This special issue, originating from the ‘Roots to Global Food Security’ meeting at the SEB Annual Meeting in Manchester (2–4 July 2014), not only showcases fundamental science in root growth regulation, root-to-shoot signalling, and crop management, but also demonstrates its importance in securing global food supplies. Many of the authors of the articles collected herein conducted their PhD studies or research within Bill Davies’ group, and a significant feature of this group is the number of PhD graduates who have gone on to forge significant scientific and publishing careers of their own throughout the world. This meeting provided not only an opportunity to discuss issues of scientific importance to Bill, but, once again, to draw together colleagues who have benefited from his friendship and guidance over the years.
Strigolactones are a new group of plant hormones that suppress shoot branching. In roots, they regulate primary-root growth and lateral-root formation and increase root-hair elongation. Reception of strigolactones occurs via a specific cellular system which includes a D14-like/MAX2-like/SCF complex that, upon perception of strigolactone signalling, leads to certain degradation of receptors and to the release of downstream targets. This signalling pathway may eventually result in changes in actin-filament bundling, cellular trafficking, and PIN localization in the plasma membrane. As a result, auxin flux may be regulated in the shoot or root. Strigolactones are also involved with the response to phosphate conditions in roots, acting by both dampening auxin transport via depletion of PIN2 from the plasma membrane and inducing TIR1 transcription to increase auxin perception. In these instances and, possibly, others, strigolactones manipulate the auxin pathway, affecting its transport, perception or both. However, other mechanisms for strigolactone-regulated plant development and the involvement of other plant hormones are evident.
Nitric oxide (NO) is a gaseous reactive oxygen species (ROS) that has evolved as a signaling hormone in many physiological processes in animals. In plants it has been demonstrated to be a crucial regulator of development, acting as a signaling molecule present at each step of the plant life cycle. NO has also been implicated as a signal in biotic and abiotic responses of plants to the environment. Remarkably, despite this plethora of effects and functional relationships, the fundamental knowledge of NO production, sensing, and transduction in plants remains largely unknown or inadequately characterized. In this review we cover the current understanding of NO production, perception, and action in different physiological scenarios. We especially address the issues of enzymatic and chemical generation of NO in plants, NO sensing and downstream signaling, namely the putative cGMP and Ca2+ pathways, ion-channel activity modulation, gene expression regulation, and the interface with other ROS, which can have a profound effect on both NO accumulation and function. We also focus on the importance of NO in cell–cell communication during developmental processes and sexual reproduction, namely in pollen tube guidance and embryo sac fertilization, pathogen defense, and responses to abiotic stress.
Barley (Hordeum vulgare ssp. vulgare) is an excellent model for understanding agricultural responses to climate change. Its initial domestication over 10 millennia ago and subsequent wide migration provide striking evidence of adaptation to different environments, agro-ecologies and uses. A bottleneck in the selection of modern varieties has resulted in a reduction in total genetic diversity and a loss of specific alleles relevant to climate-smart agriculture. However, extensive and well-curated collections of landraces, wild barley accessions (H. vulgaressp. spontaneum) and other Hordeum species exist and are important new allele sources. A wide range of genomic and analytical tools have entered the public domain for exploring and capturing this variation, and specialized populations, mutant stocks and transgenics facilitate the connection between genetic diversity and heritable phenotypes. These lay the biological, technological and informational foundations for developing climate-resilient crops tailored to specific environments that are supported by extensive environmental and geographical databases, new methods for climate modelling and trait/environment association analyses, and decentralized participatory improvement methods. Case studies of important climate-related traits and their constituent genes – including examples that are indicative of the complexities involved in designing appropriate responses – are presented, and key developments for the future highlighted.
Growing agricultural demands in the face of impending inorganic phosphate (Pi) shortages underscore a need for a better understanding of plant development under conditions of Pi deprivation. Pi is an essential nutrient that is a major component of fertilizer. Plants have evolved strategies to improve the acquisition of this nutrient by altering root development under shortage conditions. We show that signaling peptides thought to act redundantly in Arabidopsis thaliana development have distinct functions in response to Pi deprivation. Using microscopy and confocal imaging, roots were analyzed for growth rate and cellular composition. Using expression microarrays, genes influencing development in response to phosphate deprivation were identified. ROOT GROWTH FACTOR1 (RGF1) and RGF2 influenced different aspects of root development under conditions of Pi deprivation. We found that RGF2 influenced the longitudinal growth rate in the primary root in response to Pi deprivation, whereas RGF1 affected circumferential cell number in the root meristem. These data suggest that the mechanisms controlling adaptive development can depend on disparate functions of genes thought to act redundantly, thus elucidating new functions for important developmental regulators.
