated more quickly and had greater aboveground biomass when grown in competition with other species. There was no evidence of a difference in seedling survival, but seed size was positively correlated with a number of traits, including net assimilation rates, greater germination success, and faster germination under competition. In mixtures, the positive effect of seed mass on germination success and speed of germination was even more beneficial for crop progenitors than for other wild species, suggesting greater fitness. Thus, selection for larger seeded individuals under competition may have been stronger in the crop progenitors.The strong competitive ability of Fertile Crescent cereal crop progenitors, linked to their larger seedling size, represents an important ecological difference between these species and other wild grasses in the region. It is consistent with the hypothesis that competition within plant communities surrounding human settlements, or under early cultivation, benefited progenitor species, favoring their success as crops.

Bryophyte C:N:P stoichiometry, biogeochemical niches and elementome plasticity driven by environment and coexistence.

Ecological stoichiometry and studies of biogeochemical niches have mainly focused on plankton and vascular plants, but the phenotypically closest modern relatives of early plants, bryophytes, have been largely neglected. We analysed C:N:P stoichiometries and elemental compositions (K, Na, Mg, Ca, S, Fe) of 35 widely distributed bryophyte species inhabiting springs. We estimated bryophyte C:N:P ratios and their biogeochemical niches, investigated how elementomes respond to the environment and determined whether they tend to diverge more for coexisting than non-coexisting individuals and species. The median C:N:P was 145:8:1, intermediate between Redfield's ratio for marine plankton and those for vascular plants. Biogeochemical niches were differentiated amongst species and were phylogenetically conserved. Differences in individual and species-specific elementomes increased with coexistence between species. Our results provide an evolutionary bridge between the ecological stoichiometries of algae and vascular plants and suggest that differences in elementomes could be used to understand community assemblages and functional diversity.

Drought is a stronger driver of soil respiration and microbial communities than nitrogen or phosphorus addition in two Mediterranean tree species.

The drivers of global change, such as increasing drought and nutrient deposition, are affecting soils and their microbial communities in many different habitats, but how these factors interact remains unclear. Quercus ilex and Pinus sylvestris are two important tree species in Mediterranean montane areas that respond differently to drought, which may be associated with the soils in which they grow. We measured soil respiration and physiologically profiled microbial communities to test the impact of drought and subsequent recovery on soil function and diversity for these two species. We also tested whether the addition of nitrogen and phosphorus modified these effects. Drought was the stronger driver of changes to the soil communities, decreasing diversity (Shannon index), and evenness for both species and decreasing soil respiration for Q. ilex when N was added. Soil respiration for P. sylvestris during the drought period was positively affected by N addition but was not affected by water stress. P addition during the drought period did not affect soil respiration for either tree species but did interact with soil-water content to affect community evenness for P. sylvestris. The two species also differed following the recovery from drought. Soil respiration for Q. ilex recovered fully after the drought treatment ended but decreased for P. sylvestris, whereas the soil community was more resilient for P. sylvestris than Q. ilex. Nutrient addition did not affect respiration or community composition or diversity during the recovery period. Soil respiration was generally weakly positively correlated with soil diversity. We demonstrate that short-term water stress and nutrient addition can have variable effects on the soil communities associated with different tree species and that the compositions of the communities can become uncoupled from soil respiration. Overall, we show that drought may be a stronger driver of changes to soil communities than nitrogen or phosphorus deposition.

A Return to the Wild: Root Exudates and Food Security.

Challenges to food security under conditions of global change are forcing us to increase global crop production. Focussing on belowground plant traits, especially root exudation, has great promise to meet this challenge. Root exudation is the release of a vast array of compounds into the soil. These exudates are involved in many biotic and abiotic interactions. Wild relatives of crops provide a large potential source of information and genetic material and have desirable traits that could be incorporated into modern breeding programs. However, root exudates are currently underexploited. Here, we highlight how the traits of root exudates of crop wild relatives could be used to improve agricultural output and reduce environmental impacts, particularly by decreasing our dependence on pesticides and fertilisers.

Re-analysis of archaeobotanical remains from pre- and early agricultural sites provides no evidence for a narrowing of the wild plant food spectrum during the origins of agriculture in southwest Asia.

Archaeobotanical evidence from southwest Asia is often interpreted as showing that the spectrum of wild plant foods narrowed during the origins of agriculture, but it has long been acknowledged that the recognition of wild plants as foods is problematic. Here, we systematically combine compositional and contextual evidence to recognise the wild plants for which there is strong evidence of their deliberate collection as food at pre-agricultural and early agricultural sites across southwest Asia. Through sample-by-sample analysis of archaeobotanical remains, a robust link is established between the archaeological evidence and its interpretation in terms of food use, which permits a re-evaluation of the evidence for the exploitation of a broad spectrum of wild plant foods at pre-agricultural sites, and the extent to which this changed during the development of early agriculture. Our results show that relatively few of the wild taxa found at pre- and early agricultural sites can be confidently recognised as contributing to the human diet, and we found no evidence for a narrowing of the plant food spectrum during the adoption of agriculture. This has implications for how we understand the processes leading to the domestication of crops, and points towards a mutualistic relationship between people and plants as a driving force during the development of agriculture.

