BackgroundPhosphorus (P) is an essential element for plant growth and development but it is often a limiting nutrient in soils. Hence, P acquisition from soil by plant roots is a subject of ...considerable interest in agriculture, ecology and plant root biology. Root architecture, with its shape and structured development, can be considered as an evolutionary response to scarcity of resources.ScopeThis review discusses the significance of root architecture development in response to low P availability and its beneficial effects on alleviation of P stress. It also focuses on recent progress in unravelling cellular, physiological and molecular mechanisms in root developmental adaptation to P starvation. The progress in a more detailed understanding of these mechanisms might be used for developing strategies that build upon the observed explorative behaviour of plant roots.ConclusionsThe role of root architecture in alleviation of P stress is well documented. However, this paper describes how plants adjust their root architecture to low-P conditions through inhibition of primary root growth, promotion of lateral root growth, enhancement of root hair development and cluster root formation, which all promote P acquisition by plants. The mechanisms for activating alterations in root architecture in response to P deprivation depend on changes in the localized P concentration, and transport of or sensitivity to growth regulators such as sugars, auxins, ethylene, cytokinins, nitric oxide (NO), reactive oxygen species (ROS) and abscisic acid (ABA). In the process, many genes are activated, which in turn trigger changes in molecular, physiological and cellular processes. As a result, root architecture is modified, allowing plants to adapt effectively to the low-P environment. This review provides a framework for understanding how P deficiency alters root architecture, with a focus on integrated physiological and molecular signalling.
The role of MtCEP1, a member of the CEP (C-terminally encoded peptide) signaling peptide family, was examined in Medicago truncatula root development. MtCEP1 was expressed in root tips, vascular ...tissue, and young lateral organs, and was up-regulated by low nitrogen levels and, independently, by elevated CO2. Overexpressing MtCEP1 or applying MtCEP1 peptide to roots elicited developmental phenotypes: inhibition of lateral root formation, enhancement of nodulation, and the induction of periodic circumferential root swellings, which arose from cortical, epidermal, and pericycle cell divisions and featured an additional cortical cell layer. MtCEP peptide addition to other legume species induced similar phenotypes. The enhancement of nodulation by MtCEP1 is partially tolerant to high nitrate, which normally strongly suppresses nodulation. These nodules develop faster, are larger, and fix more nitrogen in the absence and presence of inhibiting nitrate levels. At 25mM nitrate, nodules formed on pre-existing swelling sites induced by MtCEP1 overexpression. RNA interference-mediated silencing of several MtCEP genes revealed a negative correlation between transcript levels of MtCEP1 and MtCEP2 with the number of lateral roots. MtCEP1 peptide-dependent phenotypes were abolished or attenuated by altering or deleting key residues in its 15 amino acid domain. RNA-Seq analysis revealed that 89 and 116 genes were significantly up- and down-regulated, respectively, by MtCEP1 overexpression, including transcription factors WRKY, bZIP, ERF, and MYB, homologues of LOB29, SUPERROOT2, and BABY BOOM. Taken together, the data suggest that the MtCEP1 peptide modulates lateral root and nodule development in M. truncatula.
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.
Biological nitrogen fixation in legumes occurs in nodules that are initiated in the root cortex following Nod factor recognition at the root surface, and this requires coordination of diverse ...developmental programs in these different tissues. We show that while early Nod factor signaling associated with calcium oscillations is limited to the root surface, the resultant activation of Nodule Inception (NIN) in the root epidermis is sufficient to promote cytokinin signaling and nodule organogenesis in the inner root cortex. NIN or a product of its action must be associated with the transmission of a signal between the root surface and the cortical cells where nodule organogenesis is initiated. NIN appears to have distinct functions in the root epidermis and the root cortex. In the epidermis, NIN restricts the extent of Early Nodulin 11 (ENOD11) expression and does so through competitive inhibition of ERF Required for Nodulation (ERN1). In contrast, NIN is sufficient to promote the expression of the cytokinin receptor Cytokinin Response 1 (CRE1), which is restricted to the root cortex. Our work in Medicago truncatula highlights the complexity of NIN action and places NIN as a central player in the coordination of the symbiotic developmental programs occurring in differing tissues of the root that combined are necessary for a nitrogen-fixing symbiosis.
BackgroundA hypothetical ideotype is presented to optimize water and N acquisition by maize root systems. The overall premise is that soil resource acquisition is optimized by the coincidence of root ...foraging and resource availability in time and space. Since water and nitrate enter deeper soil strata over time and are initially depleted in surface soil strata, root systems with rapid exploitation of deep soil would optimize water and N capture in most maize production environments.• The ideotype Specific phenes that may contribute to rooting depth in maize include (a) a large diameter primary root with few but long laterals and tolerance of cold soil temperatures, (b) many seminal roots with shallow growth angles, small diameter, many laterals, and long root hairs, or as an alternative, an intermediate number of seminal roots with steep growth angles, large diameter, and few laterals coupled with abundant lateral branching of the initial crown roots, (c) an intermediate number of crown roots with steep growth angles, and few but long laterals, (d) one whorl of brace roots of high occupancy, having a growth angle that is slightly shallower than the growth angle for crown roots, with few but long laterals, (e) low cortical respiratory burden created by abundant cortical aerenchyma, large cortical cell size, an optimal number of cells per cortical file, and accelerated cortical senescence, (f) unresponsiveness of lateral branching to localized resource availability, and (g) low Km and high Vmax for nitrate uptake. Some elements of this ideotype have experimental support, others are hypothetical. Despite differences in N distribution between low-input and commercial maize production, this ideotype is applicable to low-input systems because of the importance of deep rooting for water acquisition. Many features of this ideotype are relevant to other cereal root systems and more generally to root systems of dicotyledonous crops.
