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Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves

  • Yuejing Zhang , Yi Ru , Zhenzhen Shi , Hanqi Wang , Ji Zhang , Jianping Wu , Hailong Pang and Hanqing Feng EMAIL logo
Published/Copyright: October 14, 2023
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Open Life Sciences
From the journal Open Life Sciences Volume 18 Issue 1

Abstract

In the process of the production of recombinant proteins by using an Agrobacterium-mediated transient gene expression system, the effectiveness of the control of light conditions pre- and post-agroinfiltration on efficiency of transient expression is worth being evaluated. In this study, Nicotiana benthamiana plants were used as a bioreactor to investigate the effects of different light conditions pre- and post-agroinfiltration on the transient expression of green fluorescent protein (GFP). The results showed that the plants grown under light condition for 5 weeks had the highest level of transient expression among those grown for 4–8 weeks. In the pre-agroinfiltration, the level of transient expression of GFP was obviously decreased by the increase in light intensity or by the shortening of the photoperiod. Although the shortening of the photoperiod post-agroinfiltration also decreased the level of transient expression, moderate light intensity post-agroinfiltration was needed for higher level of transient expression efficiency. However, there was no strong correlation between the transient expression efficiency and plant growth. The results suggested that light condition was an important factor affecting the level of transient expression in plants. Hence, light conditions should be optimized to obtain higher productivity of recombinant protein from transient expression systems.

Graphical abstract

Keywords: Nicotiana benthamiana ; transient expression; light intensity; photoperiod; biomass parameters

1 Introduction

Transgenic plants are an effective system for the study of the function, expression, and regulation of target genes. And, in recent years, transgenic plants have become the main platform for the production of recombinant pharmaceutical proteins [1,2]. The platform for the production of plant-based recombinant protein is more reliable, scalable, low-cost, and safe than the traditional expression systems using cell cultures from mammals, yeast, and bacteria [3,4]. More importantly, since plants are important food sources for human and animals, it is expected that transgenic plants can be used to prepare oral recombinant proteins or vaccines, without need of protein purification, which represents a significant advantage for plants over traditional expression systems [5–7].

Despite the obvious advantages of plants as efficient expression platforms, achieving high recombinant protein yields remains a challenge [8]. There are two major methods to express the target genes in plants. The first one is to develop a stable transgenic line, in which the gene coding the desired protein is inserted into the plant genome and its expression is derived by certain promoter, such as the cauliflower mosaic virus 35S promoter. Through succeeding generations, the foreign gene inserted in the genomes becomes heritable. The second one is to express the desired protein in plants through transient expression [2,9,10]. For the gene transient expression, the target gene is inserted in the vector and is delivered into the plant cells via Agrobacterium tumefaciens through a process called agroinfiltration (i.e., the vector containing the expression cassette of the gene of interest is carried by A. tumefaciens, which is used to infiltrate plants and thus deliver the gene of interest into the plant cells). After entering plant cells, the most of the target gene remains episomal, instead of integrating into the genome, and can be transcriptionally competent [11–14]. Compared with time-consuming stable transgenic lines, the production of desired proteins by transient expression has obvious advantages, including less time with more protein expression, consistency in protein accumulation with lower cost, and easy manipulation without any biosafety concerns. Additionally, the production of pharmaceutical proteins, antibody, or vaccine in plant cells by transient expression system would allow to rapidly cope with new diseases and mutation pathogens in our day-to-day life [15–17].

In order to improve the efficiency of transient gene expression in plants, much attention is focused on the modification of the functional region of the vector. These modification include design of 5′ and 3′ untranslated fragment, use of strong promoters, and addition of enhancer [18–20]. However, there are very few studies on whether plant growth condition and external environmental factor(s) could be utilized to improve the efficiency or increase protein yields from transient gene expression in plants.

It is well known that light is one of the most important environmental factors affecting plant physiology by deriving photosynthesis or acting as signaling. It has been reported that light intensity, photoperiod, and growth period under light condition have deep influences on the morphogenesis, development, and growth of plants, thus determining the production and the quality of plants [21,22]. However, less attention has been paid to the importance of light conditions on the efficiency of transient gene expression in plants. In fact, the plants for the transient gene expression must be grown under certain light condition, and light intensity and photoperiod can be controlled, especially when greenhouse is considered as the factory to produce valuable recombinant/therapeutic proteins in demand [23,24]. Hence, if light can actually impact the efficiency or protein yields from transient gene expression in plants, it is expected that light conditions in the process of the transient gene expression should be largely optimized.

In addition, different stages during the transient gene expression in plants would be considered carefully for the optimization of light condition. As described above, before infiltration with A. tumefaciens, the plants have experienced normal growth for a certain period. After infiltration with A. tumefaciens, an additional growth period is needed for the plants to complete the expression of the target genes and the accumulation of the desired proteins [25,26]. For achieving higher efficiency of transient gene expression or higher production of the desired proteins, one can assume that pre-agroinfiltration and post-agroinfiltration could require different light conditions. However, such issue has not been extensively investigated.

In this work, by using green fluorescent protein (GFP) as a reporter, we showed that light conditions, including growth period under light condition, light intensity, and photoperiod impact the efficiency of transient expression in Nicotiana benthamiana leaves during pre-agroinfiltration and post-agroinfiltration. We believe that this study would be helpful in developing new understanding on the effect of light conditions on the efficiency of transient gene expression. At the same time, this research would also be helpful in understanding how to utilize light to improve the yields of pharmaceutical protein, vaccine, and antibody, which are produced by transient gene expression in plants grown in green house with highly-controlled light condition.

2 Materials and methods

2.1 Plant material

Peat pellets were placed into a propagation tray, and water was added into the propagation tray. After the peat pellets absorbed the water for 1 h, two N. benthamiana seeds were added into each peat pellet and the tray was covered with a transparent plastic dome and placed at 25°C with 50% humidity. The light intensity and light: dark regime are indicated in Section 2.4, and where not indicated were applied at 100 μmol m−2 s−1 and 16/8 h. Two weeks after planting, the dome was removed, the water in the tray was drained, and Jack’s fertilizer with a concentration of 1.48 g/L was added. The plants continued to grow in the same environmental conditions as described above, and Jack’s fertilizer was supplied every day. In the third week, the plants with peat pellets were transferred to a new tray to provide adequate space for further growth until they are ready to be infiltrated at the time point needed.

