Marcin Zadworny

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes.

Fine roots acquire essential soil resources and mediate biogeochemical cycling in terrestrial ecosystems. Estimates of carbon and nutrient allocation to build and maintain these structures remain uncertain because of the challenges of consistently measuring and interpreting fine-root systems. Traditionally, fine roots have been defined as all roots ≤ 2 mm in diameter, yet it is now recognized that this approach fails to capture the diversity of form and function observed among fine-root orders. Here, we demonstrate how order-based and functional classification frameworks improve our understanding of dynamic root processes in ecosystems dominated by perennial plants. In these frameworks, fine roots are either separated into individual root orders or functionally defined into a shorter-lived absorptive pool and a longer-lived transport fine-root pool. Using these frameworks, we estimate that fine-root production and turnover represent 22% of terrestrial net primary production globally - a c. 30% reduction from previous estimates assuming a single fine-root pool. Future work developing tools to rapidly differentiate functional fine-root classes, explicit incorporation of mycorrhizal fungi into fine-root studies, and wider adoption of a two-pool approach to model fine roots provide opportunities to better understand below-ground processes in the terrestrial biosphere.

Decomposition of the finest root branching orders : linking belowground dynamics to fine-root function and structure

Root turnover is fastest in the finest roots of the root system (first root order). Additionally, tissue chemistry varies among even the finest root orders and between white roots and older, pigmented roots. Yet the effects of pigmentation and order on root decomposition have rarely been examined. We separated the first four root orders (all <1 mm) of four temperate tree species into three classes: white first- and second-order roots; pigmented first- and second-order roots; and pigmented third- and fourth-order roots. Roots were enclosed in litterbags and buried under their own and under a common species canopy in a 34-year-old common garden in Poland. When comparing decomposition of different root orders over 36 months, pigmented third- and fourth-order roots with a higher C:N ratio decomposed more rapidly, losing 20–40% of their mass, than pigmented first- and second-order roots, which lost no more than 20%. When comparing decomposition of roots of different levels of pigmentation within the same root ...

Contrasting the morphology, anatomy and fungal colonization of new pioneer and fibrous roots

Not all roots born as first-order branches are the same and this has important consequences for overall function. We hypothesized that, compared with fibrous roots, pioneer roots are built to live longer at the expense of absorptive capacity. We tested this hypothesis by investigating pioneer and fibrous roots in their first 14 d of life in the arbuscular mycorrhizal tree species: Acer negundo, Acer saccharum, Juglans nigra, Liriodendron tulipifera and Populus tremuloides. Root observations were made with root-access boxes that allowed roots to be sampled at known ages in field-grown trees. Compared to fibrous roots, pioneer roots had larger diameter, lower specific root length, greater average length and a lack of mycorrhizal or nonmycorrhizal fungal colonization. Pioneer roots < 14 d old had more layers of hypodermis with a lower percentage of putative passage cells and more protoxylem groups than similar age fibrous roots. Our results suggest that pioneer roots are constructed for defense against biotic and abiotic challenges, exploration of soil distal to the stem, high fibrous root branching and secondary development with high axial hydraulic conductivity at the expense of mycorrhizal colonization and high absorptive capacity for water and nutrients.

Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest

The identification of plant functional traits that can be linked to ecosystem processes is of wide interest, especially for predicting vegetational responses to climate change. Root diameter of the finest absorptive roots may be one plant trait that has wide significance. Do species with relatively thick absorptive roots forage in nutrient-rich patches differently from species with relatively fine absorptive roots? We measured traits related to nutrient foraging (root morphology and architecture, root proliferation, and mycorrhizal colonization) across six coexisting arbuscular mycorrhizal (AM) temperate tree species with and without nutrient addition. Root traits such as root diameter and specific root length were highly correlated with root branching intensity, with thin-root species having higher branching intensity than thick-root species. In both fertilized and unfertilized soil, species with thin absorptive roots and high branching intensity showed much greater root length and mass proliferation but lower mycorrhizal colonization than species with thick absorptive roots. Across all species, fertilization led to increased root proliferation and reduced mycorrhizal colonization. These results suggest that thin-root species forage more by root proliferation, whereas thick-root species forage more by mycorrhizal fungi. In mineral nutrient-rich patches, AM trees seem to forage more by proliferating roots than by mycorrhizal fungi.