Plant roots have greatly diversified in form and function since the emergence of the first land plants, but the global organization of functional traits in roots remains poorly understood. Here we ...analyse a global dataset of 10 functionally important root traits in metabolically active first-order roots, collected from 369 species distributed across the natural plant communities of 7 biomes. Our results identify a high degree of organization of root traits across species and biomes, and reveal a pattern that differs from expectations based on previous studies of leaf traits. Root diameter exerts the strongest influence on root trait variation across plant species, growth forms and biomes. Our analysis suggests that plants have evolved thinner roots since they first emerged in land ecosystems, which has enabled them to markedly improve their efficiency of soil exploration per unit of carbon invested and to reduce their dependence on symbiotic mycorrhizal fungi. We also found that diversity in root morphological traits is greatest in the tropics, where plant diversity is highest and many ancestral phylogenetic groups are preserved. Diversity in root morphology declines sharply across the sequence of tropical, temperate and desert biomes, presumably owing to changes in resource supply caused by seasonally inhospitable abiotic conditions. Our results suggest that root traits have evolved along a spectrum bounded by two contrasting strategies of root life: an ancestral 'conservative' strategy in which plants with thick roots depend on symbiosis with mycorrhizal fungi for soil resources and a more-derived 'opportunistic' strategy in which thin roots enable plants to more efficiently leverage photosynthetic carbon for soil exploration. These findings imply that innovations of belowground traits have had an important role in preparing plants to colonize new habitats, and in generating biodiversity within and across biomes.
The symbiosis between arbuscular mycorrhizal (AM) fungi and plants is evolutionarily widespread. The response of plant growth to inoculation by these fungi (mycorrhizal growth response; MGR) is ...highly variable, ranging from positive to negative. Some of this variation is hypothesized to be associated with root structure and function. Specifically, species with a coarse root architecture, and thus a limited intrinsic capacity to absorb soil nutrients, are expected to derive the greatest growth benefit from inoculation with AM fungi. To test this hypothesis, previously published literature and phylogenetic information were combined in a meta‐analysis to examine the magnitude and direction of relationships among several root architectural traits and MGR. Published studies differed in the magnitude and direction of relationships between root architecture and MGR. However, when combined, the overall relationship between MGR and allocation to roots, root diameter, root hair length and root hair density did not differ significantly from zero. These findings indicate that possessing coarse roots is not necessarily a predictor of plant growth response to AM fungal colonization. Root architecture is therefore unlikely to limit the evolution of variation in MGR.
Summary
In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on ...generating cutting‐edge, meaningful and integrated knowledge. Consideration of the below‐ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below‐ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below‐ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine‐root vs coarse‐root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I–VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers’ views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.
Legume crops related to the model plant Medicago truncatula can adapt their root architecture to environmental conditions, both by branching and by establishing a symbiosis with rhizobial bacteria to ...form nitrogen‐fixing nodules. Soil salinity is a major abiotic stress affecting plant yield and root growth. Previous transcriptomic analyses identified several transcription factors linked to the M. truncatula response to salt stress in roots, including NAC (NAM/ATAF/CUC)‐encoding genes. Over‐expression of one of these transcription factors, MtNAC969, induced formation of a shorter and less‐branched root system, whereas RNAi‐mediated MtNAC969 inactivation promoted lateral root formation. The altered root system of over‐expressing plants was able to maintain its growth under high salinity, and roots in which MtNAC969 was down‐regulated showed improved growth under salt stress. Accordingly, expression of salt stress markers was decreased or induced in MtNAC969 over‐expressing or RNAi roots, respectively, suggesting a repressive function for this transcription factor in the salt‐stress response. Expression of MtNAC969 in central symbiotic nodule tissues was induced by nitrate treatment, and antagonistically affected by salt in roots and nodules, similarly to senescence markers. MtNAC969 RNAi nodules accumulated amyloplasts in the nitrogen‐fixing zone, and were prematurely senescent. Therefore, the MtNAC969 transcription factor, which is differentially affected by environmental cues in root and nodules, participates in several pathways controlling adaptation of the M. truncatula root system to the environment.
Strigolactones (SLs) or their derivatives have recently been defined as novel phytohormones that regulate root development. However, it remains unclear whether SLs mediate root growth in response to ...phosphorus (P) and nitrogen (N) deficiency. In this study, the responses of root development in rice (Oryza sativa L.) to different levels of phosphate and nitrate supply were investigated using wild type (WT) and mutants defective in SL synthesis (d10 and d27) or insensitive to SL (d3). Reduced concentration of either phosphate or nitrate led to increased seminal root length and decreased lateral root density in WT. Limitation of either P or N stimulated SL production and enhanced expression of D10, D17, and D27 and suppressed expression of D3 and D14 in WT roots. Mutation of D10, D27, or D3 caused loss of sensitivity of root response to P and N deficiency. Application of the SL analogue GR24 restored seminal root length and lateral root density in WT and d10 and d27 mutants but not in the d3 mutant, suggesting that SLs were induced by nutrient-limiting conditions and led to changes in rice root growth via D3. Moreover, P or N deficiency or GR24 application reduced the transport of radiolabelled indole-3-acetic acid and the activity of DR5::GUS auxin reporter in WT and d10 and d27 mutants. These findings highlight the role of SLs in regulating rice root development under phosphate and nitrate limitation. The mechanisms underlying this regulatory role involve D3 and modulation of auxin transport from shoots to roots.
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