Most scientific research is publicly funded, and yet we have to pay to access it. This absurd situation should not be allowed to continue. (...) - Magazine Ouishare, by Sara Rodriguez Marin, 25 February 2015
The quest to determine the genetic basis of root system architecture (RSA) has been greatly facilitated by recent developments in root phenotyping techniques. Methods that are accurate, high throughput, and control for environmental factors are especially attractive for quantitative trait locus mapping. Here, we describe the adaptation of a nondestructive in vivo gel-based root imaging platform for use in maize (Zea mays). We identify a large number of contrasting RSA traits among 25 founder lines of the maize nested association mapping population and locate 102 quantitative trait loci using the B73 (compact RSA) × Ki3 (exploratory RSA) mapping population. Our results suggest that a phenotypic tradeoff exists between small, compact RSA and large, exploratory RSA.
Heat stress is a major limiting factor of grapevine production and quality. Acclimation and recovery are essential to ensure plant survival, and the recovery mechanisms can be independent of the heat response mechanisms. An experimental set up with and without acclimation to heat followed by recovery [stepwise acclimation and recovery (SAR) and stepwise recovery (SR), respectively] was applied to two grapevine varieties, Touriga Nacional (TN), and Trincadeira (TR), with different tolerance to abiotic stress. Major differences were found between leaves of SAR and SR, especially after recovery; in SAR, almost all parameters returned to basal levels while in SR they remained altered. Acclimation led to a swifter and short-term antioxidative response, affecting the plant to a lesser extent than SR. Significant differences were found among varieties: upon stress, TN significantly increased ascorbate and glutathione reduction levels, boosting the cell's redox-buffering capacity, while TR needed to synthesize both metabolites, its response being insufficient to keep the redox state at working levels. TR was affected by stress for a longer period and the up-regulation pattern of antioxidative stress genes was more obvious. In TN, heat shock proteins were significantly induced, but the canonical heat-stress gene signature was not evident probably because no shutdown of the housekeeping metabolism was needed.
Root-knot nematodes (RKNs) are ubiquitous parasites with an amazing capacity to interact with a very large variety of plant species. They are sedentary endoparasitic nematodes that depend on the induction of a permanent feeding site in living roots to complete their life cycle. RKNs interfere with the genetic programmes of their hosts to transform root vascular cells into giant cells (GCs) through the injection of nematode effectors from their oesophageal glands. Dramatic rearrangements in GCs cytoskeleton, alteration of cell cycle mechanisms, such as mitosis and endoreduplication, readjustment of enzymes involved in carbohydrate synthesis and degradation are among those processes modified in GCs. GCs act as sinks to provide nutrients for life cycle completion from J2 larvae to adult females. The female produces an egg offspring protected by a gelatinous matrix and the free-living stage, J2, hatch from these eggs, completing the nematode life cycle. The model species Arabidopsis thaliana allowed easy in vivo observations of the interaction by video-enhanced contrast light microscopy on infected roots, and the wide range of existing genetic and molecular tools of this plant model has extended its use. Holistic approaches to tackle gene expression combined with cell biology techniques, as isolation of GCs by laser capture microdissection, allowed GC-specific transcriptomic analysis, generating vast lists of differentially expressed genes. However, the design of consistent functional hypothesis about these genes and their products will require the development of in silico analysis tools for comparisons among the transcriptomes of plant–nematode compatible interactions. The understanding of the processes subjacent to GC differentiation and maintenance, as well as a deeper knowledge of RKN mode of parasitism, will provide tools for new control methods of these devastating agricultural pests.
Grapevine is a well-studied, economically relevant crop, whose associated bacteria could influence its organoleptic properties. In this study, the spatial and temporal dynamics of the bacterial communities associated with grapevine organs (leaves, flowers, grapes, and roots) and soils were characterized over two growing seasons to determine the influence of vine cultivar, edaphic parameters, vine developmental stage (dormancy, flowering, preharvest), and vineyard. Belowground bacterial communities differed significantly from those aboveground, and yet the communities associated with leaves, flowers, and grapes shared a greater proportion of taxa with soil communities than with each other, suggesting that soil may serve as a bacterial reservoir. A subset of soil microorganisms, including root colonizers significantly enriched in plant growth-promoting bacteria and related functional genes, were selected by the grapevine. In addition to plant selective pressure, the structure of soil and root microbiota was significantly influenced by soil pH and C:N ratio, and changes in leaf- and grape-associated microbiota were correlated with soil carbon and showed interannual variation even at small spatial scales. Diazotrophic bacteria, e.g., Rhizobiaceae and Bradyrhizobium spp., were significantly more abundant in soil samples and root samples of specific vineyards. Vine-associated microbial assemblages were influenced by myriad factors that shape their composition and structure, but the majority of organ-associated taxa originated in the soil, and their distribution reflected the influence of highly localized biogeographic factors and vineyard management.