Root exudate metabolomes change under drought and show limited capacity for recovery.

Root exudates comprise a large variety of compounds released by plants into the rhizosphere, including low-molecular-weight primary metabolites (particularly saccharides, amino acids and organic acids) and secondary metabolites (phenolics, flavonoids and terpenoids). Changes in exudate composition could have impacts on the plant itself, on other plants, on soil properties (e.g. amount of soil organic matter), and on soil organisms. The effects of drought on the composition of root exudates, however, have been rarely studied. We used an ecometabolomics approach to identify the compounds in the exudates of Quercus ilex (holm oak) under an experimental drought gradient and subsequent recovery. Increasing drought stress strongly affected the composition of the exudate metabolome. Plant exudates under drought consisted mainly of secondary metabolites (71% of total metabolites) associated with plant responses to drought stress, whereas the metabolite composition under recovery shifted towards a dominance of primary metabolites (81% of total metabolites). These results strongly suggested that roots exude the most abundant root metabolites. The exudates were changed irreversibly by the lack of water under extreme drought conditions, and the plants could not recover.

Cereal progenitors differ in stand harvest characteristics from related wild grasses.

The domestication of crops in the Fertile Crescent began approximately 10,000 years ago indicating a change from a hunter-gatherer lifestyle to a sedentary, agriculture-based existence. The exploitation of wild plants changed during this transition, such that a small number of crops were domesticated from the broader range of species gathered from the wild. However, the reasons for this change are unclear.Previous studies have shown unexpectedly that crop progenitors are not consistently higher yielding than related wild grass species, when growing without competition. In this study, we replicate more closely natural competition within wild stands, using two greenhouse experiments to investigate whether cereal progenitors exhibit a greater seed yield per unit area than related wild species that were not domesticated.Stands of cereal progenitors do not provide a greater total seed yield per unit ground area than related wild species, but these crop progenitors do have greater reproductive efficiency than closely related wild species, with nearly twice the harvest index (the ratio of harvested seeds to total shoot dry mass).These differences arise because the progenitors have greater seed yield per tiller than closely related wild species, due to larger individual seed size but no reduction in seed number per tiller. The harvest characteristics of cereal progenitors may have made them a more attractive prospect than closely related wild species for the early cultivators who first planted these species, or could suggest an ecological filtering mechanism. Synthesis. Overall, we show that the maintenance of a high harvest index under competition, the packaging of seed in large tillers, and large seeds, consistently distinguish crop progenitors from closely related wild grass species. However, the archaeological significance of these findings remains unclear, since a number of more distantly related species, including wild oats, have an equally high or higher harvest index and yield than some of the progenitor species. Domestication of the earliest cereal crops from the pool of wild species available cannot therefore be explained solely by species differences in yield and harvest characteristics, and must also consider other plant traits.

Thirsty tree roots exude more carbon.

Root exudation is an important input of carbon into soils and affects plant and soil communities, but little is known about the effect of climatic factors such as drought on exudation, and its ability to recover. We studied the impact of increasing drought on root exudation and its subsequent recovery in the Mediterranean tree species Quercus ilex L. in a greenhouse study by measuring the amount of total organic carbon in exudates. The amount of exudation per unit root area increased with drought duration and was 21% higher under the most extreme drought scenario compared with the non-droughted control. The amount of root exudation did not differ between the treatments following 6 weeks of re-watering, indicating a strong capacity for recovery in this species. We concluded that drought could affect the amount of root exudation, which could in turn have a large impact on microbial activity in the rhizosphere, and alter these microbial communities, at least in the short term. This tree species may be able to return to normal levels of root exudation after a drought event, but long-term exudate-mediated impacts on Mediterranean forest soils may be an unforeseen effect of drought.

How did the domestication of Fertile Crescent grain crops increase their yields?