2.2 Preparation of bacterial cultures for plant transformation

A. tumefaciens LBA4404 strains harboring the binary vector with the GFP gene were streaked on Agrobacterium rhizogene medium (0.5% peptone, 0.1% yeast extract, 0.5% beef extract, 0.5% sucrose, 0.05% MgSO4, 1.5% agar, pH 7.4) containing kanamycin (50 μg/mL), rifampicin (25 μg/mL), and chloramphenicol (25 μg/mL). Similarly, the EHA105 strains harboring the same vector were streaked on Agrobacterium rhizogene medium containing kanamycin (50 μg/mL) and rifampicin (25 μg/mL). After 24 h growth, the monoclone were picked out from the Agrobacterium rhizogene medium and inoculated into 50 mL Agrobacterium rhizogene broth medium (0.5% peptone, 0.1% yeast extract, 0.5% beef extract, 0.5% sucrose, 0.002% MgSO4, pH 7.4) with antibiotics, at 28°C overnight in a shaker at 180 rpm. The bacteria were collected by centrifugation at 5,000 rpm for 10 min and then washed by infiltration buffer (10 mM MES-KOH, pH 5.5; 10 mM MgSO4, 100 μM acetosyringone). Then, the bacteria were collected again and re-suspended in the infiltration buffer. The bacterial concentrations were determined by measuring optical density (OD) at 600 nm and were diluted to the concentrations needed.

2.3 Syringe infiltration

N. benthamiana leaves with the same size were selected, and 2 mL of bacterial suspension was taken up with a 5 mL sterile syringe. Then a small nick was created with a needle in the epidermis on the back side of the leaf. The A. tumefaciens in infiltration buffer was injected into the nick with a syringe without a needle.

2.4 Material treatments

In the first set of the experiment, the 4-, 5-, 6-, 7-, or 8-week-old N. benthamiana plants that were grown under the conditions as described in Section 2.1 were used for the infection with LBA4404 or EHA105 strain. For LBA4404 strain infection, the A. tumefaciens concentration was set at OD at a wavelength of 600 nm (OD600) 0.8, and the infected plants were incubated for 2 days under the conditions as described in Section 2.1. For EHA105 strain infection, the A. tumefaciens concentration was set at OD600 0.6, and the infected plants were incubated for 4 days under the conditions as described in Section 2.1.

In the second set of the experiment, the 5-week-old N. benthamiana plants that were grown under different light intensities at 50, 100, 150, 200, and 250 μmol m−2 s−1, respectively, were used for the infection with LBA4404 or EHA105 strain. The A. tumefaciens concentration and the time of incubation was the same as those in the first set of the experiment.

In the third set of the experiment, the 5-week-old N. benthamiana plants, which were grown under different light: dark regime at 16/8, 12/12, and 8/16 h, respectively, were used for the infection with LBA4404 or EHA105 strain. The A. tumefaciens concentration and the time of incubation was the same as those in the first set of the experiment.

In the fourth set of the experiment, the 5-week-old N. benthamiana plants were used for the infection with LBA4404 or EHA105 strain. The A. tumefaciens concentration was the same as those in the first set of the experiment. After the LBA4404 strain infection, the infected plants were incubated for 2 days under different light intensities at 50, 100, 150, 200, and 250 μmol m−2 s−1, respectively. After the EHA105 strain infection, the infected plants were incubated for 4 days under different light intensities at 50, 100, 150, 200, and 250 μmol m−2 s−1, respectively.

In the fifth set of the experiment, the 5-week-old N. benthamiana plants were used for the infection with LBA4404 or EHA105 strain. The A. tumefaciens concentration was the same as those in the first set of the experiment. After the LBA4404 strain infection, the infected plants were incubated for 2 days under different light: dark regime at 16/8, 12/12, and 8/16 h, respectively. After the EHA105 strain infection, the infected plants were incubated for 4 days under different light: dark regime at 16/8, 12/12, and 8/16 h, respectively.

The concentration of bacterial solution and infiltration days of above experiments were the best conditions for GFP expression, which were obtained from the screening of the previous experiments.

2.5 GFP fluorescence detection and photography

The fluorescence from the GFP in the infected leaves was detected and photographed by fluorescence stereoscope (Leica M205 FA, Germany) with excitation wavelength of 450–490 nm and emission wavelength of 500–550 nm. Fluorescence images were quantitatively analyzed with Image J software.

2.6 Biomass parameters

The leaves of the plants were taken and photographed, and the area of the leaves was measured by Photoshop software. The fresh weight was immediately measured and recorded using an analytical balance. The fresh samples were dried at 70°C in an oven, until a constant weight was obtained, and the dry weight was measured immediately. All the above biomass parameters were measured immediately after GFP fluorescence detection.

2.7 Statistical analysis

The value obtained was the average value of at least three independent experiments, and the data were mean values of at least three plants. Data were analyzed via one-way analysis of variance with SPSS statistical software (Version 20.0, IBM Corporation). The data were analyzed with Duncan’s multiple comparison. A probability level of 0.05 is considered as statistical significance. Pearson correlation coefficients were calculated using SPSS software (version 20.0, IBM Corporation).

3 Results

3.1 Effects of growth period under light condition on transient expression and biomass parameters

The growth period under light condition (i.e., the age of plants) could be one of the important factors that affect the yield of recombinant protein. We first studied the effects of growth period under light condition on transient expression of GFP gene, which were produced by the infection of LBA4404 and EHA105 strains. Compared with the control groups (LBA4404 and EHA105 strains without GFP), infection with LBA4404 or EHA105 strain carrying GFP gene induced transient expression of GFP (Figure S1c and Figure 1). We compared the green fluorescence from GFP expression among the plants with different growth period under light condition. The result showed that, with the increase of growth period under light condition (from 4 to 8 weeks), the green fluorescence from GFP expression increased first and then decreased. As a whole, the fluorescence from GFP expression in the plants infected with LBA4404 strain was higher than those infected with EHA105 strain. The 5-week-old plants had the highest level of fluorescence among all the plants with different growth period (Figure 1a and b). Thus, in the work later, the 5-week-old plants were chosen as the representatives to study the effects of other light condition on transient expression.

Figure 1 Changes of fluorescence intensity and biomass parameters of leaves infected with LBA4404 and EHA105 strains at different ages. (a) Representative images indicating the green fluorescence intensity of plants infected with LBA4404 and EHA105 strains at 4-, 5-, 6-, 7-, or 8-week-old, Bar = 2 mm. (b) Green fluorescence intensity of plants infected with LBA4404 and EHA105 strains at 4-, 5-, 6-, 7-, or 8-week-old. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.
Figure 1

Changes of fluorescence intensity and biomass parameters of leaves infected with LBA4404 and EHA105 strains at different ages. (a) Representative images indicating the green fluorescence intensity of plants infected with LBA4404 and EHA105 strains at 4-, 5-, 6-, 7-, or 8-week-old, Bar = 2 mm. (b) Green fluorescence intensity of plants infected with LBA4404 and EHA105 strains at 4-, 5-, 6-, 7-, or 8-week-old. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.

As presented in Figure 1c–e, we also measured the biomass parameters of the plants with different growth periods under light condition, including fresh weight, dry weight, and leaf area. It was found that all of these three parameters increased with the increase of the growth period of the plants under light condition, although, there was no significant difference in fresh weight and dry weight between the 5- and 6-week-old plants. Combined the results presented in Figure 1, it is suggested that the growth period of the plants under light condition can affect the transient expression efficiency, but there was no strong negative correlation between the transient expression efficiency and biomass among the plants with different growth period under light condition (Figure S1a and b).

