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Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention

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Published/Copyright: December 31, 2021
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Open Life Sciences
From the journal Open Life Sciences Volume 16 Issue 1

Abstract

We used brightfield and epifluorescence microscopy, as well as permeability tests, to investigate the apoplastic histochemical features of plant roots associated with ion hyperaccumulation, invasion, and tolerance of oligotrophic conditions. In hyperaccumulator species with a hypodermis (exodermis absent), ions penetrated the root apex, including the root cap. By contrast, in non-hyperaccumulator species possessing an exodermis, ions did not penetrate the root cap. In vivo, the lignified hypodermis blocked the entry of ions into the cortex, while root exodermis absorbed ions and restricted them to the cortex. The roots of the hyperaccumulators Pteris vittata and Cardamine hupingshanensis, as well as the aquatic invasives Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes, contained lignin and pectins. These compounds may trap and store ions before hypodermis maturation, facilitating ion hyperaccumulation and retention in the apoplastic spaces of the roots. These apoplastic histochemical features were consistent with certain species-specific characters, including ion hyperaccumulation, invasive behaviors in aquatic environments, or tolerance of oligotrophic conditions. We suggest that apoplastic histochemical features of the root may act as invasion mechanisms, allowing these invasive aquatic plants to outcompete indigenous plants for ions.

Keywords: ions hyperaccumulator; histochemistry; oligotrophic environment; phytoremediation

1 Introduction

Several species in the genus Pteris (Pteridaceae), including Pteris vittata, hyperaccumulate ions such as arsenic (As) and chromium (Cr) [1,2,3,4]. The uptake, transport, translocation, and detoxification of heavy metals in the roots and fronds of these species have been well studied [2,3,4]. Pteris species have also evolved various anatomical features and hyperaccumulator functions to adapt to terrestrial, xeric, epiphytic, and rupicolous environments [3,4,5,6,7]. Cardamine hupingshanensis (Brassicaceae), which is found in Selenium (Se)-rich environments, is another well-known hyperaccumulator of ions, including Se and cadmium (Cd) [8,9,10]. Some invasive aquatic plants, including Alternanthera philoxeroides (Amaranthaceae), Eichhornia crassipes (Pontederiaceae), and Pistia stratiotes (Araceae), also hyperaccumulate ions: these species purify eutrophic water bodies and tend to outcompete indigenous plants in similar hostile environments [11,12,13,14,15,16,17,18,19,20]. Similarly, plants in the Proteaceae have evolved cluster roots with lignified or phenol-rich cortical walls to adapt to environments deficient in phosphorus and other nutrients [21,22,23]. Plants with cluster roots potentially facilitate alterations in plant community structure [24] and outcompete species without cluster roots [25]. Thus, cluster roots are highly desirable in crop breeding [26]. Paspalum distichum (Poaceae), a typical amphibious plant, is a non-hyperaccumulator with an endodermis and an exodermis in its roots [27].

In vascular plants, the lignified, suberized endodermis and exodermis act as apoplastic barriers, restricting water-solute exchange, reducing oxygen loss after submersion, and supporting adaptation to terrestrial environments [10,27,28,29,30,31,32,33,34,35,36,37]. The exodermis has Casparian bands in the primary walls and has suberin lamellae and/or lignin in the secondary walls [27,28,29,30,32,33,34,35,38]. Permeability tests showed that the lignified cortex and the hypodermis block ion exchange in Alternanthera philoxeroides and brassicas [18,39,40,41,42,43,44]. The cortical walls of the cluster roots in the Proteaceae contain soluble phenolic or lignin-like compounds that retain fluorescent agents (e.g., fluorol yellow 088); the presence of these compounds reflects an adaptation to nutrient deprivation [21,45,46,47,48,49,50,51,52]. In addition, the velamen, rhizodermis, and hairs of epiphytic orchids have pectins, which also facilitate ion uptake [53,54,55]. The surfaces of the mucilage hairs of Brasenia schreberi (Cabombaceae) have polysaccharides in various patterns that absorb berberine during different development stages in vivo [31,56].