The female flower of hop (Humulus lupulus var. lupulus) is an essential ingredient that gives characteristic aroma, bitterness and durability/stability to beer. However, the molecular genetic basis for identifying DNA markers in hop for breeding and to study its domestication has been poorly established. Here, we provide draft genomes for two hop cultivars [cv. Saazer (SZ) and cv. Shinshu Wase (SW)] and a Japanese wild hop [H. lupulus var. cordifolius; also known as Karahanasou (KR)]. Sequencing and de novo assembly of genomic DNA from heterozygous SW plants generated scaffolds with a total size of 2.05 Gb, corresponding to approximately 80% of the estimated genome size of hop (2.57 Gb). The scaffolds contained 41,228 putative protein-encoding genes. The genome sequences for SZ and KR were constructed by aligning their short sequence reads to the SW reference genome and then replacing the nucleotides at single nucleotide polymorphism (SNP) sites. De novoRNA sequencing (RNA-Seq) analysis of SW revealed the developmental regulation of genes involved in specialized metabolic processes that impact taste and flavor in beer. Application of a novel bioinformatics tool, phylogenetic comparative RNA-Seq (PCP-Seq), which is based on read depth of genomic DNAs and RNAs, enabled the identification of genes related to the biosynthesis of aromas and flavors that are enriched in SW compared to KR. Our results not only suggest the significance of historical human selection process for enhancing aroma and bitterness biosyntheses in hop cultivars, but also serve as crucial information for breeding varieties with high quality and yield.
Iron (Fe) homeostasis is integrated with the production of reactive oxygen species (ROS), and distribution at the root tip participates in the control of root growth. Excess Fe increases ferritin abundance, enabling the storage of Fe, which contributes to protection of plants against Fe-induced oxidative stress. AtFer1 and AtFer3 are the two ferritin genes expressed in the meristematic zone, pericycle and endodermis of the Arabidopsis thaliana root, and it is in these regions that we observe Fe stained dots. This staining disappears in the triple fer1-3-4 ferritin mutant. Fe excess decreases primary root length in the same way in wild-type and in fer1-3-4 mutant. In contrast, the Fe-mediated decrease of lateral root (LR) length and density is enhanced in fer1-3-4 plants due to a defect in LR emergence. We observe that this interaction between excess Fe, ferritin, and root system architecture (RSA) is in part mediated by the H2O2/O2·− balance between the root cell proliferation and differentiation zones regulated by the UPB1 transcription factor. Meristem size is also decreased in response to Fe excess in ferritin mutant plants, implicating cell cycle arrest mediated by the ROS-activated SMR5/SMR7 cyclin-dependent kinase inhibitors pathway in the interaction between Fe and RSA.
Upland cotton is a model for polyploid crop domestication and transgenic improvement. Here we sequenced the allotetraploid Gossypium hirsutum L. acc. TM-1 genome by integrating whole-genome shotgun reads, bacterial artificial chromosome (BAC)-end sequences and genotype-by-sequencing genetic maps. We assembled and annotated 32,032 A-subgenome genes and 34,402 D-subgenome genes. Structural rearrangements, gene loss, disrupted genes and sequence divergence were more common in the A subgenome than in the D subgenome, suggesting asymmetric evolution. However, no genome-wide expression dominance was found between the subgenomes. Genomic signatures of selection and domestication are associated with positively selected genes (PSGs) for fiber improvement in the A subgenome and for stress tolerance in the D subgenome. This draft genome sequence provides a resource for engineering superior cotton lines.
During vascular development, procambial and cambial cells give rise to xylem and phloem cells. Because the vascular tissue is deeply embedded, it has been difficult to analyze the processes of vascular development in detail. Here, we establish a novel in vitro experimental system in which vascular development is induced in Arabidopsis thaliana leaf-disk cultures using bikinin, an inhibitor of glycogen synthase kinase 3 proteins. Transcriptome analysis reveals that mesophyll cells in leaf disks synchronously turn into procambial cells and then differentiate into tracheary elements. Leaf-disk cultures from plants expressing the procambial cell markers TDRpro:GUS and TDRpro:YFP can be used for spatiotemporal visualization of procambial cell formation. Further analysis with the tdr mutant and TDIF (tracheary element differentiation inhibitory factor) indicates that the key signaling TDIF-TDR-GSK3s regulates xylem differentiation in leaf-disk cultures. This new culture system can be combined with analysis using the rich material resources for Arabidopsis including cell-marker lines and mutants, thus offering a powerful tool for analyzing xylem cell differentiation.