3.2 Effects of different light intensities before agroinfiltration on transient expression and biomass parameters

As shown in Figure 2a and b, we studied the effects of different light intensity before agroinfiltration on transient expression of GFP gene after infection by LBA4404 and EHA105 strains. When the light intensity is at 50 μmol m−2 s−1, the fluorescence from GFP expression in the plants infected with LBA4404 and EHA105 strains was the highest among the other light intensities. With the increase of light intensity from 50 to 250 μmol m−2 s−1, the green fluorescence from GFP expression decreased. Additionally, the measurement of the biomass parameters showed that with the increase of the light intensity (from 50 to 250 μmol m−2 s−1) before agroinfiltration, the fresh weight, dry weight, and leaf area of the plant increased first but then decreased. The fresh and dry weight peaked at 150 μmol m−2 s−1, while the leaf area peaked at 100 μmol m−2 s−1 (Figure 2c–e). These results showed that the light intensity before agroinfiltration can affect the GFP expression, and moderate light intensity can enhance plant growth while excessive light intensity would inhibit the growth of plants. Combined the results presented in Figure 2, it is suggested that there was no strong correlation between the transient expression efficiency and biomass parameters among the plants with different intensity before agroinfiltration (Figure S1a and b).

Figure 2 Changes of fluorescence intensity and biomass parameters of the plant leaves at different light intensities before agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 before LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 before LBA4404 and EHA105 strains agroinfiltration. These plants were placed back into the original light intensities after agroinfiltration to continue incubation. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.
Figure 2

Changes of fluorescence intensity and biomass parameters of the plant leaves at different light intensities before agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 before LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 before LBA4404 and EHA105 strains agroinfiltration. These plants were placed back into the original light intensities after agroinfiltration to continue incubation. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.

3.3 Effects of different light/dark regime before agroinfiltration on transient expression and biomass parameters

The fluorescence from GFP expression was highest when the light/dark regime before agroinfiltration was 16/8 h among the plants with three different light: dark regimes (16/8, 12/12, or 8/16 h). Decrease in photoperiod from 16/8 to 12/12 h reduced fluorescence from GFP expression. However, there was no significant difference in fluorescence from GFP expression between the light: dark regime at 12/12 h and at 8/16 h (Figure 3b).

Figure 3 Changes of fluorescence intensity and biomass parameters of the plant leaves at different photoperiods before agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the photoperiods at 16/8, 12/12, and 8/16 h before LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the photoperiods at 16/8, 12/12, and 8/16 h before LBA4404 and EHA105 strains agroinfiltration. These plants were placed back into the original photoperiods after agroinfiltration to continue incubation. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.
Figure 3

Changes of fluorescence intensity and biomass parameters of the plant leaves at different photoperiods before agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the photoperiods at 16/8, 12/12, and 8/16 h before LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the photoperiods at 16/8, 12/12, and 8/16 h before LBA4404 and EHA105 strains agroinfiltration. These plants were placed back into the original photoperiods after agroinfiltration to continue incubation. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.

With the shortening of photoperiod before agroinfiltration, leaf area decreased. The changes in the values of fresh weight and dry weight under different light/dark regime before agroinfiltration presented a similar pattern with the changes of leaf area (Figure 3c–e). This indicates that the light: dark regime at 16/8 h before agroinfiltration was more beneficial to the growth of plants. Combined the results presented in Figure 3, it is suggested that there was no strong positive correlation between the transient expression efficiency and biomass parameters among the plants grown with different light/dark regime before agroinfiltration (Figure S1a and b).

3.4 Effects of different light intensities after agroinfiltration on transient expression and biomass parameters

Figure 4 shows the effects of different light intensities after agroinfiltration on the green fluorescence from GFP expression. The results indicated that with the increase of light intensity (from 50 to 250 μmol m−2 s−1) after agroinfiltration, the fluorescence from GFP expression increased first and then decreased. The fluorescence from GFP expression peaked at 150 μmol m−2 s−1, which was obviously higher than that at other light intensities after agroinfiltration.

Figure 4 Changes of fluorescence intensity and biomass parameters of the plant leaves at different light intensities after agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 after LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 after LBA4404 and EHA105 strains agroinfiltration. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.
Figure 4

Changes of fluorescence intensity and biomass parameters of the plant leaves at different light intensities after agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 after LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the light intensities at 50, 100, 150, 200, 250 μmol m−2 s−1 after LBA4404 and EHA105 strains agroinfiltration. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.

There was no significant difference in the fresh weight of the infected plants at different light intensities after agroinfiltration. Similarly, leaf area and dry weight did not change significantly at different light intensities after agroinfiltration (Figure 4c–e). The results showed that the light intensity after agroinfiltration had no effect on the fresh weight, dry weight, and leaf area. There was no correlation between the transient expression efficiency and biomass parameters among the plants at different light intensities after agroinfiltration.

3.5 Effects of different light/dark regime after agroinfiltration on transient expression and biomass parameters

The fluorescence from GFP expression peaked when the light/dark regime after agroinfiltration was at 16/8 h, which was significantly higher than that at 12/12 or 8/16 h (Figure 5a and b).

Figure 5 Changes of fluorescence intensity and biomass parameters of the plant leaves at different photoperiods after agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the photoperiods at 16/8, 12/12, and 8/16 h after LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the photoperiods at 16/8, 12/12, and 8/16 h after LBA4404 and EHA105 strains agroinfiltration. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.
Figure 5

Changes of fluorescence intensity and biomass parameters of the plant leaves at different photoperiods after agroinfiltration. (a) Representative pictures indicating the green fluorescence intensity of plants that were treated under the photoperiods at 16/8, 12/12, and 8/16 h after LBA4404 and EHA105 strains agroinfiltration. Bar = 2 mm. (b) Fluorescence intensity of plants under the photoperiods at 16/8, 12/12, and 8/16 h after LBA4404 and EHA105 strains agroinfiltration. (c) Fresh weight, FW. (d) Leaf area, LA. (e) Dry weight, DW. Different lowercase letters indicate significant differences (P < 0.05) among the different treatments.

No significant changes in the fresh weight, dry weight, and leaf area were observed under the different photoperiods after agroinfiltration (Figure 5). This indicates that the accumulation of plant biomass was unaffected by the different photoperiods after agroinfiltration. There was no correlation between the transient expression efficiency and biomass parameters among the plants with different light/dark regime after agroinfiltration.