In this study, we aimed to identify the apoplastic histochemical features of the root cortical walls that facilitate ion uptake and retention, leading to ion hyperaccumulation and reflecting an adaptation to nutrient-deprived environments. To identify these features, we investigated the roots of seven representative hyperaccumulator, invasive, and/or oligotrophic plants: the aerial species, Pteris vittata and Chlorophytum comosum; the wetland species, Cardamine hupingshanensis and Paspalum distichum; and the aquatic species, Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes. We also tested the apoplastic permeability of Pteris vittata and Paspalum distichum. An improved understanding of these plant roots’ apoplastic histochemical features might help explain how these plants become invasive, tolerate oligotrophic conditions, and hyperaccumulate ions [4,5,8,10,11,12,19,20,22,23,25,26]. These data will support the development of plants that can be used for the phytoremediation of ion-contaminated soils and oligotrophic water. Our results will also provide suggestions for the breeding of crops that can outcompete weed species [3,8,11,12,14,19,23,25,26].

2 Materials and methods

2.1 Plant sourcing and collection

Mature specimens of Pteris vittata, Paspalum distichum, Chlorophytum comosum, Cardamine hupingshanensis, Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes were identified in the Testing Ground of Yangtze University (Jingzhou City, Hubei Province, China) in October 2020. We collected samples of the adventitious aerial roots of Pteris vittata, which grow on walls in the cracks between bricks, and of Chlorophytum comosum, which propagate via shoots with adventitious aerial roots. We collected the roots of Cardamine hupingshanensis and Paspalum distichum from a wetland area. We collected the roots of Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes from ponds. Ten roots were collected from each species of five plants and immediately fixed in formaldehyde-alcohol-acetic acid [57]. Eight fresh, intact specimens of Pteris vittata and Paspalum distichum were used for the apoplastic permeability tests [18,30,33,34,35].

2.2 Microstructure and histochemistry

Root tissues were sectioned freehand, using a two-sided razor blade, under a stereoscope (JNOEC JSZ6, China). Root sections were cut at 10 and 20 mm from the root tip, as well as at the point where the cortex began to slough off. Sections were divided into three sets, such that each set included sections of each plant and at same distance from the root tip. Each set of sections was then stained with one of three stains: 0.1% (w/v) berberine hemisulfate-aniline blue (BAB) to test for Casparian bands and lignin in the cell walls [38,58], phloroglucinol-HCl to test for lignin in the cell walls [59], and 0.02% (w/v) ruthenium red to test for pectin in the cell walls [55,60].

All sections were washed 2–3 times with sterile water, mounted with sterile water, and examined using brightfield microscopy under a Leica DME microscope (Germany). Specimens were photographed with a digital camera and a micrometer (Nikon E5400, Japan). Specimens stained with BAB were viewed under ultraviolet light on an Olympus IX71 epifluorescence microscope with excitation filter G 365 nm, absorption filter barriers U-WB (blue light), dichromatic mirror DM 500, compensation excitation filter BP 450–480, and compensation absorption filter BA 515. BAB-stained specimens were photographed using a digital camera and a micrometer (RZ200C-21, Ruizhi Cop., China) [27].

2.3 Apoplastic permeability

We tested the apoplastic permeability of whole fresh specimens of Pteris vittata and Paspalum distichum. We tested ion uptake using the apoplastic permeability tests of Seago et al., Meyer et al., and Meyer and Peterson [38,61,62], with modifications. In brief, we immersed the roots of the whole plants in the berberine solution without separating the roots from the plants; the plants remained intact. This modification allowed us to use the permeability tests to assess how the plants absorbed ions. Three intact plant roots were left unstained as the negative control. Three additional intact plants roots (tracer control) were immersed in 100 mL of 0.05% berberine hemisulfate for 1 h and washed with sterile water. The final three intact plant roots were immersed in 100 mL of 0.05% berberine hemisulfate for 1 h, washed with sterile water, immersed in 0.05 M potassium thiocyanate for 0.5 h, and washed again with sterile water. Roots were sectioned freehand and viewed under UV light as described by Seago et al. [38].