Root clusters are bunches of hairy rootlets that enhance nutrient uptake among many plants. Since first being reported in 1974, the involvement of rhizobacteria in their formation has received conflicting support. Attempts to identify specific causative organisms have failed and their role has remained speculative. We set up a gnotobiotic experiment using two root-clustered species, Viminaria juncea (Fabaceae) and Hakea laurina (Proteaceae), and inoculated them with two plant-growth-promoting rhizobacteria (PGPR), Bradyrhizobium elkanii and Bacillus mageratium, that produce indole-3-acetic-acid (IAA). Plants were suspended in water culture with four combinations of nitrogen and phosphorus. Clusters only developed in the presence of PGPR in two treatments, were greatly enhanced in another four, suppressed in five, and unaffected in five. Nitrogen amendment was associated with a higher density of clusters. Bradyrhizobium promoted cluster formation in Hakea, whereas Bacillus promoted cluster formation in Viminaria and suppressed it in Hakea. Greater root cluster numbers were due either to a larger root system induced by PGPR (indirect resource effect) and/or to more clusters per unit length of parent root (direct morphogenetic effect). The results are interpreted in terms of greater IAA production by Bradyrhizobium than Bacillus and greater sensitivity of Viminaria to IAA than Hakea.
Jethro Tull (1674 - 21 February 1741, New Style) was an English agricultural pioneer from Berkshire who helped bring about the British Agricultural Revolution. He perfected a horse-drawn seed drill in 1701 that economically sowed the seeds in neat rows. He later developed a horse-drawn hoe.
RSA is determined by interacting genetic and environmental factors. • RSA can provide growth advantages under different environmental conditions. • Expression of a specific gene regulating RSA can confer a growth advantage. • Drought tolerance in crops has a large genetic component and is correlated to RSA. • RSA is an unexplored research area that could impact food production worldwide.
Andres Zurita's insight:
Root system architecture (RSA) plays a major role in plant fitness, crop performance, and grain yield yet only recently has this role been appreciated. RSA describes the spatial arrangement of root tissue within the soil and is therefore crucial to nutrient and water uptake. Recent studies have identified many of the genetic and environmental factors influencing root growth that contribute to RSA. Some of the identified genes have the potential to limit crop loss caused by environmental extremes and are currently being used to confer drought tolerance. It is hypothesized that manipulating these and other genes that influence RSA will be pivotal for future crop advancements worldwide.
Increase in demand for our primary foodstuffs is outstripping increase in yields, an expanding gap that indicates large potential food shortages by mid-century. This comes at a time when yield improvements are slowing or stagnating as the approaches of the Green Revolution reach their biological limits. Photosynthesis, which has been improved little in crops and falls far short of its biological limit, emerges as the key remaining route to increase the genetic yield potential of our major crops. Thus, there is a timely need to accelerate our understanding of the photosynthetic process in crops to allow informed and guided improvements via in-silico-assisted genetic engineering. Potential and emerging approaches to improving crop photosynthetic efficiency are discussed, and the new tools needed to realize these changes are presented.
Arabidopsis (Arabidopsis thaliana) absorbs inorganic phosphate (Pi) from the soil through an active transport process mediated by the nine members of the PHOSPHATE TRANSPORTER1 (PHT1) family. These proteins share a high level of similarity (greater than 61%), with overlapping expression patterns. The resulting genetic and functional redundancy prevents the analysis of their specific roles. To overcome this difficulty, our approach combined several mutations with gene silencing to inactivate multiple members of the PHT1 family, including a cluster of genes localized on chromosome 5 (PHT1;1, PHT1;2, and PHT1;3). Physiological analyses of these lines established that these three genes, along with PHT1;4, are the main contributors to Pi uptake. Furthermore, PHT1;1 plays an important role in translocation from roots to leaves in high phosphate conditions. These genetic tools also revealed that some PHT1 transporters likely exhibit a dual affinity for phosphate, suggesting that their activity is posttranslationally controlled. These lines display significant phosphate deficiency-related phenotypes (e.g. biomass and yield) due to a massive (80%–96%) reduction in phosphate uptake activities. These defects limited the amount of internal Pi pool, inducing compensatory mechanisms triggered by the systemic Pi starvation response. Such reactions have been uncoupled from PHT1 activity, suggesting that systemic Pi sensing is most probably acting downstream of PHT1.