4 Discussion

The present work mainly studied the influence of light condition on plant transient expression. The growth period under light condition (i.e., the age of plants) could be the most easily controlled light factor during plant growth. As shown in the present work, the biomass of the plants used for the transient expression increased with the increase of the age of plants (from 4 to 8 weeks) (Figure 1). However, the increase in the growth period under light condition did not correspondingly enhance the transient expression efficiency. The 5-week-old plants had highest level of fluorescence among the 4-, 5-, 6-, 7-, or 8-week-old plants (Table 1). This indicated that the production of recombinant protein requires optimal plant growth period. The transient protein expression level decreased as the plant growth period generated more biomass, reflecting the greater protein synthesis potential of young plants. Consistent with our observations, the works from group of Dodds et al. and Saur et al. found that the success of transient gene expression decreased with the age of the N. benthamiana plants, and they suggested that this could be attributed to the cold shock protein of A. tumefaciens, which can trigger immune responses including a burst of reactive oxygen species, from old plants, but not from young plants [27,28]. On the other hand, in theory, the cell walls of younger plants are more relaxed for faster cell division, compared to those in the older plants [29,30]. Previous work reported that relaxation of cell wall may render the plant more vulnerable to biotic intruders by facilitating pathogen entry, allowing enhanced nutrient leakage, and increasing availability of resources for pathogens [31]. Thus, we assume that the younger plants are most susceptible to the infection and spread of A. tumefaciens than the older ones and, as the result, the transient expression of foreign gene by agroinfiltration increased in the younger plants.

Table 1

Best conditions for fluorescence intensity and biomass parameters of leaves infected by LBA4404 and EHA105 strains under different conditions

Agrobacterium strains Fluorescence intensity and biomass parameters Growth period (w) Before agroinfiltration After agroinfiltration
Light intensity (μmol m−2 s−1) Photoperiod (h) Light intensity (μmol m−2 s−1) Photoperiod (h)
LBA4404 Fluorescence intensity 5 50 16/8 150 16/8
Fresh weight 8 150 16/8 — 16/8
Leaf area 8 100 16/8 — 16/8
Dry weight 8 150 16/8 — 16/8
EHA105 Fluorescence intensity 5 50 16/8 150 16/8
Fresh weight 8 150 16/8 — 16/8
Leaf area 8 100 16/8 — 16/8
Dry weight 8 150 16/8 — 16/8

Note: “−” represents no difference in biomass parameters at different light intensities.

It is well known that light intensity and photoperiod can affect plant growth [32]. However, light conditions where the transient expression takes place in plants should also be controlled for recombinant protein accumulation, rather than only for plant growth. The light conditions for recombinant protein yield are likely different between pre- and post-agroinfiltration processes, since different biological events occur during pre- and post-inoculation [26,33]. Before agroinfiltration, light condition would make the plant more susceptible to Agrobacterium. In contrast, after agroinfiltration, light control would aim to enhance the transient expression of recombinant protein. Thus, in the present work, we investigated the effect of light intensity and photoperiod in the pre- and post-agroinfiltration on the transient expression and plant growth. For N. benthamiana plants, increase in the light intensity (from 50 to 250 μmol m−2 s−1) before agroinfiltration decreased the level of transient expression of GFP gene (Figure 2), although light intensity before agroinfiltration from 100 to 200 μmol m−2 s−1 can enhance the plant growth (Table 1). The mechanism for the decrease of the transient expression by the increase in the light intensity before agroinfiltration is unclear. One of the possible reasons is that the increase in the light intensity before agroinfiltration could increase the resistance of the plants to A. tumefaciens, since previous works have reported that plants acclimated to high light displayed increased resistance against virulent Pseudomonas syringae pv. tomato DC3000 [34,35]. We also found that the shortening of the photoperiod before agroinfiltration not only decreased the plant growth but also reduced the transient expression efficiency. Recent work showed that growth under long day compared with growth under short day enhances the expression of defense-related genes and resistance of plant to the necrotrophic pathogen [36]. Thus, it is possible that light intensity and photoperiod in the pre-agroinfiltration could affect the transient expression efficiency via affecting the resistance of plant to A. tumefaciens, although the actual mechanism is still unknown and could be different from the assumed.

Further study in the present works showed that the effects of light intensity and photoperiod in the post-agroinfiltration on the plant growth and transient expression efficiency are obviously different from those in the pre-agroinfiltration. Although the shortening of the photoperiod after agroinfiltration, similarly to the shortening of the photoperiod before agroinfiltration, also decreased the level of transient expression (Figures 3 and 5), the increase in the light intensity after agroinfiltration did not cause the gradual decrease in the level of transient expression efficiency. Instead, the light intensity after agroinfiltration from 100 to 200 μmol m−2 s−1 effectively enhanced the level of transient expression efficiency (Table 1). In addition, the changes of the light intensity and photoperiod in the post-agroinfiltration did not obviously affect the plant growth (Figures 4 and 5). It is difficult to explain why the effects of pre- and post-inoculation light condition on the level of transient expression and plant growth are so different. On the one hand, the A. tumefaciens-mediated transient expression is a process involving a series of complex biological events, including A. tumefaciens infection, T-DNA transfer from A. tumefaciens, protein biosynthesis, and its accumulation in leaf tissue. Such process could inevitably affect the plant growth under light condition, possibly via affecting photosynthesis, respiration, and other metabolism [37–39]. On the other hand, the effects of light condition on plants could be more complex. Besides the effects of light on plant resistance and growth, it has been reported that light intensity and photoperiod can influence post-translational protein modifications and degradation, and other physiological process that could be related to the biological events of Agrobacterium-mediated transient expression [24,40–44]. For example, Zambre et al. observed that light can affect the ability to T-DNA transfer possibly by changing some physiological and metabolic processes in plant cells [24]. In addition, the studies from Zhang and Zhou showed that light intensity can affect protein synthesis by regulating the synthesis and signal transduction of endogenous hormones in plants [45]. Thus, complexity would be further increased, when one would attempt to explain the reasons for the effects of pre- and post-inoculation light condition on the level of transient expression and plant growth and the reasons for the difference between both of them.

However, the aim of the present work is to present whether the light condition can affect the transient expression level in plant and how to utilize the information obtained to optimize the pre- and post-inoculation light condition for efficient recombinant protein production in Agrobacterium-mediated transient expression systems. This could be important for the production of plant-based recombinant proteins in the plant factories, in which illumination condition is highly controlled. Optimized illumination can largely decrease the gratuitous consumption of energy and increase the yield of recombinant proteins, compared to the unoptimized light condition. It is also noted that, besides light, air temperature and relative humidity can also affect the transient expression reactions, which involve T-DNA transfer, recombinant protein accumulation, plant defense responses, and protein degradation [46–48]. The different pharmaceutical proteins produced from different plant species could need different environmental condition. Thus, enhancement of the production of certain recombinant protein by environmental control is still a challenge. Nonetheless, compared to temperature and relative humidity, light condition is more easily to be controlled. Thus, light condition would be considered as the primary environmental factor to be applied in recombinant protein production by plant-based transient expression systems.

5 Conclusions

In conclusion, the present work suggests that light condition is an important factor in the process of transient expression. The effect of different light intensities and photoperiod on the expression of foreign genes is different. The 5-week-old plants had the highest level of transient expression among those grown for 4–8 weeks. In the pre-agroinfiltration, the increase in light intensity or shortening of the photoperiod can reduce the level of transient expression of GFP was obviously decreased. In the post-agroinfiltration, the shortening of the photoperiod post-agroinfiltration also decreased the level of transient expression, while moderate light intensity enhanced the level of transient expression efficiency. Totally, there was no strong correlation between the transient expression efficiency and plant growth under different light conditions. Hence, light conditions should be optimized to obtain higher productivity of recombinant protein from transient expression systems.

