Key message
This article describes the composition of root exudates, how these metabolites are released to the rhizosphere and their importance in the recruitment of beneficial microbiota that ...alleviate plant stress.
Metabolites secreted to the rhizosphere by roots are involved in several processes. By modulating the composition of the root exudates, plants can modify soil properties to adapt and ensure their survival under adverse conditions. They use several strategies such as (1) changing soil pH to solubilize nutrients into assimilable forms, (2) chelating toxic compounds, (3) attracting beneficial microbiota, or (4) releasing toxic substances for pathogens, etc. In this work, the composition of root exudates as well as the different mechanisms of root exudation have been reviewed. Existing methodologies to collect root exudates, indicating their advantages and disadvantages, are also described. Factors affecting root exudation have been exposed, including physical, chemical, and biological agents which can produce qualitative and quantitative changes in exudate composition. Finally, since root exudates play an important role in the recruitment of mycorrhizal fungi and plant growth-promoting rhizobacteria (PGPR), the mechanisms of interaction between plants and the beneficial microbiota have been highlighted.
SUMMARY
Plants forage soil for water and nutrients, whose distribution is patchy and often dynamic. To improve their foraging activities, plants have evolved mechanisms to modify the physicochemical ...properties and microbial communities of the rhizosphere, i.e. the soil compartment under the influence of the roots. This dynamic interplay in root−soil−microbiome interactions creates emerging properties that impact plant nutrition and health. As a consequence, the rhizosphere can be considered an extended root phenotype, a manifestation of the effects of plant genes on their environment inside and/or outside of the organism. Here, we review current understanding of how plants shape the rhizosphere and the benefits it confers to plant fitness. We discuss future research challenges and how applying their solutions in crops will enable us to harvest the benefits of the extended root phenotype.
Significance Statement
Plants have evolved mechanisms to modify the physicochemical properties and microbial communities of the rhizosphere. Here, we review our current knowledge on how plants create this extended phenotype through root−soil−microbiome interactions and the benefits it confers to plant fitness.
A worldview of root traits Valverde‐Barrantes, Oscar J.; Freschet, Grégoire T.; Roumet, Catherine ...
The New phytologist,
September 2017, Letnik:
215, Številka:
4
Journal Article
Recenzirano
Odprti dostop
Fine-root traits play key roles in ecosystem processes, but the drivers of fine-root trait diversity remain poorly understood. The plant economic spectrum (PES) hypothesis predicts that leaf and root ...traits evolved in coordination. Mycorrhizal association type, plant growth form and climate may also affect root traits. However, the extent to which these controls are confounded with phylogenetic structuring remains unclear.
Here we compiled information about root and leaf traits for > 600 species. Using phylogenetic relatedness, climatic ranges, growth form and mycorrhizal associations, we quantified the importance of these factors in the global distribution of fine-root traits.
Phylogenetic structuring accounts for most of the variation for all traits excepting root tissue density, with root diameter and nitrogen concentration showing the strongest phylogenetic signal and specific root length showing intermediate values. Climate was the second most important factor, whereas mycorrhizal type had little effect. Substantial trait coordination occurred between leaves and roots, but the strength varied between growth forms and clades.
Our analyses provide evidence that the integration of roots and leaves in the PES requires better accounting of the variation in traits across phylogenetic clades. Inclusion of phylogenetic information provides a powerful framework for predictions of belowground functional traits at global scales.