3 Results and discussion

At 10 mm from the tips of the adventitious aerial roots of Pteris vittata, the root wall contained pectins from the endodermis to the rhizodermis and hairs (Figure 1a); the inner cortex had lignin-rich sclerenchyma layers and retained berberine around the endodermis (Figure 1b); and the surfaces of the rhizodermis and hairs accumulated substantial amounts of berberine or berberine thiocyanate crystals (Figure 1b–d). Berberine penetrated to the cortex of the Pteris vittata roots close to the root tips (Figure 1c and d), as indicated by the intense yellow fluorescence from the rhizodermis to the cortex. Similarly, intense yellow fluorescence was observed close to the tips of the roots of Paspalum distichum (Figure 1e), but berberine did not penetrate the root cap of this species. The walls of the adventitious aerial roots of Chlorophytum comosum also contained pectins from the endodermis to the rhizodermis and hairs (Figure 1f). Similar to Pteris vittata, the surfaces of the rhizodermis and hairs accumulated large amounts of berberine before metaxylem development (Figure 1g). After metaxylem development, the hairs were nearly sloughed off, but the exodermis and the rhizodermis surface continued to retain berberine (Figure 1h).

Figure 1 Photomicrographs of the adventitious roots of (a–d) Pteris vittata, (e) Paspalum distichum, and (f–h) Chlorophytum comosum. Scale bars = 50 μm. (a) Sectioned at 10 mm from root tip. Endodermis (arrowhead), cortex, rhizodermis, and hairs. Stain: ruthenium red. (b) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), lignified cortex (*), cortex, rhizodermis, and hairs. Stain: BAB. (c) Sectioned at 10 mm from root tip. Protoxylem, lignified thickened cortex (*), hypodermis, rhizodermis, and hairs, showing heavy accumulation of berberine thiocyanate. Stain: berberine (apoplastic tracer) and potassium thiocyanate. (d) Root tip showing root cap and entrance of berberine thiocyanate (arrowhead) close to the root tip; rhizodermis and hairs showing berberine thiocyanate accumulation (*). Stain: berberine (apoplastic tracer) and potassium thiocyanate. (e) Root tip showing root cap and entrance of berberine thiocyanate (arrowhead) close to the root tip; rhizodermis with limited berberine thiocyanate accumulation (*). Stain: berberine (apoplastic tracer) and potassium thiocyanate. (f) Sectioned at 10 mm from root tip. Pith, endodermis (arrowhead), cortex, hypodermis, rhizodermis, and hairs. Stain: ruthenium red. (g) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, exodermis (arrow), rhizodermis, and hairs. Stain: BAB. (h) Sectioned at 20 mm from root tip. Protoxylem, metaxylem, endodermis (arrowhead), cortex, exodermis (arrow), rhizodermis, and hairs. Stain: BAB. Abbreviations: ae, aerenchyma; co, cortex; h, hairs; hy, hypodermis; ic, intercellular space; mx, metaxylem; pa, parenchyma; pi, pith; px, protoxylem; rc, root cap; rh, rhizodermis; sc, sclerenchyma layer; sx, secondary xylem.
Figure 1

Photomicrographs of the adventitious roots of (a–d) Pteris vittata, (e) Paspalum distichum, and (f–h) Chlorophytum comosum. Scale bars = 50 μm. (a) Sectioned at 10 mm from root tip. Endodermis (arrowhead), cortex, rhizodermis, and hairs. Stain: ruthenium red. (b) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), lignified cortex (*), cortex, rhizodermis, and hairs. Stain: BAB. (c) Sectioned at 10 mm from root tip. Protoxylem, lignified thickened cortex (*), hypodermis, rhizodermis, and hairs, showing heavy accumulation of berberine thiocyanate. Stain: berberine (apoplastic tracer) and potassium thiocyanate. (d) Root tip showing root cap and entrance of berberine thiocyanate (arrowhead) close to the root tip; rhizodermis and hairs showing berberine thiocyanate accumulation (*). Stain: berberine (apoplastic tracer) and potassium thiocyanate. (e) Root tip showing root cap and entrance of berberine thiocyanate (arrowhead) close to the root tip; rhizodermis with limited berberine thiocyanate accumulation (*). Stain: berberine (apoplastic tracer) and potassium thiocyanate. (f) Sectioned at 10 mm from root tip. Pith, endodermis (arrowhead), cortex, hypodermis, rhizodermis, and hairs. Stain: ruthenium red. (g) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, exodermis (arrow), rhizodermis, and hairs. Stain: BAB. (h) Sectioned at 20 mm from root tip. Protoxylem, metaxylem, endodermis (arrowhead), cortex, exodermis (arrow), rhizodermis, and hairs. Stain: BAB. Abbreviations: ae, aerenchyma; co, cortex; h, hairs; hy, hypodermis; ic, intercellular space; mx, metaxylem; pa, parenchyma; pi, pith; px, protoxylem; rc, root cap; rh, rhizodermis; sc, sclerenchyma layer; sx, secondary xylem.

