In situ seasonal patterns of root auxin concentrations and meristem length in an arctic sedge.

Seasonal dynamics of root growth play an important role in large-scale ecosystem processes; they are largely governed by growth regulatory compounds and influenced by environmental conditions. Yet, our knowledge about physiological drivers of root growth is mostly limited to laboratory-based studies on model plant species. We sampled root tips of Eriophorum vaginatum and analyzed their auxin concentrations and meristem lengths biweekly over a growing season in situ in a subarctic peatland, both in surface soil and at the permafrost thawfront. Auxin concentrations were almost five times higher in surface than in thawfront soils and increased over the season, especially at the thawfront. Surprisingly, meristem length showed an opposite pattern and was almost double in thawfront compared with surface soils. Meristem length increased from peak to late season in the surface soils but decreased at the thawfront. Our study of in situ seasonal dynamics in root physiological parameters illustrates the potential for physiological methods to be applied in ecological studies and emphasizes the importance of in situ measurements. The strong effect of root location and the unexpected opposite patterns of meristem length and auxin concentrations likely show that auxin actively governs root growth to ensure a high potential for nutrient uptake at the thawfront.

Root and shoot phenology, architecture, and organ properties: an integrated trait network among 44 herbaceous wetland species.

Integrating traits across above- and belowground organs offers comprehensive insights into plant ecology, but their various functions also increase model complexity. This study aimed to illuminate the interspecific pattern of whole-plant trait correlations through a network lens, including a detailed analysis of the root system. Using a network algorithm that allows individual traits to belong to multiple modules, we characterize interrelations among 19 traits, spanning both shoot and root phenology, architecture, morphology, and tissue properties of 44 species, mostly herbaceous monocots from Northern Ontario wetlands, grown in a common garden. The resulting trait network shows three distinct yet partially overlapping modules. Two major trait modules indicate constraints of plant size and form, and resource economics, respectively. These modules highlight the interdependence between shoot size, root architecture and porosity, and a shoot-root coordination in phenology and dry-matter content. A third module depicts leaf biomechanical adaptations specific to wetland graminoids. All three modules overlap on shoot height, suggesting multifaceted constraints of plant stature. In the network, individual-level traits showed significantly higher centrality than tissue-level traits do, demonstrating a hierarchical trait integration. The presented whole-plant, integrated network suggests that trait covariation is essentially function-driven rather than organ-specific.

High frequency root dynamics: sampling and interpretation using replicated robotic minirhizotrons.

Automating dynamic fine root data collection in the field is a longstanding challenge with multiple applications for co-interpretation and synthesis for ecosystem understanding. High frequency root data are only achievable with paired automated sampling and processing. However, automatic minirhizotron (root camera) instruments are still rare and data are often not collected in natural soils or analysed at high temporal resolution. Instruments must also be affordable for replication and robust under variable natural conditions. Here, we show a system built with off-the-shelf parts which samples at sub-daily resolution. We paired this with a neural network to analyse all images collected. We performed two mesocosm studies and two field trials alongside ancillary data collection (soil CO2 efflux, temperature, and moisture content, and 'PhenoCam'-derived above-ground dynamics). We produce robust and replicated daily time series of root dynamics under all conditions. Temporal root changes were a stronger driver than absolute biomass on soil CO2 efflux in the mesocosm. Proximal sensed above-ground dynamics and below-ground dynamics from minirhizotron data were not synchronized. Root properties extracted were sensitive to soil moisture and occasionally to time of day (potentially relating to soil moisture). This may only affect high frequency imagery and should be considered in interpreting such data.

Temporal dynamics of fine root production, mortality and turnover deviate across branch orders in a larch stand.

Fine roots play a key role in carbon, nutrient, and water biogeochemical cycles in forest ecosystems. However, inter-annual dynamics of fine root production, mortality, and turnover on the basis of long-term measurement have been less studied. Here, field scanning rhizotrons were employed for tracking fine root by branch order over a 6 years period in a larch plantation. For total fine roots, from the first- to the fifth-order roots, annual root length production, length mortality, standing crops, and turnover rate varied up to 3.4, 2.3, 1.5, and 2.3-folds during the study period, respectively. The inter-annual variability of those roots indices in the first-order and the second-order roots were greater than that of the higher order (third- to fifth-order) roots. The turnover rate was markedly larger for the first-order roots than for the higher order roots, showing the greatest variability up to 20 times. Seasonal dynamics of root length production followed a general concentrated pattern with peak typically occurring in June or July, whereas root length mortality followed a general bimodal mortality pattern with the dominant peak in May and the secondary peak in August or October. Furthermore, the seasonal patterns of root length production and mortality were similar across years, especially for the first-order and the second-order roots. These results from long-term observation were beneficial for reducing uncertainty of characterizing fine root demography in consideration of large variation among years. Our findings highlight it is important for better understanding of fine root dynamics and determining root demography through distinguishing observation years and root branch orders.