Optimizing root system architecture can overcome yield limitations in crop plants caused by water or nutrient shortages. Classic breeding approaches are difficult because the trait is governed by ...many genes and is difficult to score. We generated transgenic Arabidopsis thaliana and tobacco (Nicotiana tabacum) plants with enhanced root-specific degradation of the hormone cytokinin, a negative regulator of root growth. These transgenic plants form a larger root system, whereas growth and development of the shoot are similar. Elongation of the primary root, root branching, and root biomass formation were increased by up to 60% in transgenic lines, increasing the root-to-shoot ratio. We thus demonstrated that a single dominant gene could regulate a complex trait, root growth. Moreover, we showed that cytokinin regulates root growth in a largely organ-autonomous fashion that is consistent with its dual role as a hormone with both paracrine and long-distance activities. Transgenic plants had a higher survival rate after severe drought treatment. The accumulation of several elements, including S, P, Mn, Mg, Zn, as well as Cd from a contaminated soil, was significantly increased in shoots. Under conditions of sulfur or magnesium deficiency, leaf chlorophyll content was less affected in transgenic plants, demonstrating the physiological relevance of shoot element accumulation. Our approach might contribute to improve drought tolerance, nutrient efficiency, and nutrient content of crop plants.
Despite its relevance for agricultural production, environmental stress-induced growth inhibition, which is responsible for significant yield reductions, is only poorly understood. Here, we ...investigated the molecular mechanisms underlying cell cycle inhibition in young proliferating leaves of the model plant Arabidopsis thaliana when subjected to mild osmotic stress. A detailed cellular analysis demonstrated that as soon as osmotic stress is sensed, cell cycle progression rapidly arrests, but cells are kept in a latent ambivalent state allowing a quick recovery (pause). Remarkably, cell cycle arrest coincides with an increase in 1-aminocyclopropane-1-carboxylate levels and the activation of ethylene signaling. Our work showed that ethylene acts on cell cycle progression via inhibition of cyclin-dependent kinase A activity independently of EIN3 transcriptional control. When the stress persists, cells exit the mitotic cell cycle and initiate the differentiation process (stop). This stop is reflected by early endoreduplication onset, in a process independent of ethylene. Nonetheless, the potential to partially recover the decreased cell numbers remains due to the activity of meristemoids. Together, these data present a conceptual framework to understand how environmental stress reduces plant growth.
A controlled flow of porphyrin metabolites is critical for organisms, but little is known about the control of porphyrin biosynthesis under environmental stress. We monitored transgenic rice (Oryza ...sativa) plants expressing Myxococcus xanthus protoporphyrinogen oxidase (PPO) for their response to drought stress. Transgenic plants showed significantly improved drought tolerance, as indicated by a higher shoot water potential, less oxidative damage, and a more favorable redox balance compared with wild-type plants. Both transgenic and wild-type plants responded to the onset of drought stress, even prior to changes in shoot water potential and oxidative metabolism, by drastically scavenging porphyrin intermediates in leaves, which was crucial for alleviating reactive oxygen species-induced stress. Protoporphyrin IX, protochlorophyHide, magnesiumprotoporphyrin IX, and its methyl ester were absent or hardly detected with the intensification of water stress (-3.1 MPa) in the wild type, whereas transgenic plants retained these intermediates to some extent. Additionally, the expression and activity of most enzymes involved in porphyrin biosynthesis, particularly in the chlorophyll branch, were primarily down-regulated under dehydrating conditions, with stronger repression in the wild type than in transgenic plants. There was up-regulation of Glutamate 1-Semialdehyde Aminotransferase, PPO1, and Fe Chelatasel transcripts in drought-stressed transgenic plants, enabling the transgenic plants to make larger pools of 5-aminolevulinic acid and protoporphyrin IX available for subsequent steps in the heme branch. Overexpression of PPO ultimately protected the transgenic plants from drought-induced cytotoxicity, demonstrating clearly that manipulation of porphyrin biosynthesis can produce drought-tolerant plants. Our results support a possible role for tetrapyrroles in signaling their metabolic state and in plant protection under drought stress conditions.