Acknowledgements

The authors gratefully acknowledge Klaas Bouwmeester (Laboratory of Phytopathology, Wageningen University in the Netherlands) for the gift of the vectors and Agrobacterium tumefaciens strains.

  1. Funding information: This study was supported by the Gansu Colleges Industry Support Plan Project (grant number 2023CYZC-20), the Key Research and Development Plan Project of Gansu Province (grant number 22YF7NA119), the Major Project of Science and Technology Plan of Gansu Province (grant number 22ZD1NA001), Guiding Scientific and Technological Innovation Development of Gansu Province (grant number 2019ZX-05), the Open Fund of New Rural Development Institute of Northwest Normal University, Postgraduate Research Funding Project of Northwest Normal University (grant number 2021KYZZ01037), Excellent Doctoral Dissertation Cultivation Funding Program of Northwest Normal University, and Excellent Doctoral Program of Science and Technology Program of Gansu Province (grant number 23JRRA697; 23JRRA707).

  2. Author contributions: Y.J.Z.: designed and performed the experiments, analyzed the data and results, and wrote the manuscript. Y.R., Z.Z.S., and H.Q.W.: assisted with the performance and analysis of the experiments. J.Z., J.P.W., and H.L.P.: analyzed the experiments and supervised the study. H.Q.F.: conceived the project, designed the experiments, and revised the manuscript. All authors read and approved the final manuscript.

  3. Conflict of interest: Authors state no conflict of interest.

  4. 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: 2023-05-09
Revised: 2023-07-02
Accepted: 2023-08-27
Published Online: 2023-10-14

© 2023 the author(s), published by De Gruyter

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

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  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
https://doi.org/10.1515/biol-2022-0732
Keywords for this article
Nicotiana benthamiana; transient expression; light intensity; photoperiod; biomass parameters
Creative Commons
BY 4.0