Regional distribution patterns of wetland monocots with different root turnover strategies are associated with local variation in soil temperature.

Herbaceous perennial wetland monocots in Northern Ontario, Canada, show dichotomous root overwintering patterns, either with full senescence in autumn or survival over the winter, comparable to deciduous and evergreen leaf habits in trees. To test if these root strategies differ in their associations with growing season length, soil temperatures were recorded in autumn, winter and spring on 38 wetland sites with their dominant species being either of these two root overwintering strategies, altogether 19 monocot species. Traits associated with these strategies were assessed in garden experiments for a subset of these species. Sites with species with autumn-senescing roots were, on average, warmer than sites with species with overwintering roots. The 13 coldest sites were all sites of species with overwintering roots. Spring shoot growth in the field was delayed in species with autumn-senescing roots, despite their higher shoot relative growth rates in the garden, possibly due to the necessity to produce roots first. We conclude that species with autumn-senescing roots are more constrained by temperature than species with overwintering roots, limiting their occurrence in cool climates to locally warm soils and constraining their distribution towards the north. This is comparable to constraints on distribution of deciduous and evergreen trees.

Dwelling in the deep - strongly increased root growth and rooting depth enhance plant interactions with thawing permafrost soil.

Climate-warming-induced permafrost thaw exposes large amounts of carbon and nitrogen in soil at considerable depths, below the seasonally thawing active layer. The extent to which plant roots can reach and interact with these hitherto detached, deep carbon and nitrogen stores remains unknown. We aimed to quantify how permafrost thaw affects root dynamics across soil depths and plant functional types compared with above-ground abundance, and potential consequences for plant-soil interactions. A decade of experimental permafrost thaw strongly increased total root length and growth in the active layer, and deep roots invaded the newly thawed permafrost underneath. Root litter input to soil across all depths was 10 times greater with permafrost thaw. Root growth timing was unaffected by experimental permafrost thaw but peaked later in deeper soil, reflecting the seasonally receding thaw front. Deep-rooting species could sequester 15 N added at the base of the ambient active layer in October, which was after root growth had ceased. Deep soil organic matter that has long been locked up in permafrost is thus no longer detached from plant processes upon thaw. Whether via nutrient uptake, carbon storage, or rhizosphere priming, plant root interactions with thawing permafrost soils may feed back on our climate both positively and negatively.

Limited linkages of aboveground and belowground phenology: A study in grape.

PREMISE OF THE STUDY: Plant phenology influences resource utilization, carbon fluxes, and interspecific interactions. Although controls on aboveground phenology have been studied to some degree, controls on root phenology are exceptionally poorly understood. METHODS: We used minirhizotrons to examine the timing of grape root production over 5 yr in Fredonia, New York, USA, in a humid continental climate; and over 3 yr in Oakville, California, USA, in a Mediterranean climate. We used data from previous experiments to examine the relationship of root phenology with aboveground phenology. We compared interannual variability in root and shoot growth and determined the influence of abiotic factors on the timing of root initiation, peak root standing crop, peak root growth rate, and cessation of root growth. KEY RESULTS: Root phenology was not tightly coupled with aboveground phenological periods. Both sites typically had one yearly root flush and high interannual variability in root growth. Root phenology was more variable in California than in New York. In this and other published studies, interannual variation in root phenology was greater than variation in aboveground phenology. The three phenological phases of root growth-root initiation, peak root growth, and root cessation-were related to different suites of abiotic factors. CONCLUSIONS: Root phenology is highly variable among years. Analysis of potential controlling factors over several years suggest that belowground phenological phases should be analyzed separately from each other. If aboveground grape phenology responds differently than belowground phenology to changes in air temperature, global warming may further uncouple the timing of aboveground and belowground growth.

Above- and belowground phenology responses of subtropical Chinese fir (Cunninghamia lanceolata) to soil warming, precipitation exclusion and their interaction.