Limonium bicolor
, a typical recretohalophyte that lives in saline environments, excretes excessive salt to the environment through epidermal salt glands to avoid salt stress. The aim of this study ...was to screen for
L. bicolor
genes involved in salt secretion by high-throughput RNA sequencing. We established the experimental procedure of salt secretion using detached mature leaves, in which the optimal salt concentration was determined as 200 mM NaCl. The detached salt secretion system combined with Illumina deep sequencing were applied. In total, 27,311 genes were annotated using an
L. bicolor
database, and 2040 of these genes were differentially expressed, of which 744 were up-regulated and 1260 were down-regulated with the NaCl versus the control treatment. A gene ontology enrichment analysis indicated that genes related to ion transport, vesicles, reactive oxygen species scavenging, the abscisic acid-dependent signaling pathway and transcription factors were found to be highly expressed under NaCl treatment. We found that 102 of these genes were likely to be involved in salt secretion, which was confirmed using salt-secretion mutants. The present study identifies the candidate genes in the
L. bicolor
salt gland that are highly associated with salt secretion. In addition, a salt-transporting pathway is presented to explain how Na
+
is excreted by the salt gland in
L. bicolor
. These findings will shed light on the molecular mechanism of salt secretion from the salt glands of plants.
Trehalose-6-phosphate (T6P) is a signaling metabolite that regulates carbon metabolism, developmental processes, and growth in plants. In Arabidopsis (Arabidopsis thaliana), T6P signaling is, at ...least in part, mediated through inhibition of the SNF1-related protein kinase SnRKl. To investigate the role of T6P signaling in a heterotrophic, starch-accumulating storage organ, transgenic potato (Solatium tuberosum) plants with altered T6P levels specifically in their tubers were generated. Transgenic lines with elevated T6P levels (B33-TPS, expressing Escherichia coli osmoregulatory trehalose synthesis A OtsA, which encodes a T6P synthase) displayed reduced starch content, decreased ATP contents, and increased respiration rate diagnostic for high metabolic activity. On the other hand, lines with significantly reduced T6P (B33-TPP, expressing E. coli OtsB, which encodes a T6P phosphatase) showed accumulation of soluble carbohydrates, hexose phosphates, and ATP, no change in starch when calculated on a fresh weight basis, and a strongly reduced tuber yield. ¹⁴C Glucose feeding to transgenic tubers indicated that carbon partitioning between starch and soluble carbohydrates was not altered. Transcriptional profiling of B33-TPP tubers revealed that target genes of SnRKl were strongly up-regulated and that T6P inhibited potato tuber SnRKl activity in vitro. Among the SnRKl target genes in B33-TPP tubers, those involved in the promotion of cell proliferation and growth were down-regulated, while an inhibitor of cell cycle progression was up-regulated. T6P-accumulating tubers were strongly delayed in sprouting, while those with reduced T6P sprouted earlier than the wild type. Early sprouting of B33-TPP tubers correlated with a reduced abscisic acid content. Collectively, our data indicate that T6P plays an important role for potato tuber growth.
Since the first ultrastructural investigations of sieve tubes in the early 1960s, their structure has been a matter of debate. Because sieve tube structure defines frictional interactions in the tube ...system, the presence of Ñ protein obstructions shown in many transmission electron micrographs led to a discussion about the mode of phloem transport. At present, it is generally agreed that P protein agglomerations are preparation artifacts due to injury, the lumen of sieve tubes is free of obstructions, and phloem flow is driven by an osmotically generated pressure differential according to Münch's classical hypothesis. Here, we show that the phloem contains a distinctive network of protein filaments. Stable transgenic lines expressing Arabidopsis thaliana Sieve-Element-Occlusion-Related1 (SEORI)-yellow fluorescent protein fusions show that At SEOR1 meshworks at the margins and clots in the lumen are a general feature of living sieve tubes. Live imaging of phloem flow and flow velocity measurements in individual tubes indicate that At SEOR1 agglomerations do not markedly affect or alter flow. A transmission electron microscopy preparation protocol has been generated showing sieve tube ultrastructure of unprecedented quality. A reconstruction of sieve tube ultrastructure served as basis for tube resistance calculations. The impact of agglomerations on phloem flow is discussed.
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