Before the cortex sloughed off, the adventitious roots of Cardamine hupingshanensis had pectins and lignin with even and Φ thickenings from the endodermis to the rhizodermis walls (Figure 2a–c). Similarly, pectins and lignified even thickenings were found from the endodermis to the rhizodermis walls in the adventitious roots of the aquatic plants Alternanthera philoxeroides (Figure 2d–f), Eichhornia crassipes (Figure 3a–c), and Pistia stratiotes (Figure 3d–f). In the adventitious roots of Alternanthera philoxeroides (Figure 2d–f) and Pistia stratiotes (Figure 3d–f), the cortex had typical radial schizogenous aerenchyma, while in the adventitious roots of Cardamine hupingshanensis (Figure 2a–c) and Eichhornia crassipes (Figure 3a–c), the cortex had radial lysigenous aerenchyma. The hypodermis of Eichhornia crassipes had lignified sclerenchyma layers (Figure 3a and c).

Figure 2 Photomicrographs of the adventitious roots of (a–c) Cardamine hupingshanensis and (d–f) Alternanthera philoxeroides. Scale bars = 50 μm. (a) Sectioned at 10 mm from root tip. Protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, and rhizodermis. Stain: ruthenium red. (b) Sectioned at 10 mm from root tip. Protoxylem, metaxylem, endodermis (arrowhead), cortex, lignified cortex (*), cortical lignified Φ thickenings (arrows), intercellular space, hypodermis, and rhizodermis. Stain: BAB. Image from [10] used with the permission of Open Life Sciences. (c) Sectioned at 50 mm from root tip. Secondary xylem, parenchyma, endodermis (white arrowhead), cortex, inner cortical lignified Φ thickening (black arrowhead), outer cortical lignified Φ thickenings (black arrows), lignified cortex (*), intercellular space, and hypodermis. Stain: phloroglucinol-HCl. Image from [10] used with the permission of Open Life Sciences. (d) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, and rhizodermis. Stain: ruthenium red. (e) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: BAB. Image from [18] used with the permission of Flora. (f) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), and hypodermis. Stain: phloroglucinol-HCl.
Figure 2

Photomicrographs of the adventitious roots of (a–c) Cardamine hupingshanensis and (d–f) Alternanthera philoxeroides. Scale bars = 50 μm. (a) Sectioned at 10 mm from root tip. Protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, and rhizodermis. Stain: ruthenium red. (b) Sectioned at 10 mm from root tip. Protoxylem, metaxylem, endodermis (arrowhead), cortex, lignified cortex (*), cortical lignified Φ thickenings (arrows), intercellular space, hypodermis, and rhizodermis. Stain: BAB. Image from [10] used with the permission of Open Life Sciences. (c) Sectioned at 50 mm from root tip. Secondary xylem, parenchyma, endodermis (white arrowhead), cortex, inner cortical lignified Φ thickening (black arrowhead), outer cortical lignified Φ thickenings (black arrows), lignified cortex (*), intercellular space, and hypodermis. Stain: phloroglucinol-HCl. Image from [10] used with the permission of Open Life Sciences. (d) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, and rhizodermis. Stain: ruthenium red. (e) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: BAB. Image from [18] used with the permission of Flora. (f) Sectioned at 10 mm from root tip. Protoxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), and hypodermis. Stain: phloroglucinol-HCl.