Plant phenology plays an important role in nutrient cycling and carbon balance in forest ecosystems, but its response to the interaction of global warming and precipitation reduction remains unclear. In this study, an experiment with factorial soil warming (ambient, ambient +5 °C) and precipitation exclusion (ambient, ambient -50 %) was conducted in a subtropical Chinese fir (Cunninghamia lanceolata) plantation. We investigated the effects of soil warming, precipitation exclusion, and their interactions on Chinese fir phenology involving tree height and fine root growth. In the meantime, the impact of tree height growth and related climatic factors on fine root production was also assessed. The results showed that: (1) more variable phenology responses were observed in fine root growth than in tree height growth to the climatic treatments; the duration of fine root growth and tree height growth was significantly reduced by the precipitation exclusion and warming treatment, respectively; phenology differences of fine root and tree height growth caused by the solo warming and precipitation exclusion treatment were further enhanced by the combined treatment; and despite the greater inter-annual phenology stability of tree height growth than that of fine root growth, both of them showed insignificant response to all the climate treatments; (2) asynchrony of phenology between tree height and fine root growth was significantly enlarged by solo warming and precipitation exclusion treatments, and further enlarged by the combined treatment; (3) fine root production was significantly and positively correlated with air, and soil temperature, and tree height growth as well, which was altered by warming and precipitation exclusion treatments. Our results demonstrated that climatic changes significantly and differently alter phenology of, and extend the phenology asynchrony between, above and below ground plant components, and also highlight the climate-sensitive and variable nature of root phenology. Overall, these phenology responses to climatic change may weaken the close link between fine root production and tree height growth, which may result in temporal mismatch between nutrient demand and supply in Chinese fir plantation.

Responses of root phenology in ecotypes of Eriophorum vaginatum to transplantation and warming in the Arctic.

The effect of climate change on phenology and growth is less understood for belowground plant tissues than for aboveground plant tissues, particularly in high-latitude regions. Ecotypes within a species adapted to a locality may display different responses to climate change. We established two common garden plots in the Arctic tundra north of the Brooks Range in northern Alaska. Three ecotypes of Eriophorum vaginatum along a latitudinal gradient were transplanted into common gardens, and half of the transplants were warmed using open-top chambers (OTCs). Minirhizotrons were used to track the root phenology during the growing seasons of 2016 and 2017. Warming with OTCs (approximately +1 °C in air) did not affect the root biomass, root production or root phenology. The southern ecotype (from 67°16'N) of Eriophorum vaginatum transplanted northward experienced delayed startup and root production compared to two northern ecotypes (from 68°38'N and 69°25'N), although significant differences were not observed in the three ecotypes in terms of root production, root biomass and growth duration at the two sites. Our results suggest that as the climate warms, ecotypes of Eriophorum vaginatum may be able to adjust their duration of root growth and root productivity by phenotypic plasticity, although the degree of plasticity controlling the root startup time may vary between southern and northern ecotypes.

Separating the effects of air and soil temperature on silver birch. Part I. Does soil temperature or resource competition determine the timing of root growth?

The aboveground parts of boreal forest trees mostly grow earlier, and the roots later, in the growing season. We aimed to experimentally test whether the extrinsic driver of soil temperature or the intrinsic driver (resource competition between plant parts) is a more important control for the root and shoot growth of silver birch (Betula pendula Roth) seedlings. Sixteen two-year-old seedlings were grown in controlled environment rooms for two simulated growing seasons (GS1, GS2). In GS1, all the seedlings were acclimatized under the same conditions, but in GS2, the soil temperature treatments were: (i) constant 10 °C (Cool); (ii) constant 18 °C (Warm); (iii) early growing season at 10 °C, switched to 18 °C later (Early Cool Late Warm, ECLW) and (iv) early growing season 18 °C, switched to 10 °C later (Early Warm Late Cool, EWLC). The treatments did not affect growth allocation between shoots and roots. Warm soil benefitted shoot elongation as it slowed down in EWLC and accelerated in ECLW after the soil temperature switch. However, whole-tree biomasses were similar to Cool and the seedlings grew largest in Warm. Phenology was not strongly affected by soil temperature, and root and shoot growth did not usually peak simultaneously. Short root mortality increased strongly in ECLW and decreased in EWLC after the soil temperature switch. Long root longevity was not significantly affected but long root growth ceased earliest in ECLW. Soil warming increased foliar nutrient contents. Growth dynamics were not solely driven by soil temperature, but resource competition also played a significant role. The study showed the importance of soil temperature for fine root dynamics not only through root growth but also via root mortality, as soil warming increased mortality even more than growth. Soil temperature has complex effects on tree and soil functioning, which further affects carbon dynamics in forest ecosystems that have a climate feedback.

Temperature and moisture dependence of daily growth of Scots pine (Pinus sylvestris L.) roots in Southern Finland.