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  2. Systemic investigation of inetetamab in combination with small molecules to treat HER2-overexpressing breast and gastric cancers
  3. Immunosuppressive treatment for idiopathic membranous nephropathy: An updated network meta-analysis
  4. Identifying two pathogenic variants in a patient with pigmented paravenous retinochoroidal atrophy
  5. Effects of phytoestrogens combined with cold stress on sperm parameters and testicular proteomics in rats
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  7. Neutrophilia with subclinical Cushing’s disease: A case report and literature review
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  10. Novel CPLANE1 c.8948dupT (p.P2984Tfs*7) variant in a child patient with Joubert syndrome
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  13. High glucose and high lipid induced mitochondrial dysfunction in JEG-3 cells through oxidative stress
  14. Pharmacological inhibition of the ubiquitin-specific protease 8 effectively suppresses glioblastoma cell growth
  15. Levocarnitine regulates the growth of angiotensin II-induced myocardial fibrosis cells via TIMP-1
  16. Age-related changes in peripheral T-cell subpopulations in elderly individuals: An observational study
  17. Single-cell transcription analysis reveals the tumor origin and heterogeneity of human bilateral renal clear cell carcinoma
  18. Identification of iron metabolism-related genes as diagnostic signatures in sepsis by blood transcriptomic analysis
  19. Long noncoding RNA ACART knockdown decreases 3T3-L1 preadipocyte proliferation and differentiation
  20. Surgery, adjuvant immunotherapy plus chemotherapy and radiotherapy for primary malignant melanoma of the parotid gland (PGMM): A case report
  21. Dosimetry comparison with helical tomotherapy, volumetric modulated arc therapy, and intensity-modulated radiotherapy for grade II gliomas: A single‑institution case series
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  23. Refractory hypokalemia with sexual dysplasia and infertility caused by 17α-hydroxylase deficiency and triple X syndrome: A case report
  24. Meta-analysis of cancer risk among end stage renal disease undergoing maintenance dialysis
  25. 6-Phosphogluconate dehydrogenase inhibition arrests growth and induces apoptosis in gastric cancer via AMPK activation and oxidative stress
  26. Experimental study on the optimization of ANM33 release in foam cells
  27. Primary retroperitoneal angiosarcoma: A case report
  28. Metabolomic analysis-identified 2-hydroxybutyric acid might be a key metabolite of severe preeclampsia
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  30. Effect of spaceflight on the phenotype and proteome of Escherichia coli
  31. Comparison of immunotherapy combined with stereotactic radiotherapy and targeted therapy for patients with brain metastases: A systemic review and meta-analysis
  32. Activation of hypermethylated P2RY1 mitigates gastric cancer by promoting apoptosis and inhibiting proliferation
  33. Association between the VEGFR-2 -604T/C polymorphism (rs2071559) and type 2 diabetic retinopathy
  34. The role of IL-31 and IL-34 in the diagnosis and treatment of chronic periodontitis
  35. Triple-negative mouse breast cancer initiating cells show high expression of beta1 integrin and increased malignant features
  36. mNGS facilitates the accurate diagnosis and antibiotic treatment of suspicious critical CNS infection in real practice: A retrospective study
  37. The apatinib and pemetrexed combination has antitumor and antiangiogenic effects against NSCLC
  38. Radiotherapy for primary thyroid adenoid cystic carcinoma
  39. Design and functional preliminary investigation of recombinant antigen EgG1Y162–EgG1Y162 against Echinococcus granulosus
  40. Effects of losartan in patients with NAFLD: A meta-analysis of randomized controlled trial
  41. Bibliometric analysis of METTL3: Current perspectives, highlights, and trending topics
  42. Performance comparison of three scaling algorithms in NMR-based metabolomics analysis
  43. PI3K/AKT/mTOR pathway and its related molecules participate in PROK1 silence-induced anti-tumor effects on pancreatic cancer
  44. The altered expression of cytoskeletal and synaptic remodeling proteins during epilepsy
  45. Effects of pegylated recombinant human granulocyte colony-stimulating factor on lymphocytes and white blood cells of patients with malignant tumor
  46. Prostatitis as initial manifestation of Chlamydia psittaci pneumonia diagnosed by metagenome next-generation sequencing: A case report
  47. NUDT21 relieves sevoflurane-induced neurological damage in rats by down-regulating LIMK2
  48. Association of interleukin-10 rs1800896, rs1800872, and interleukin-6 rs1800795 polymorphisms with squamous cell carcinoma risk: A meta-analysis
  49. Exosomal HBV-DNA for diagnosis and treatment monitoring of chronic hepatitis B
  50. Shear stress leads to the dysfunction of endothelial cells through the Cav-1-mediated KLF2/eNOS/ERK signaling pathway under physiological conditions
  51. Interaction between the PI3K/AKT pathway and mitochondrial autophagy in macrophages and the leukocyte count in rats with LPS-induced pulmonary infection
  52. Meta-analysis of the rs231775 locus polymorphism in the CTLA-4 gene and the susceptibility to Graves’ disease in children
  53. Cloning, subcellular localization and expression of phosphate transporter gene HvPT6 of hulless barley
  54. Coptisine mitigates diabetic nephropathy via repressing the NRLP3 inflammasome
  55. Significant elevated CXCL14 and decreased IL-39 levels in patients with tuberculosis
  56. Whole-exome sequencing applications in prenatal diagnosis of fetal bowel dilatation
  57. Gemella morbillorum infective endocarditis: A case report and literature review
  58. An unusual ectopic thymoma clonal evolution analysis: A case report
  59. Severe cumulative skin toxicity during toripalimab combined with vemurafenib following toripalimab alone
  60. Detection of V. vulnificus septic shock with ARDS using mNGS
  61. Novel rare genetic variants of familial and sporadic pulmonary atresia identified by whole-exome sequencing
  62. The influence and mechanistic action of sperm DNA fragmentation index on the outcomes of assisted reproduction technology
  63. Novel compound heterozygous mutations in TELO2 in an infant with You-Hoover-Fong syndrome: A case report and literature review
  64. ctDNA as a prognostic biomarker in resectable CLM: Systematic review and meta-analysis
  65. Diagnosis of primary amoebic meningoencephalitis by metagenomic next-generation sequencing: A case report
  66. Phylogenetic analysis of promoter regions of human Dolichol kinase (DOLK) and orthologous genes using bioinformatics tools
  67. Collagen changes in rabbit conjunctiva after conjunctival crosslinking
  68. Effects of NM23 transfection of human gastric carcinoma cells in mice
  69. Oral nifedipine and phytosterol, intravenous nicardipine, and oral nifedipine only: Three-arm, retrospective, cohort study for management of severe preeclampsia
  70. Case report of hepatic retiform hemangioendothelioma: A rare tumor treated with ultrasound-guided microwave ablation
  71. Curcumin induces apoptosis in human hepatocellular carcinoma cells by decreasing the expression of STAT3/VEGF/HIF-1α signaling
  72. Rare presentation of double-clonal Waldenström macroglobulinemia with pulmonary embolism: A case report
  73. Giant duplication of the transverse colon in an adult: A case report and literature review
  74. Ectopic thyroid tissue in the breast: A case report
  75. SDR16C5 promotes proliferation and migration and inhibits apoptosis in pancreatic cancer
  76. Vaginal metastasis from breast cancer: A case report
  77. Screening of the best time window for MSC transplantation to treat acute myocardial infarction with SDF-1α antibody-loaded targeted ultrasonic microbubbles: An in vivo study in miniswine
  78. Inhibition of TAZ impairs the migration ability of melanoma cells
  79. Molecular complexity analysis of the diagnosis of Gitelman syndrome in China
  80. Effects of maternal calcium and protein intake on the development and bone metabolism of offspring mice
  81. Identification of winter wheat pests and diseases based on improved convolutional neural network
  82. Ultra-multiplex PCR technique to guide treatment of Aspergillus-infected aortic valve prostheses
  83. Virtual high-throughput screening: Potential inhibitors targeting aminopeptidase N (CD13) and PIKfyve for SARS-CoV-2
  84. Immune checkpoint inhibitors in cancer patients with COVID-19
  85. Utility of methylene blue mixed with autologous blood in preoperative localization of pulmonary nodules and masses
  86. Integrated analysis of the microbiome and transcriptome in stomach adenocarcinoma
  87. Berberine suppressed sarcopenia insulin resistance through SIRT1-mediated mitophagy
  88. DUSP2 inhibits the progression of lupus nephritis in mice by regulating the STAT3 pathway
  89. Lung abscess by Fusobacterium nucleatum and Streptococcus spp. co-infection by mNGS: A case series
  90. Genetic alterations of KRAS and TP53 in intrahepatic cholangiocarcinoma associated with poor prognosis
  91. Granulomatous polyangiitis involving the fourth ventricle: Report of a rare case and a literature review