Figure 3 Photomicrographs of the adventitious roots of (a–c) Eichhornia crassipes and (d–f) Pistia stratiotes. Scale bars = 50 μm. (a) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, sclerenchyma layer, and rhizodermis. Stain: ruthenium red. (b) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: BAB. (c) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (white arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, sclerenchyma layer, and rhizodermis. Stain: phloroglucinol-HCl. (d) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, and rhizodermis. Stain: ruthenium red. (e) Sectioned at 10 mm from root tip. Metaxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: BAB. (f) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: phloroglucinol-HCl.
Figure 3

Photomicrographs of the adventitious roots of (a–c) Eichhornia crassipes and (d–f) Pistia stratiotes. Scale bars = 50 μm. (a) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, sclerenchyma layer, and rhizodermis. Stain: ruthenium red. (b) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: BAB. (c) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (white arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, sclerenchyma layer, and rhizodermis. Stain: phloroglucinol-HCl. (d) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, hypodermis, and rhizodermis. Stain: ruthenium red. (e) Sectioned at 10 mm from root tip. Metaxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: BAB. (f) Sectioned at 10 mm from root tip. Pith, protoxylem, metaxylem, endodermis (arrowhead), cortex, aerenchyma, lignified cortex (*), hypodermis, and rhizodermis. Stain: phloroglucinol-HCl.

The endodermis and the exodermis are key impermeable apoplastic barriers that are common in vascular plant roots [28,29,36,37,63,64,65,66,67,68]. Apoplastic barriers can be histochemically characterized by the presence of Casparian bands, suberin lamellae, and lignin; these barriers protect tissues from oxygen shortages and inhibit water-solute exchanges [18,23,30,34,35,69,70,71,72,73,74]. All the species examined in this study had roots with an endodermis, but only the roots of Paspalum distichum and Chlorophytum comosum had an exodermis [27,75]. The roots of the other species included in this study (Pteris vittata, Cardamine hupingshanensis, Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes) lacked an exodermis but possessed a hypodermis with lignin, as has been described in a variety of other plants, including Adiantum reniforme var. sinense, Brassica sp., Oenanthe javanica, Lycopodium obscurum, Pelargonium hortorum, Platycerium bifurcatum, and Selaginella sp. [10,37,39,40,41,42,43,44,66,76,77,78,79]. The cluster roots of various genera in the Proteaceae (e.g., Banksia, Grevillea, and Hakea) have a hypodermis containing soluble phenolic or lignin-like compounds, which have similar histochemical features with lignin of hypodermis in this studied species [21,49,50,51,52].

Lignified Φ and even thickenings that are distributed between the endodermis and the hypodermis of the cortical walls are typical of roots in the Brassicaceae, including in the genera Brassica, Noccaea, and Cardamine [10,39,40,41,42,43,44]. These thickenings act as barriers to ion transport. Unlike plants in the Brassicaceae, Pelargonium hortorum has larger Φ thickenings at the hypodermis [77]. The roots of Platycerium bifurcatum, Pleopeltis sp., and Doryopteris triphylla have lignified sclerenchyma layers around the endodermis [78,79,82,83,84], while the roots of Selaginella sp. have an exodermis [79]. In the heavy metal hyperaccumulator Noccaea caerulescens, the inner cortical walls of roots contain pectins and lignin [43]. Here lignified cortical thickenings were found in the roots of Pteris vittata [85], Cardamine hupingshanensis [10], Alternanthera philoxeroides [18], Eichhornia crassipes, and Pistia stratiotes.

In Pteris vittata and Chlorophytum comosum, the rhizodermis and hair walls contained pectins and accumulated a large amount of berberine. Similarly, the orchid root velamen also contains pectins and accumulates ions [53,54,55]. The root rhizodermis and hair walls of the hyperaccumulating ecotype of Sedum alfredii accumulated substantial Leadmium Green AM dye [80]; roots in this species also have thin inner cortical walls that contain large amounts of highly methylated pectin [81]. The root surfaces of Chlorophytum comosum retained berberine, similar to retention of polysaccharides by the smooth, immature mucilage hairs of Brasenia schreberi; the retention of berberine thiocyanate grains by the Pteris vittata root surfaces was similar to that of the mature mucilage hairs of Brasenia schreberi in vivo [31,56]. The rhizodermis surface retains little berberine in Adiantum reniforme var. sinense [37] and retains none in Metasequoia glyptostroboides [32], Cardamine hupingshanensis [10], and Alternanthera philoxeroides [18]. By contrast, our results showed that the surface of the root rhizodermis in Pteris vittata and Chlorophytum comosum retained substantial berberine. Pectins were present from the endodermis to the rhizodermis walls in Cardamine hupingshanensis, Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes. However, pectins are only found in the peri-endodermal thickenings of Noccaea caerulescens [39,43].