Scots pine (Pinus sylvestris L.) is one of the most important conifers in Northern Europe. In boreal forests, over one-third of net primary production is allocated to roots. Pioneer roots expand the horizontal and vertical root systems and transport nutrients and water from belowground to aboveground. Fibrous roots, often colonized by mycorrhiza, emerge from the pioneer roots and absorb water and nutrients from the soil. In this study, we installed three flatbed scanners to detect the daily growth of both pioneer and fibrous roots of Scots pine during the growing season of 2018, a year with an unexpected summer drought in Southern Finland. The growth rate of both types of roots had a positive relationship with temperature. However, the relations between root elongation rate and soil moisture differed significantly between scanners and between root types indicating spatial heterogeneity in soil moisture. The pioneer roots were more tolerant to severe environmental conditions than the fibrous roots. The pioneer roots initiated elongation earlier and ceased it later than the fibrous roots. Elongation ended when the temperature dropped below the threshold temperature of 4 °C for pioneer roots and 6 °C for fibrous roots. During the summer drought, the fibrous roots halted root surface area growth at the beginning of the drought, but there was no drought effect on the pioneer roots over the same period. To compare the timing of root production and the aboveground organs' production, we used the CASSIA model, which estimates the aboveground tree carbon dynamics. In this study, root growth started and ceased later than growth of aboveground organs. Pioneer roots accounted for 87% of total root productivity. We suggest that future carbon allocation models should separate the roots by root types (pioneer and fibrous), as their growth patterns are different and they have different reactions to changes in the soil environment.

Remarkable Similarity in Timing of Absorptive Fine-Root Production Across 11 Diverse Temperate Tree Species in a Common Garden.

Long-term minirhizotron observations of absorptive fine roots provide insights into seasonal patterns of belowground root production and carbon dynamics. Our objective was to compare root dynamics over time across mature individuals of 11 temperate trees species: five evergreen and six deciduous. We analyzed the timing and growth on 1st-and 2nd-order roots in minirhizotron images down to a vertical depth of 35 cm, as well as monthly and total annual length production. Production patterns were related to total annual precipitation of the actual and previous year of root production over 6 years. The main or largest peak of annual fine-root production occurred between June and September for almost all species and years. In most years, when peaks occurred, the timing of peak root production was synchronized across all species. A linear mixed model revealed significant differences in monthly fine-root length production across species in certain years (species x year, P < 0.0001), which was strongly influenced by three tree species. Total annual root production was much higher in 2000-2002, when there was above-average rainfall in the previous year, compared with production in 2005-2007, which followed years of lower-than-average rainfall (2003-2006). Compared to the wetter period all species experienced a decline of at least 75% in annual production in the drier years. Total annual root length production was more strongly associated with previous year's (P < 0.001) compared with the actual year's precipitation (P = 0.003). Remarkably similar timing of monthly absorptive fine-root growth can occur across multiple species of diverse phylogeny and leaf habit in a given year, suggesting a strong influence of extrinsic factors on absorptive fine-root growth. The influence of previous year precipitation on annual absorptive fine-root growth underscores the importance of legacy effects in biological responses and suggests that a growth response of temperate trees to extreme precipitation or drought events can be exacerbated across years.

Seasonal Patterns of Fine Root Production and Turnover in a Mature Rubber Tree (Hevea brasiliensis Müll. Arg.) Stand- Differentiation with Soil Depth and Implications for Soil Carbon Stocks.

Fine root dynamics is a main driver of soil carbon stocks, particularly in tropical forests, yet major uncertainties still surround estimates of fine root production and turnover. This lack of knowledge is largely due to the fact that studying root dynamics in situ, particularly deep in the soil, remains highly challenging. We explored the interactions between fine root dynamics, soil depth, and rainfall in mature rubber trees (Hevea brasiliensis Müll. Arg.) exposed to sub-optimal edaphic and climatic conditions. A root observation access well was installed in northern Thailand to monitor root dynamics along a 4.5 m deep soil profile. Image-based measurements of root elongation and lifespan of individual roots were carried out at monthly intervals over 3 years. Soil depth was found to have a significant effect on root turnover. Surprisingly, root turnover increased with soil depth and root half-life was 16, 6-8, and only 4 months at 0.5, 1.0, 2.5, and 3.0 m deep, respectively (with the exception of roots at 4.5 m which had a half-life similar to that found between depths of 1.0 and 2.5 m). Within the first two meters of the soil profile, the highest rates of root emergence occurred about 3 months after the onset of the rainy season, while deeper in the soil, root emergence was not linked to the rainfall pattern. Root emergence was limited during leaf flushing (between March and May), particularly within the first two meters of the profile. Between soil depths of 0.5 and 2.0 m, root mortality appeared independent of variations in root emergence, but below 2.0 m, peaks in root emergence and death were synchronized. Shallow parts of the root system were more responsive to rainfall than their deeper counterparts. Increased root emergence in deep soil toward the onset of the dry season could correspond to a drought acclimation mechanism, with the relative importance of deep water capture increasing once rainfall ceased. The considerable soil depth regularly explored by fine roots, even though significantly less than in surface layers in terms of root length density and biomass, will impact strongly the evaluation of soil carbon stocks.