The effective development of salt tolerant crops requires an understanding that the evolution of halophytes, glycophytes and our major grain crops has involved significantly different processes. Halophytes (and other edaphic endemics) generally arose through colonization of habitats in severe disequilibrium by pre-adapted individuals, rather than by gradual adaptation from populations of ‘glycophytes’. Glycophytes, by contrast, occur in low sodium ecosystems, where sodium was and is the major limiting nutrient in herbivore diets, suggesting that their evolution reflects the fact that low sodium individuals experienced lower herbivory and had higher fitness. For domestication/evolution of crop plants, the selective pressure was human imposed and involved humans co-opting functions of defense and reproductive security. Unintended consequences of this included loss of tolerance to various stresses and loss of the genetic variability needed to correct that. Understanding, combining and manipulating all three modes of evolution are now critical to the development of salt tolerant crops, particularly those that will offer food security in countries with few economic resources and limited infrastructure. Such efforts will require exploiting the genetic structures of recently evolved halophytes, the genetic variability of model plants, and endemic halophytes and ‘minor’ crops that already exist.
The plasticity of root architecture is crucial for plants to acclimate to unfavourable environments including low nitrogen (LN) stress. How maize roots coordinate the growth of axile roots and lateral roots (LRs), as well as longitudinal and radial cell behaviours in response to LN stress, remains unclear. Maize plants were cultivated hydroponically under control (4 mm nitrate) and LN (40 μm) conditions. Temporal and spatial samples were taken to analyse changes in the morphology, anatomical structure and carbon/nitrogen (C/N) ratio in the axile root and LRs. LN stress increased axile root elongation, reduced the number of crown roots and decreased LR density and length. LN stress extended cell elongation zones and increased the mature cell length in the roots. LN stress reduced the cell diameter and total area of vessels and increased the amount of aerenchyma, but the number of cell layers in the crown root cortex was unchanged. The C/N ratio was higher in the axile roots than in the LRs. Maize roots acclimate to LN stress by optimizing the anatomical structure and N allocation. As a result, axile root elongation is favoured to efficiently find available N in the soil.
The development and growth of plants, as well as their successful adaptation to a variety of environments, is highly dependent on the conduction of water, nutrients and other important molecules throughout the plant body. Xylem is a specialized vascular tissue that serves as a conduit of water and minerals and provides mechanical support for upright growth. Wood, also known as secondary xylem, constitutes the major part of mature woody stems and roots. In the past two decades, a number of key factors including hormones, signal transducers and (post)transcriptional regulators have been shown to control xylem formation. We outline the main mechanisms shown to be essential for xylem development in various plant species, with an emphasis on Arabidopsis thaliana, as well as several tree species where xylem has a long history of investigation. We also summarize the processes which have been shown to be instrumental during xylem maturation. This includes mechanisms of cell wall formation and cell death which collectively complete xylem cell fate.
One strategy for sessile plants to adapt to their surrounding environment involves the modulation of their various internal phytohormone signaling and distributions when the plants sense environmental change. There are currently dozens of identified phytohormones in plant cells and they act in concert to regulate plant growth, development, metabolism and defense. It has been determined that phytohormones often act together to achieve certain physiological functions. Thus, the study of hormone–hormone interactions is becoming a competitive research field for deciphering the underlying regulatory mechanisms. Among phytohormones, jasmonate and ethylene present a fascinating case of synergism and antagonism. They are commonly recognized as defense hormones that act synergistically. Plants impaired in jasmonate and/or ethylene signaling are susceptible to infections by necrotrophic fungi, suggesting that these two hormones are both required for defense. Moreover, jasmonate and ethylene also act antagonistically, such as in the regulation of apical hook development and wounding responses. Here, we highlight the recent breakthroughs in the understanding of jasmonate–ethylene co-actions and point out the potential power of studying protein–protein interactions for systematically exploring signal cross-talk.
Climate change is a current global concern and, despite continuing controversy about the magnitude of its effects, has affected the food production systems and supply chain (IPCC, 2014a and IPCC, 2014b). Climate change has an impact not only on crop production or food security (Fischer et al., 2005 and Gregory et al., 2005), but also on food safety, incidence and prevalence of foodborne diseases (Bezirtzoglou et al., 2011, Lal et al., 2012, Miraglia et al., 2009 and Tirado et al., 2010).
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