In the apoplastic permeability test, the berberine tracer penetrated to the cortex of both Pteris vittata (exodermis absent) and Paspalum distichum (exodermis present) near the root tips [27,75], similar to what has been shown in Iris germanica (exodermis present) [61,86]. The berberine tracer also penetrated the root caps of Pteris vittata, similar to the results in Vicia faba (exodermis absent) [86]. However, the berberine tracer was unable to penetrate the root cap of Paspalum distichum, similar to what has been shown in Zea mays (exodermis present) and Iris germanica (exodermis present) [61,86]. Many berberine thiocyanate grains adhered to the mature hypodermis of Pteris vittata. By contrast, few berberine thiocyanate grains adhered to the mature exodermis of Paspalum distichum at the root surface [27,75]. The lignified hypodermis of Alternanthera philoxeroides blocks the entrance of ions into the cortex [18]. The root exodermis has only been shown to absorb berberine in vivo in Phalaris arundinacea, Zizania latifolia, and Artemisia spp. [30,34,35].

Based on the apoplastic histochemical features of the roots and their permeability, we hypothesize that the root hairs of Pteris vittata and Chlorophytum comosum have pectins that capture ions from the atmosphere, which helps these plants to survive in an oligotrophic aerial environment. Like Pteris vittata and Chlorophytum comosum, the epiphytic Orchidaceae use pectins to capture ions from the atmosphere [53,54,55]. Similarly, Brasenia schreberi uses polysaccharides to capture ions [7,31,39,53,54,55,56]. The carpet-like root system of Pteris vittata has many adventitious roots that absorb captured ions, leading to the hyperaccumulation of ions such as As and Cr [1,2,3,4,7,31,39,53,54,55,56,80,81,86,87]. We suggest that the lignified thickenings and pectins in the roots of Cardamine hupingshanensis, Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes may trap ions before the hypodermis matures. These ions are then retained in the lignified walls, giving these species a competitive advantage over indigenous plants, particularly in oligotrophic environments [8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,39,40,41,42,43,44]. Finally, the dense, fine roots of Cardamine hupingshanensis may allow the plant to hyperaccumulate Se in a manner that is similar to the hyperaccumulation of Cd in the dense root hairs of certain Arabidopsis thaliana genotypes [10,88] and in the phenol-rich cluster roots of species in the Proteaceae [21,22,23,24,25,49,50,51,52]. This ability to hyperaccumulate ions supports the adaptation of these plants to phosphorus deprivation and/or nutrient-poor environments [22,23,26,50,52].