  92. Studying infant mortality: A demographic analysis based on data mining models
  93. Metaplastic breast carcinoma with osseous differentiation: A report of a rare case and literature review
  94. Protein Z modulates the metastasis of lung adenocarcinoma cells
  95. Inhibition of pyroptosis and apoptosis by capsaicin protects against LPS-induced acute kidney injury through TRPV1/UCP2 axis in vitro
  96. TAK-242, a toll-like receptor 4 antagonist, against brain injury by alleviates autophagy and inflammation in rats
  97. Primary mediastinum Ewing’s sarcoma with pleural effusion: A case report and literature review
  98. Association of ADRB2 gene polymorphisms and intestinal microbiota in Chinese Han adolescents
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  100. Study on the cytokines related to SARS-Cov-2 in testicular cells and the interaction network between cells based on scRNA-seq data
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  106. Identification of lysosome-related genes in connection with prognosis and immune cell infiltration for drug candidates in head and neck cancer
  107. Development of an instrument-free and low-cost ELISA dot-blot test to detect antibodies against SARS-CoV-2
  108. Research progress on gas signal molecular therapy for Parkinson’s disease
  109. Adiponectin inhibits TGF-β1-induced skin fibroblast proliferation and phenotype transformation via the p38 MAPK signaling pathway
  110. The G protein-coupled receptor-related gene signatures for predicting prognosis and immunotherapy response in bladder urothelial carcinoma
  111. α-Fetoprotein contributes to the malignant biological properties of AFP-producing gastric cancer
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  114. Significance of sTREM-1 and sST2 combined diagnosis for sepsis detection and prognosis prediction
  115. Diagnostic value of serum neuroactive substances in the acute exacerbation of chronic obstructive pulmonary disease complicated with depression
  116. Research progress of AMP-activated protein kinase and cardiac aging
  117. TRIM29 knockdown prevented the colon cancer progression through decreasing the ubiquitination levels of KRT5
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  120. The early diagnosis and pathogenic mechanisms of sepsis-related acute kidney injury
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  122. Erianin alleviates collagen-induced arthritis in mice by inhibiting Th17 cell differentiation
  123. Loss of ACOX1 in clear cell renal cell carcinoma and its correlation with clinical features
  124. Signalling pathways in the osteogenic differentiation of periodontal ligament stem cells
  125. Crosstalk between lactic acid and immune regulation and its value in the diagnosis and treatment of liver failure
  126. Clinicopathological features and differential diagnosis of gastric pleomorphic giant cell carcinoma
  127. Traumatic brain injury and rTMS-ERPs: Case report and literature review
  128. Extracellular fibrin promotes non-small cell lung cancer progression through integrin β1/PTEN/AKT signaling
  129. Knockdown of DLK4 inhibits non-small cell lung cancer tumor growth by downregulating CKS2
  130. The co-expression pattern of VEGFR-2 with indicators related to proliferation, apoptosis, and differentiation of anagen hair follicles
  131. Inflammation-related signaling pathways in tendinopathy
  132. CD4+ T cell count in HIV/TB co-infection and co-occurrence with HL: Case report and literature review
  133. Clinical analysis of severe Chlamydia psittaci pneumonia: Case series study
  134. Bioinformatics analysis to identify potential biomarkers for the pulmonary artery hypertension associated with the basement membrane
  135. Influence of MTHFR polymorphism, alone or in combination with smoking and alcohol consumption, on cancer susceptibility
  136. Catharanthus roseus (L.) G. Don counteracts the ampicillin resistance in multiple antibiotic-resistant Staphylococcus aureus by downregulation of PBP2a synthesis
  137. Combination of a bronchogenic cyst in the thoracic spinal canal with chronic myelocytic leukemia
  138. Bacterial lipoprotein plays an important role in the macrophage autophagy and apoptosis induced by Salmonella typhimurium and Staphylococcus aureus
  139. TCL1A+ B cells predict prognosis in triple-negative breast cancer through integrative analysis of single-cell and bulk transcriptomic data
  140. Ezrin promotes esophageal squamous cell carcinoma progression via the Hippo signaling pathway
  141. Ferroptosis: A potential target of macrophages in plaque vulnerability
  142. Predicting pediatric Crohn's disease based on six mRNA-constructed risk signature using comprehensive bioinformatic approaches
  143. Applications of genetic code expansion and photosensitive UAAs in studying membrane proteins
  144. HK2 contributes to the proliferation, migration, and invasion of diffuse large B-cell lymphoma cells by enhancing the ERK1/2 signaling pathway
  145. IL-17 in osteoarthritis: A narrative review
  146. Circadian cycle and neuroinflammation
  147. Probiotic management and inflammatory factors as a novel treatment in cirrhosis: A systematic review and meta-analysis
  148. Hemorrhagic meningioma with pulmonary metastasis: Case report and literature review
  149. SPOP regulates the expression profiles and alternative splicing events in human hepatocytes
  150. Knockdown of SETD5 inhibited glycolysis and tumor growth in gastric cancer cells by down-regulating Akt signaling pathway
  151. PTX3 promotes IVIG resistance-induced endothelial injury in Kawasaki disease by regulating the NF-κB pathway
  152. Pancreatic ectopic thyroid tissue: A case report and analysis of literature
  153. The prognostic impact of body mass index on female breast cancer patients in underdeveloped regions of northern China differs by menopause status and tumor molecular subtype
  154. Report on a case of liver-originating malignant melanoma of unknown primary
  155. Case report: Herbal treatment of neutropenic enterocolitis after chemotherapy for breast cancer
  156. The fibroblast growth factor–Klotho axis at molecular level
  157. Characterization of amiodarone action on currents in hERG-T618 gain-of-function mutations
  158. A case report of diagnosis and dynamic monitoring of Listeria monocytogenes meningitis with NGS
  159. Effect of autologous platelet-rich plasma on new bone formation and viability of a Marburg bone graft
  160. Small breast epithelial mucin as a useful prognostic marker for breast cancer patients
  161. Continuous non-adherent culture promotes transdifferentiation of human adipose-derived stem cells into retinal lineage
  162. Nrf3 alleviates oxidative stress and promotes the survival of colon cancer cells by activating AKT/BCL-2 signal pathway
  163. Favorable response to surufatinib in a patient with necrolytic migratory erythema: A case report
  164. Case report of atypical undernutrition of hypoproteinemia type
  165. Down-regulation of COL1A1 inhibits tumor-associated fibroblast activation and mediates matrix remodeling in the tumor microenvironment of breast cancer
  166. Sarcoma protein kinase inhibition alleviates liver fibrosis by promoting hepatic stellate cells ferroptosis
  167. Research progress of serum eosinophil in chronic obstructive pulmonary disease and asthma
  168. Clinicopathological characteristics of co-existing or mixed colorectal cancer and neuroendocrine tumor: Report of five cases
  169. Role of menopausal hormone therapy in the prevention of postmenopausal osteoporosis
  170. Precisional detection of lymph node metastasis using tFCM in colorectal cancer
  171. Advances in diagnosis and treatment of perimenopausal syndrome
  172. A study of forensic genetics: ITO index distribution and kinship judgment between two individuals
  173. Acute lupus pneumonitis resembling miliary tuberculosis: A case-based review
  174. Plasma levels of CD36 and glutathione as biomarkers for ruptured intracranial aneurysm
  175. Fractalkine modulates pulmonary angiogenesis and tube formation by modulating CX3CR1 and growth factors in PVECs
  176. Novel risk prediction models for deep vein thrombosis after thoracotomy and thoracoscopic lung cancer resections, involving coagulation and immune function
  177. Exploring the diagnostic markers of essential tremor: A study based on machine learning algorithms
  178. Evaluation of effects of small-incision approach treatment on proximal tibia fracture by deep learning algorithm-based magnetic resonance imaging
  179. An online diagnosis method for cancer lesions based on intelligent imaging analysis
  180. Medical imaging in rheumatoid arthritis: A review on deep learning approach
  181. Predictive analytics in smart healthcare for child mortality prediction using a machine learning approach
  182. Utility of neutrophil–lymphocyte ratio and platelet–lymphocyte ratio in predicting acute-on-chronic liver failure survival
  183. A biomedical decision support system for meta-analysis of bilateral upper-limb training in stroke patients with hemiplegia
  184. TNF-α and IL-8 levels are positively correlated with hypobaric hypoxic pulmonary hypertension and pulmonary vascular remodeling in rats
  185. Stochastic gradient descent optimisation for convolutional neural network for medical image segmentation
