Dataset Information

Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara.

ABSTRACT: Flooding is a common stress factor in both natural and agricultural systems, and affects plant growth by the slow diffusion rate of gases in water. This results in low oxygen concentrations in submerged tissues, and hence in a decreased respiration rate. Understanding the responses of plants to flooding is essential for the management of wetland ecosystems, and may benefit research to improve the flood tolerance of crop species. This study describes the response to partial submergence of bittersweet (Solanum dulcamara). Bittersweet is a Eurasian species that grows both in dry habitats such as coastal dunes, and in wetlands, and therefore is a suitable model plant for studying responses to a variety of environmental stresses. A further advantage is that the species is closely related to flood-intolerant crops such as tomato and eggplant. The species constitutively develops dormant primordia on the stem, which we show to have a predetermined root identity. We investigated adventitious root growth from these primordia during flooding. The synchronized growth of roots from the primordia was detected after 2-3 days of flooding and was due to a combination of cell division and cell elongation. Gene expression analysis demonstrated that the molecular response to flooding began within 2 h and included activation of hypoxia and ethylene signalling genes. Unexpectedly, these early changes in gene expression were very similar in primordia and adjacent stem tissue, suggesting that there is a dominant general response in tissues during early flooding.

SUBMITTER: Dawood T

PROVIDER: S-EPMC3922303 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara.

Dawood Thikra T Rieu Ivo I Wolters-Arts Mieke M Derksen Emiel B EB Mariani Celestina C Visser Eric J W EJ

AoB PLANTS 20140209 0

Flooding is a common stress factor in both natural and agricultural systems, and affects plant growth by the slow diffusion rate of gases in water. This results in low oxygen concentrations in submerged tissues, and hence in a decreased respiration rate. Understanding the responses of plants to flooding is essential for the management of wetland ecosystems, and may benefit research to improve the flood tolerance of crop species. This study describes the response to partial submergence of bitters ...[more]

PMID: 24790121

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Project description:Background and aimsFlooding can occur at any stage of the life cycle of a plant, but often adaptive responses of plants are only studied at a single developmental stage. It may be anticipated that juvenile plants may respond differently from mature plants, as the amount of stored resources may differ and morphological changes can be constrained. Moreover, different water depths may require different strategies to cope with the flooding stress, the expression of which may also depend on developmental stage. This study investigated whether flooding-induced adventitious root formation and plant growth were affected by flooding depth in Solanum dulcamara plants at different developmental stages.MethodsJuvenile plants without pre-formed adventitious root primordia and mature plants with primordia were subjected to shallow flooding or deep flooding for 5 weeks. Plant growth and the timing of adventitious root formation were monitored during the flooding treatments.Key resultsAdventitious root formation in response to shallow flooding was significantly constrained in juvenile S. dulcamara plants compared with mature plants, and was delayed by deep flooding compared with shallow flooding. Complete submergence suppressed adventitious root formation until up to 2 weeks after shoots restored contact with the atmosphere. Independent of developmental stage, a strong positive correlation was found between adventitious root formation and total biomass accumulation during shallow flooding.ConclusionsThe potential to deploy an escape strategy (i.e. adventitious root formation) may change throughout a plant's life cycle, and is largely dependent on flooding depth. Adaptive responses at a given stage of the life cycle thus do not necessarily predict how the plant responds to flooding in another growth stage. As variation in adventitious root formation also correlates with finally attained biomass, this variation may form the basis for variation in resistance to shallow flooding among plants.