4 Conclusion

Histochemical analyses indicate that pectins and lignin are present in several parts of the plant root walls, including the cortex, endodermis, exodermis or hypodermis, rhizodermis, and hairs [8,9,10,11,12,13,14,15,16,17,18,19,20,31,39,40,41,42,43,44,52,53,54,55,56,80,81,86]. These compounds, including the polysaccharides and phenolics, may facilitate ion uptake and retention in plants [8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,34,35,39,40,41,42,43,44,52,53,54,55,56, 61,66,75,80,81,86]. In hyperaccumulator species without an exodermis (hypodermis), ions penetrate the root apex as well as the root cap [66,86]. By contrast, ions do not penetrate the root cap in non-hyperaccumulator species possessing an exodermis [27,61,66,75,86]. It has been shown in vivo that the lignified hypodermis of the root blocks the entry of ions into the cortex [18,86], while the root exodermis absorbs ions, trapping them within the exodermis walls [30,34,35,61,75,86]. The root hairs of Pteris vittata and Chlorophytum comosum are pectin-rich, reflecting an adaptation to the oligotrophic aerial environment [31,39,43,53,54,55,56,80,81]. The roots of the hyperaccumulators Pteris vittata and Cardamine hupingshanensis, as well as those of the invasive aquatic plants Alternanthera philoxeroides, Eichhornia crassipes, and Pistia stratiotes, have lignin and pectins in the cortex and rhizodermis; these structures may trap and store ions before hypodermis maturation. This hyperaccumulation of ions supports the survival of these plants in oligotrophic environments [8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,39,40,41,42,43,44,52]. We suggest that the apoplastic histochemical features of invasive aquatic plant roots may allow such plants to acquire ions more efficiently than indigenous plants, and these features can thus be considered invasive mechanisms [11,12,13,14,15,16,17,18,19,20]. The histochemical features associated with hyperaccumulation are highly desirable for crop improvement, as well as when designing plants for the phytoremediation of ion-contaminated soils and for the population of eutrophic environments [11,12,13,14,15,16,17,18,19,20,26,50,51,52,89,90,91,92,93,94].

  1. Funding information: This work was supported by the Hubei Province Key Laboratory of Conservation Biology for Shennongjia Golden Monkey Opening Fund (2019SNJ003), the Engineering Research Center of Ecology and Agriculture Use of Wetland, Ministry of Education Opening Fund, Yangtze University (KFT202004), and the Major Program on Technology Innovation of Hubei Province (2018ACA132).

  2. Conflict of interest: The authors state no conflict of interest.

  3. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2021-04-21
Revised: 2021-10-28
Accepted: 2021-11-07
Published Online: 2021-12-31

