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Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants.

ABSTRACT: Background and Aims Flooding imposes stress upon terrestrial plants because it results in oxygen deficiency, which is considered a major problem for submerged plants. A common response of terrestrial plants to flooding is the formation of aquatic adventitious roots. Some studies have shown that adventitious roots on submerged plants are capable of absorbing water and nutrients. However, there is no experimental evidence for the possible oxygen uptake function of adventitious roots or for how important this function might be for the survival of plants during prolonged submergence. This study aims to investigate whether adventitious roots absorb oxygen from the water column, and whether this new function is beneficial to the survival of completely submerged plants. Methods Taking Alternanthera philoxeroides (Mart.) Griseb. as a representative species, the profiling of the underwater oxygen gradient towards living and dead adventitious roots on completely submerged plants was conducted, the oxygen concentration in stem nodes with and without adventitious roots was measured, and the growth, survival and non-structural carbohydrate content of completely submerged plants with and without adventitious roots was investigated. Key Results Oxygen profiles in the water column of adventitious roots showed that adventitious roots absorbed oxygen from water. It is found that the oxygen concentration in stem nodes having adventitious roots was higher than that in stem nodes without adventitious roots, which implies that the oxygen absorbed by adventitious roots from water was subsequently transported from the roots to other plant tissues. Compared with plants whose adventitious roots had been pruned, those with intact adventitious roots had slower leaf shedding, slower plant mass reduction, more efficient carbohydrate economy and prolonged survival when completely submerged. Conclusions The adventitious roots of A. philoxeroides formed upon submergence can absorb oxygen from ambient water, thereby alleviating the adverse effects of oxygen deficiency, enabling efficient utilization of carbohydrates and delaying the death of completely submerged plants.

SUBMITTER: Ayi Q

PROVIDER: S-EPMC5055620 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants.

Ayi Qiaoli Q Zeng Bo B Liu Jianhui J Li Siqi S van Bodegom Peter M PM Cornelissen Johannes H C JHC

Annals of botany. 20161001 4

Background and Aims Flooding imposes stress upon terrestrial plants because it results in oxygen deficiency, which is considered a major problem for submerged plants. A common response of terrestrial plants to flooding is the formation of aquatic adventitious roots. Some studies have shown that adventitious roots on submerged plants are capable of absorbing water and nutrients. However, there is no experimental evidence for the possible oxygen uptake function of adventitious roots or for how imp ...[more]

PMID: 27063366

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Project description:Internal aeration is crucial for root growth under waterlogged conditions. Some wetland plants have a structural barrier that impedes oxygen leakage from the basal part of roots called a radial oxygen loss (ROL) barrier. The ROL barrier reduces loss of oxygen transported via the aerenchyma to the root tips, enabling root growth into anoxic soil. The roots of some plants develop an ROL barrier under waterlogged conditions, while they remain leaky to oxygen under well-drained or aerated conditions. The main components of the inducible ROL barrier are thought to be suberin and lignin deposited at the outer cellular space (apoplast) in the outer part of roots. On the other hand, a few wetland plants including a species of Echinochloa form a constitutive ROL barrier, i.e., it is formed even in the absence of waterlogging. However, little is known about the components of constitutive ROL barriers. An ROL barrier is considered to be a characteristic of wetland species because it has not been found in any non-wetland species so far. Here, we examined whether Echinochloa species from non-waterlogged fields also form an inducible or constitutive ROL barrier. We found that three species of Echinochloa from non-waterlogged fields constitutively developed an ROL barrier under aerated conditions. Over 85% of their root exodermis cells were covered with suberin lamellae and had well-developed Casparian strips. These substances inhibited the infiltration of an apoplastic tracer (periodic acid), suggesting that the ROL barrier can also prevent the entry of phytotoxic compounds from the soil. Unlike the other Echinochloa species, E. oryzicola, which mainly inhabits rice paddies, was found to lack a constitutive ROL barrier under aerated conditions. Although close to 90% of its sclerenchyma was well lignified, it leaked oxygen from the basal part of roots. A high percentage (55%) of the root exodermis cells were not fortified with suberin lamellae. These results suggest that suberin is an important component of constitutive ROL barriers.

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.

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Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants.

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Oxygen absorption by adventitious roots promotes the survival of completely submerged terrestrial plants.

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