Avoiding transport bottlenecks in an expanding root system: Xylem vessel development in fibrous and pioneer roots under field conditions

PREMISE OF THE STUDY Root systems develop to effectively absorb water and nutrients and to rapidly transport these materials to the transpiring shoot. In woody plants, roots can be born with different functions: fibrous roots are primarily used for water and nutrient absorption, whereas pioneer roots have a greater role in transport. Because pioneer roots extend rapidly in the soil and typically quickly produce fibrous roots, they need to develop transport capacity rapidly so as to avoid becoming a bottleneck to the absorbed water of the developing fibrous roots and, as we hypothesized, immediately activate a specific type of autophagy at a precise time of their development. METHODS Using microscopy techniques, we monitored xylem development in Populus trichocarpa roots in the first 7 d after emergence under field conditions. KEY RESULTS Newly formed pioneer roots contained more primary xylem poles and had larger diameter tracheary elements than fibrous roots. While xylogenesis started later in pioneer roots than in fibrous, it was completed at the same time, resulting in functional vessels on the third to fourth day following root emergence. Programmed cell death was responsible for creating the water conducting capacity of xylem. Although the early xylogenesis processes were similar in fibrous and pioneer roots, secondary vascular development proceeded much more rapidly in pioneer roots. CONCLUSIONS Compared to fibrous roots, rapid development of transport capacity in pioneer roots is not primarily caused by accelerated xylogenesis but by larger and more numerous tracheary elements and by rapid initiation of secondary growth.

Behaviour of the hyphae of Laccaria laccata in the presence of Trichoderma harzianum in vitro

The growth rate and the behaviour of Laccaria laccata and Trichoderma harzianum hyphae in co-culture and in the rhizosphere of 3-month-old Pinus sylvestris seedlings grown in vitro were investigated. In the interaction zone, hyphae of L. laccata became more pigmented and formed short branches growing towards the hyphae of the saprobic fungus, coiled around them and penetrated sporadically. Vacuolated hyphae of T. harzianum showed protoplasm granulation and breaks in walls followed by release of protoplasts. In the rhizosphere, the mantle hyphae of L. laccata showed a tendency to surround conidia of T. harzianum. No obvious penetration of the conidial walls by the hyphae of the mycorrhizal fungus was observed by scanning electron microscopy. Instead, in rare cases, the hyphae of L. laccata showed marked wrinkles, and a partial degradation of a mucilaginous material covering the mantle appeared to occur.

Building a better foundation: improving root-trait measurements to understand and model plant and ecosystem processes

Trait-based approaches provide a useful framework to investigate plant strategies for resource acquisition, growth, and competition, as well as plant impacts on ecosystem processes. Despite significant progress capturing trait variation within and among stems and leaves, identification of trait syndromes within fine-root systems and between fine roots and other plant organs is limited. Here we discuss three underappreciated areas where focused measurements of fine-root traits can make significant contributions to ecosystem science. These include assessment of spatiotemporal variation in fine-root traits, integration of mycorrhizal fungi into fine-root-trait frameworks, and the need for improved scaling of traits measured on individual roots to ecosystem-level processes. Progress in each of these areas is providing opportunities to revisit how below-ground processes are represented in terrestrial biosphere models. Targeted measurements of fine-root traits with clear linkages to ecosystem processes and plant responses to environmental change are strongly needed to reduce empirical and model uncertainties. Further identifying how and when suites of root and whole-plant traits are coordinated or decoupled will ultimately provide a powerful tool for modeling plant form and function at local and global scales.