© 2021 Di Wu et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
  20. Discovery of novel potential KIT inhibitors for the treatment of gastrointestinal stromal tumor
  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
  26. Effects of Loofah cylindrica extract on learning and memory ability, brain tissue morphology, and immune function of aging mice
  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
  29. Gene therapy in PIDs, hemoglobin, ocular, neurodegenerative, and hemophilia B disorders
  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
  33. Mechanisms of circular RNA circ_0066147 on pancreatic cancer progression
  34. lncRNA myocardial infarction-associated transcript (MIAT) knockdown alleviates LPS-induced chondrocytes inflammatory injury via regulating miR-488-3p/sex determining region Y-related HMG-box 11 (SOX11) axis
  35. Identification of circRNA circ-CSPP1 as a potent driver of colorectal cancer by directly targeting the miR-431/LASP1 axis
  36. Hyperhomocysteinemia exacerbates ischemia-reperfusion injury-induced acute kidney injury by mediating oxidative stress, DNA damage, JNK pathway, and apoptosis
  37. Potential prognostic markers and significant lncRNA–mRNA co-expression pairs in laryngeal squamous cell carcinoma
  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
  39. ADHFE1 is a correlative factor of patient survival in cancer
  40. The association of transcription factor Prox1 with the proliferation, migration, and invasion of lung cancer
  41. Is there a relationship between the prevalence of autoimmune thyroid disease and diabetic kidney disease?
  42. Immunoregulatory function of Dictyophora echinovolvata spore polysaccharides in immunocompromised mice induced by cyclophosphamide
  43. T cell epitopes of SARS-CoV-2 spike protein and conserved surface protein of Plasmodium malariae share sequence homology
  44. Anti-obesity effect and mechanism of mesenchymal stem cells influence on obese mice
  45. Long noncoding RNA HULC contributes to paclitaxel resistance in ovarian cancer via miR-137/ITGB8 axis
  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
  52. Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis
  53. Primary localized cutaneous nodular amyloidosis presenting as lymphatic malformation: A case report
  54. Multimodal magnetic resonance imaging analysis in the characteristics of Wilson’s disease: A case report and literature review
  55. Therapeutic potential of anticoagulant therapy in association with cytokine storm inhibition in severe cases of COVID-19: A case report
  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
  57. Rufinamide (RUF) suppresses inflammation and maintains the integrity of the blood–brain barrier during kainic acid-induced brain damage
  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
https://doi.org/10.1515/biol-2021-0137
Keywords for this article
ions hyperaccumulator; histochemistry; oligotrophic environment; phytoremediation
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
  5. Iris metastasis of diffuse large B-cell lymphoma misdiagnosed as primary angle-closure glaucoma: A case report and review of the literature
  6. LncRNA PVT1 promotes cervical cancer progression by sponging miR-503 to upregulate ARL2 expression
  7. Two new inflammatory markers related to the CURB-65 score for disease severity in patients with community-acquired pneumonia: The hypersensitive C-reactive protein to albumin ratio and fibrinogen to albumin ratio
  8. Circ_0091579 enhances the malignancy of hepatocellular carcinoma via miR-1287/PDK2 axis
  9. Silencing XIST mitigated lipopolysaccharide (LPS)-induced inflammatory injury in human lung fibroblast WI-38 cells through modulating miR-30b-5p/CCL16 axis and TLR4/NF-κB signaling pathway
  10. Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats
  11. ABCB1 polymorphism in clopidogrel-treated Montenegrin patients
  12. Metabolic profiling of fatty acids in Tripterygium wilfordii multiglucoside- and triptolide-induced liver-injured rats
  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
  20. Discovery of novel potential KIT inhibitors for the treatment of gastrointestinal stromal tumor
  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
  26. Effects of Loofah cylindrica extract on learning and memory ability, brain tissue morphology, and immune function of aging mice
  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
  29. Gene therapy in PIDs, hemoglobin, ocular, neurodegenerative, and hemophilia B disorders
  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
  33. Mechanisms of circular RNA circ_0066147 on pancreatic cancer progression
  34. lncRNA myocardial infarction-associated transcript (MIAT) knockdown alleviates LPS-induced chondrocytes inflammatory injury via regulating miR-488-3p/sex determining region Y-related HMG-box 11 (SOX11) axis
  35. Identification of circRNA circ-CSPP1 as a potent driver of colorectal cancer by directly targeting the miR-431/LASP1 axis
  36. Hyperhomocysteinemia exacerbates ischemia-reperfusion injury-induced acute kidney injury by mediating oxidative stress, DNA damage, JNK pathway, and apoptosis
  37. Potential prognostic markers and significant lncRNA–mRNA co-expression pairs in laryngeal squamous cell carcinoma
  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
  39. ADHFE1 is a correlative factor of patient survival in cancer
  40. The association of transcription factor Prox1 with the proliferation, migration, and invasion of lung cancer
  41. Is there a relationship between the prevalence of autoimmune thyroid disease and diabetic kidney disease?
  42. Immunoregulatory function of Dictyophora echinovolvata spore polysaccharides in immunocompromised mice induced by cyclophosphamide
  43. T cell epitopes of SARS-CoV-2 spike protein and conserved surface protein of Plasmodium malariae share sequence homology
  44. Anti-obesity effect and mechanism of mesenchymal stem cells influence on obese mice
  45. Long noncoding RNA HULC contributes to paclitaxel resistance in ovarian cancer via miR-137/ITGB8 axis
  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
  52. Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis
  53. Primary localized cutaneous nodular amyloidosis presenting as lymphatic malformation: A case report
  54. Multimodal magnetic resonance imaging analysis in the characteristics of Wilson’s disease: A case report and literature review
  55. Therapeutic potential of anticoagulant therapy in association with cytokine storm inhibition in severe cases of COVID-19: A case report
  56. Neoadjuvant immunotherapy combined with chemotherapy for locally advanced squamous cell lung carcinoma: A case report and literature review
  57. Rufinamide (RUF) suppresses inflammation and maintains the integrity of the blood–brain barrier during kainic acid-induced brain damage
  58. Inhibition of ADAM10 ameliorates doxorubicin-induced cardiac remodeling by suppressing N-cadherin cleavage
  59. Invasive ductal carcinoma and small lymphocytic lymphoma/chronic lymphocytic leukemia manifesting as a collision breast tumor: A case report and literature review
  60. Clonal diversity of the B cell receptor repertoire in patients with coronary in-stent restenosis and type 2 diabetes
  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
  67. A two-microRNA signature predicts the progression of male thyroid cancer
  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
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