The origins of agriculture, 10 000 years ago, led to profound changes in the biology of plants exploited as grain crops, through the process of domestication. This special case of evolution under cultivation led to domesticated cereals and pulses requiring humans for their dispersal, but the accompanying mechanisms causing higher productivity in these plants remain unknown. The classical view of crop domestication is narrow, focusing on reproductive and seed traits including the dispersal, dormancy and size of seeds, without considering whole-plant characteristics. However, the effects of initial domestication events can be inferred from consistent differences between traditional landraces and their wild progenitors.We studied how domestication increased the yields of Fertile Crescent cereals and pulses using a greenhouse experiment to compare landraces with wild progenitors. We grew eight crops: barley, einkorn and emmer wheat, oat, rye, chickpea, lentil and pea. In each case, comparison of multiple landraces with their wild progenitors enabled us to quantify the effects of domestication rather than subsequent crop diversification. To reveal the mechanisms underpinning domestication-linked yield increases, we measured traits beyond those classically associated with domestication, including the rate and duration of growth, reproductive allocation, plant size and also seed mass and number.Cereal and pulse crops had on average 50% higher yields than their wild progenitors, resulting from a 40% greater final plant size, 90% greater individual seed mass and 38% less chaff or pod material, although this varied between species. Cereal crops also had a higher seed number per spike compared with their wild ancestors. However, there were no differences in growth rate, total seed number, proportion of reproductive biomass or the duration of growth.The domestication of Fertile Crescent crops resulted in larger seed size leading to a larger plant size, and also a reduction in chaff, with no decrease in seed number per individual, which proved a powerful package of traits for increasing yield. We propose that the important steps in the domestication process should be reconsidered, and the domestication syndrome broadened to include a wider range of traits.

Were Fertile Crescent crop progenitors higher yielding than other wild species that were never domesticated?

During the origin of agriculture in the Fertile Crescent, the broad spectrum of wild plant species exploited by hunter-gatherers narrowed dramatically. The mechanisms responsible for this specialization and the associated domestication of plants are intensely debated. We investigated why some species were domesticated rather than others, and which traits they shared. We tested whether the progenitors of cereal and pulse crops, grown individually, produced a higher yield and less chaff than other wild grasses and legumes, thereby maximizing the return per seed planted and minimizing processing time. We compared harvest traits of species originating from the Fertile Crescent, including those for which there is archaeological evidence of deliberate collection. Unexpectedly, wild crop progenitors in both families had neither higher grain yield nor, in grasses, less chaff, although they did have larger seeds. Moreover, small-seeded grasses actually returned a higher yield relative to the mass of seeds sown. However, cereal progenitors had threefold fewer seeds per plant, representing a major difference in how seeds are packaged on plants. These data suggest that there was no intrinsic yield advantage to adopting large-seeded progenitor species as crops. Explaining why Neolithic agriculture was founded on these species, therefore, remains an important unresolved challenge.

Ecosystem response to climatic change: the importance of the cold season.

Winter climate and snow cover are the important drivers of plant community development in polar regions. However, the impacts of changing winter climate and associated changes in snow regime have received much less attention than changes during summer. Here, we synthesize the results from studies on the impacts of extreme winter weather events on polar heathland and lichen communities. Dwarf shrubs, mosses and soil arthropods were negatively impacted by extreme warming events while lichens showed variable responses to changes in extreme winter weather events. Snow mould formation underneath the snow may contribute to spatial heterogeneity in plant growth, arthropod communities and carbon cycling. Winter snow cover and depth will drive the reported impacts of winter climate change and add to spatial patterns in vegetation heterogeneity. The challenges ahead lie in obtaining better predictions on the snow patterns across the landscape and how these will be altered due to winter climate change.

Impacts of winter icing events on the growth, phenology and physiology of sub-arctic dwarf shrubs.

The Arctic is experiencing the greatest climate change in winter, including increases in freeze-thaw cycles that can result in ice encasement of vegetation. Ice encasement can expose plants to hypoxia and greater temperature extremes, but currently the impacts of icing on plants in the field remain little understood. With this in mind, a unique field manipulation experiment was established in heathland in northern Sweden with ice encasement simulated in early March 2008, 2009 and 2010 until natural thaw each spring. In the following summers we assessed the impacts on flowering, bud phenology, shoot growth and mortality and leaf damage (measured by chlorophyll fluorescence and electrolyte leakage) of the three dominant dwarf shrub species Empetrum nigrum, Vaccinium vitis-idaea (both evergreen) and Vaccinium myrtillus (deciduous). Two consecutive winters of icing decreased V. vitis-idaea flowering by 57%, while flowering of V. myrtillus and E. nigrum remained unaffected. Vaccinium myrtillus showed earlier budburst but shoot growth for all species was unchanged. Shoot mortality of V. myrtillus and V. vitis-idaea increased after the first year (by 70 and 165%, respectively) and again for V. myrtillus following the third year (by 67%), while E. nigrum shoot mortality remained unaffected, as were chlorophyll fluorescence and electrolyte leakage in all species. Overall, the sub-arctic heathland was relatively tolerant to icing, but the considerable shoot mortality of V. myrtillus contrasting with the general tolerance of E. nigrum suggests plant community structure in the longer term could change if winters continue to see a greater frequency of icing events.