  186. Comparison of the prognostic value of four different critical illness scores in patients with sepsis-induced coagulopathy
  187. Application and teaching of computer molecular simulation embedded technology and artificial intelligence in drug research and development
  188. Hepatobiliary surgery based on intelligent image segmentation technology
  189. Value of brain injury-related indicators based on neural network in the diagnosis of neonatal hypoxic-ischemic encephalopathy
  190. Analysis of early diagnosis methods for asymmetric dementia in brain MR images based on genetic medical technology
  191. Early diagnosis for the onset of peri-implantitis based on artificial neural network
  192. Clinical significance of the detection of serum IgG4 and IgG4/IgG ratio in patients with thyroid-associated ophthalmopathy
  193. Forecast of pain degree of lumbar disc herniation based on back propagation neural network
  194. SPA-UNet: A liver tumor segmentation network based on fused multi-scale features
  195. Systematic evaluation of clinical efficacy of CYP1B1 gene polymorphism in EGFR mutant non-small cell lung cancer observed by medical image
  196. Rehabilitation effect of intelligent rehabilitation training system on hemiplegic limb spasms after stroke
  197. A novel approach for minimising anti-aliasing effects in EEG data acquisition
  198. ErbB4 promotes M2 activation of macrophages in idiopathic pulmonary fibrosis
  199. Clinical role of CYP1B1 gene polymorphism in prediction of postoperative chemotherapy efficacy in NSCLC based on individualized health model
  200. Lung nodule segmentation via semi-residual multi-resolution neural networks
  201. Evaluation of brain nerve function in ICU patients with Delirium by deep learning algorithm-based resting state MRI
  202. A data mining technique for detecting malignant mesothelioma cancer using multiple regression analysis
  203. Markov model combined with MR diffusion tensor imaging for predicting the onset of Alzheimer’s disease
  204. Effectiveness of the treatment of depression associated with cancer and neuroimaging changes in depression-related brain regions in patients treated with the mediator-deuterium acupuncture method
  205. Molecular mechanism of colorectal cancer and screening of molecular markers based on bioinformatics analysis
  206. Monitoring and evaluation of anesthesia depth status data based on neuroscience
  207. Exploring the conformational dynamics and thermodynamics of EGFR S768I and G719X + S768I mutations in non-small cell lung cancer: An in silico approaches
  208. Optimised feature selection-driven convolutional neural network using gray level co-occurrence matrix for detection of cervical cancer
  209. Incidence of different pressure patterns of spinal cerebellar ataxia and analysis of imaging and genetic diagnosis
  210. Pathogenic bacteria and treatment resistance in older cardiovascular disease patients with lung infection and risk prediction model
  211. Adoption value of support vector machine algorithm-based computed tomography imaging in the diagnosis of secondary pulmonary fungal infections in patients with malignant hematological disorders
  212. From slides to insights: Harnessing deep learning for prognostic survival prediction in human colorectal cancer histology
  213. Ecology and Environmental Science
  214. Monitoring of hourly carbon dioxide concentration under different land use types in arid ecosystem
  215. Comparing the differences of prokaryotic microbial community between pit walls and bottom from Chinese liquor revealed by 16S rRNA gene sequencing
  216. Effects of cadmium stress on fruits germination and growth of two herbage species
  217. Bamboo charcoal affects soil properties and bacterial community in tea plantations
  218. Optimization of biogas potential using kinetic models, response surface methodology, and instrumental evidence for biodegradation of tannery fleshings during anaerobic digestion
  219. Understory vegetation diversity patterns of Platycladus orientalis and Pinus elliottii communities in Central and Southern China
  220. Studies on macrofungi diversity and discovery of new species of Abortiporus from Baotianman World Biosphere Reserve
  221. Food Science
  222. Effect of berrycactus fruit (Myrtillocactus geometrizans) on glutamate, glutamine, and GABA levels in the frontal cortex of rats fed with a high-fat diet
  223. Guesstimate of thymoquinone diversity in Nigella sativa L. genotypes and elite varieties collected from Indian states using HPTLC technique
  224. Analysis of bacterial community structure of Fuzhuan tea with different processing techniques
  225. Untargeted metabolomics reveals sour jujube kernel benefiting the nutritional value and flavor of Morchella esculenta
  226. Mycobiota in Slovak wine grapes: A case study from the small Carpathians wine region
  227. Elemental analysis of Fadogia ancylantha leaves used as a nutraceutical in Mashonaland West Province, Zimbabwe
  228. Microbiological transglutaminase: Biotechnological application in the food industry
  229. Influence of solvent-free extraction of fish oil from catfish (Clarias magur) heads using a Taguchi orthogonal array design: A qualitative and quantitative approach
  230. Chromatographic analysis of the chemical composition and anticancer activities of Curcuma longa extract cultivated in Palestine
  231. The potential for the use of leghemoglobin and plant ferritin as sources of iron
  232. Investigating the association between dietary patterns and glycemic control among children and adolescents with T1DM
  233. Bioengineering and Biotechnology
  234. Biocompatibility and osteointegration capability of β-TCP manufactured by stereolithography 3D printing: In vitro study
  235. Clinical characteristics and the prognosis of diabetic foot in Tibet: A single center, retrospective study
  236. Agriculture
  237. Biofertilizer and NPSB fertilizer application effects on nodulation and productivity of common bean (Phaseolus vulgaris L.) at Sodo Zuria, Southern Ethiopia
  238. On correlation between canopy vegetation and growth indexes of maize varieties with different nitrogen efficiencies
  239. Exopolysaccharides from Pseudomonas tolaasii inhibit the growth of Pleurotus ostreatus mycelia
  240. A transcriptomic evaluation of the mechanism of programmed cell death of the replaceable bud in Chinese chestnut
  241. Melatonin enhances salt tolerance in sorghum by modulating photosynthetic performance, osmoregulation, antioxidant defense, and ion homeostasis
  242. Effects of plant density on alfalfa (Medicago sativa L.) seed yield in western Heilongjiang areas
  243. Identification of rice leaf diseases and deficiency disorders using a novel DeepBatch technique
  244. Artificial intelligence and internet of things oriented sustainable precision farming: Towards modern agriculture
  245. Animal Sciences
  246. Effect of ketogenic diet on exercise tolerance and transcriptome of gastrocnemius in mice
  247. Combined analysis of mRNA–miRNA from testis tissue in Tibetan sheep with different FecB genotypes
  248. Isolation, identification, and drug resistance of a partially isolated bacterium from the gill of Siniperca chuatsi
  249. Tracking behavioral changes of confined sows from the first mating to the third parity
  250. The sequencing of the key genes and end products in the TLR4 signaling pathway from the kidney of Rana dybowskii exposed to Aeromonas hydrophila
  251. Development of a new candidate vaccine against piglet diarrhea caused by Escherichia coli
  252. Plant Sciences
  253. Crown and diameter structure of pure Pinus massoniana Lamb. forest in Hunan province, China
  254. Genetic evaluation and germplasm identification analysis on ITS2, trnL-F, and psbA-trnH of alfalfa varieties germplasm resources
  255. Tissue culture and rapid propagation technology for Gentiana rhodantha
  256. Effects of cadmium on the synthesis of active ingredients in Salvia miltiorrhiza
  257. Cloning and expression analysis of VrNAC13 gene in mung bean
  258. Chlorate-induced molecular floral transition revealed by transcriptomes
  259. Effects of warming and drought on growth and development of soybean in Hailun region
  260. Effects of different light conditions on transient expression and biomass in Nicotiana benthamiana leaves
  261. Comparative analysis of the rhizosphere microbiome and medicinally active ingredients of Atractylodes lancea from different geographical origins
  262. Distinguish Dianthus species or varieties based on chloroplast genomes
  263. Comparative transcriptomes reveal molecular mechanisms of apple blossoms of different tolerance genotypes to chilling injury
  264. Study on fresh processing key technology and quality influence of Cut Ophiopogonis Radix based on multi-index evaluation
  265. An advanced approach for fig leaf disease detection and classification: Leveraging image processing and enhanced support vector machine methodology
  266. Erratum
  267. Erratum to “Protein Z modulates the metastasis of lung adenocarcinoma cells”
  268. Erratum to “BRCA1 subcellular localization regulated by PI3K signaling pathway in triple-negative breast cancer MDA-MB-231 cells and hormone-sensitive T47D cells”
  269. Retraction
  270. Retraction to “Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats”
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