Link between defoliation and light treatments on root vitality of five understory shrubs with different resistance to insect herbivory

Understory shrubs are frequently attacked by insect herbivores. However, very little is known regarding possible interactions between light condition, defoliation (D) and fine root vitality (% live roots) and metabolic activity, and whether different plant strategies (compensation, trade-off and equilibrium) to defoliation depend on individual species light requirements. To explore the response of roots to such conditions, an experiment was established in which we experimentally removed 50% of leaves in 1-year-old seedlings of Sambucus nigra, Cornus sanguinea, Prunus serotina, Frangula alnus and Corylus avellana grown in 15% and full sunlight. On average, defoliation leads to a 15% reduction in fine root (< 2 mm) vitality (% live roots). However, a statistically significant reduction in root vitality after defoliation was detected only in those species that are less herbivorized in nature (48% in S. nigra and 5% in C. sanguinea). On average, shade conditions (L) resulted in 18% decline in root vitality, and the effects of defoliation were also 22% higher than for plants grown in full light. Root vitality in both treatments (D and L) was significantly correlated with their dry mass, concentration of total phenol (TPh) and carbon to nitrogen ratio, and negatively correlated with nitrogen, soluble carbohydrates, starch and total non-structural carbohydrates (TNC). To a large extent, root vitality and chemistry varied by species. Higher root vitality was related to higher concentrations of phenolics, more than to N and TNC concentrations. Concentrations of phenolics also differed significantly between defoliated plants and controls. However, in defoliated plants, an increase in TPh was observed only in two species, which belong to two different groups in light requirements and susceptibility to insect grazing (C. sanguinea and P. serotina). This study indicated that higher vitality of roots occurred in species that are characterized by higher insect defoliation under natural conditions. It is likely that higher root vitality of these species was related to their high level of TPh and tannins. This was especially noticeable for the reduced light treatment, which represents natural conditions under which insect defoliation is highest. Our results suggest that varied strategies of resource allocation were used by the different species in response to variations in light and defoliation.

Lignin and lignans in plant defence: Insight from expression profiling of cinnamyl alcohol dehydrogenase genes during development and following fungal infection in Populus

Cinnamyl alcohol dehydrogenase (CAD) catalyses the final step in the biosynthesis of monolignol, the main component of lignin. Lignins, deposited in the secondary cell wall, play a role in plant defence against pathogens. We re-analysed the phylogeny of CAD/CAD-like genes using sequences from recently sequenced genomes, and analysed the temporal and spatial expression profiles of CAD/CAD-like genes in Populus trichocarpa healthy and infected plants. Three fungal pathogens (Rhizoctonia solani, Fusarium oxysporum, and Cytospora sp.), varying in lifestyle and pathogenicity, were used for plant infection. Phylogenetic analyses showed that CAD/CAD-like genes were distributed in classes represented by all members from angiosperm lineages including basal angiosperms and Selaginella. The analysed genes showed different expression profiles during development and demonstrated that three genes were involved in primary xylem maturation while five may function in secondary xylem formation. Expression analysis following inoculation with fungal pathogens, showed that five genes were induced in either stem or leaves. These results add further evidence that CAD/CAD-like genes have evolved specialised functions in plant development and defence against various pest and pathogens. Two genes (PoptrCAD11 and PoptrCAD15), which were induced under various stresses, could be treated as universal markers of plant defence using lignification or lignan biosynthesis.

Seasonal variation in chemistry, but not morphology, in roots of Quercus robur growing in different soil types

Patterns of root traits among different root orders and their variation across seasons are of considerable importance for soil resource acquisition and partitioning in forest ecosystems. We evaluated whether morphological, anatomical and biochemical traits varied among root orders of Quercus robur (L.) sampled across spring, summer and fall seasons and growing in two different soil types with contrasting site fertility. We found no consistent differences in root diameter and specific root length in relation to soil type or growing season. There was, however, a strong seasonal variation in patterns of nitrogen (N) concentration among root orders. During spring and summer, N concentration was highest in the most distal, absorptive portion of the root system. At the end of the growing season, we observed a sharp decline in the N concentration of these lower-order, absorptive roots and an increase in N concentration of the higher-order, transport roots. The specific mechanisms driving the seasonally changing N concentration remain unclear but are likely related to different functions of lower-order roots for absorption and higher-order roots for structure and storage. Future work should identify how common the observed seasonal changes in N concentration are across species and determine what specific environmental cues plants or roots use to trigger shifts in resource allocation within the root branching hierarchy.