Project description:Main conclusionSolanum dulcamara primary and adventitious roots showed qualitative and quantitative differences in their steroidal glycosides profile. This opened new venues to evaluate the bioactivity of these molecules in belowground ecosystems. The Solanum genus is characterized by the presence of steroidal glycosides (SGs) that confer herbivore resistance and serve as drug precursors in the pharmaceutical industry. Solanum dulcamara is a self-compatible, sexually reproducing species that produces seeds after buzz-pollination. In addition, primordia on the stem facilitate clonal propagation via adventitious root (AR) formation. ARs contain aerenchyma being developmentally and morphologically different from primary roots (PRs). Therefore, we hypothesized that ARs and PRs have different SG profiles. Aiming to assess differences in SGs profiles in S. dulcamara roots in relation to their origins and morphologies, we used liquid chromatography coupled to electron spray ionization quadruple time of flight mass spectrometry (LC-ESI-qToF-MS) to profile SGs from PRs and ARs of seven S. dulcamara individuals. Mass fragmentation pattern analysis indicated the presence of 31 SG-type structures, including those with spirostans and furostans moieties. We assigned the 31 structures to 9 classes of steroidal aglycons (SAgls) that differ in hydroxylation and degree of unsaturation. We found that SAgls were conjugated with di-, tri- and tetra saccharides whereby one compound contained a malonylated sugar. Principle component analysis showed that SG profiles of PRs and ARs separated on the first principal component, supporting our hypothesis. Specifically, PRs contain higher number of SGs than ARs with some compounds exclusively present in PRs. Our results reveal a high level of novel chemodiversity in PRs and ARs of Solanum dulcamara. The knowledge gained will deepen our understanding of SGs biosynthesis and their functional role in plant-environment interactions.

Project description:Background and aimsTemporal flooding is a common environmental stress for terrestrial plants. Aquatic adventitious roots (aquatic roots) are commonly formed in flooding-tolerant plant species and are generally assumed to be beneficial for plant growth by supporting water and nutrient uptake during partial flooding. However, the actual contribution of these roots to plant performance under flooding has hardly been quantified. As the investment into aquatic root development in terms of carbohydrates may be costly, these costs may - depending on the specific environmental conditions - offset the beneficial effects of aquatic roots. This study tested the hypothesis that the balance between potential costs and benefits depends on the duration of flooding, as the benefits are expected to outweigh the costs in long-term but not in short-term flooding.MethodsThe contribution of aquatic roots to plant performance was tested in Solanum dulcamara during 1-4?weeks of partial submergence and by experimentally manipulating root production. Nutrient uptake by aquatic roots, transpiration and photosynthesis were measured in plants differing in aquatic root development to assess the specific function of these roots.Key resultsAs predicted, flooded plants benefited from the presence of aquatic roots. The results showed that this was probably due to the contribution of roots to resource uptake. However, these beneficial effects were only present in long-term but not in short-term flooding. This relationship could be explained by the correlation between nutrient uptake and the flooding duration-dependent size of the aquatic root system.ConclusionsThe results indicate that aquatic root formation is likely to be selected for in habitats characterized by long-term flooding. This study also revealed only limited costs associated with adventitious root formation, which may explain the maintenance of the ability to produce aquatic roots in habitats characterized by very rare or short flooding events.

Project description:BACKGROUND: Solanum dulcamara (bittersweet, climbing nightshade) is one of the few species of the Solanaceae family native to Europe. As a common weed it is adapted to a wide range of ecological niches and it has long been recognized as one of the alternative hosts for pathogens and pests responsible for many important diseases in potato, such as Phytophthora. At the same time, it may represent an alternative source of resistance genes against these diseases. Despite its unique ecology and potential as a genetic resource, genomic research tools are lacking for S. dulcamara. We have taken advantage of next-generation sequencing to speed up research on and use of this non-model species. RESULTS: In this work, we present the first large-scale characterization of the S. dulcamara transcriptome. Through comparison of RNAseq reads from two different accessions, we were able to predict transcript-based SNP and SSR markers. Using the SNP markers in combination with genomic AFLP and CAPS markers, the first genome-wide genetic linkage map of bittersweet was generated. Based on gene orthology, the markers were anchored to the genome of related Solanum species (tomato, potato and eggplant), revealing both conserved and novel chromosomal rearrangements. This allowed a better estimation of the evolutionary moment of rearrangements in a number of cases and showed that chromosomal breakpoints are regularly re-used. CONCLUSION: Knowledge and tools developed as part of this study pave the way for future genomic research and exploitation of this wild Solanum species. The transcriptome assembly represents a resource for functional analysis of genes underlying interesting biological and agronomical traits and, in the absence of the full genome, provides a reference for RNAseq gene expression profiling aimed at understanding the unique biology of S. dulcamara. Cross-species orthology-based marker selection is shown to be a powerful tool to quickly generate a comparative genetic map, which may speed up gene mapping and contribute to the understanding of genome evolution within the Solanaceae family.

Dataset Information

Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara.

Publications

Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara.

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