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Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)

  • Yubo Wang , Bingyan Li , Yunfeng Li , Wei Du , Yueting Zhang , Yingyan Han , Chaojie Liu , Shuangxi Fan and Jinghong Hao EMAIL logo
Published/Copyright: April 29, 2022
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Open Life Sciences
From the journal Open Life Sciences Volume 17 Issue 1

Abstract

Plant bolting is regulated and controlled by various internal and external factors. We aimed to provide an improved method for breeding to determine whether there is a synergism between hormones and to explore the regulatory effect of plant hormones on the bolting of leaf lettuce. Lettuce plants were sprayed with exogenous auxin and gibberellin separately or in combination. The specific bolting period was determined by the change in stem length and cytological observation. The dynamic changes in endogenous hormones and genes closely related to bolting were analyzed. Treatment with gibberellin alone and the combined application of auxin and gibberellin induced bolting on the fourth day, and treatment with auxin alone resulted in bolting on the eighth day. In the early bolting stage, the auxin contents in the stems of the treatment groups, especially the combined gibberellin and auxin group, were higher than those of the control group. After the application of exogenous auxin and gibberellin, we found that the expression of the ARF8 and GID1 genes was upregulated. Based on the results of our study, combined treatment with exogenous gibberellin and auxin was the best method to promote the bolting of leaf lettuce, and the ARF8 and GID1 genes are closely related to this process.

Keywords: lettuce; gibberellin; auxin; bolting; gene expression

In lettuce (Lactuca sativa), the transition from the vegetative stage to the reproductive stage occurs in the meristem in the wreath. During the transition period, the apical meristem cap of vegetative branches is elongated, and then, a microflower primordium is formed [1]. Then, the stem internodes elongate rapidly, a process called bolting and inflorescence expansion, and the flowers bloom for a few days. Because lettuce is a crop grown for its foliage, early bolting is an unwelcome characteristic. Prolonging the nutritional period is conducive to leaf biomass accumulation and quality maintenance [2]. Very early varieties start bolting and flowering after planting for 7 weeks in a greenhouse, while very late varieties may bloom after planting for 4 months. Premature bolting can lead to partial or total yield loss, especially in early autumn planting in hot production areas. Therefore, the genetic basis of bolting-related regulation has been the focus of many studies for many years [3].

Inhibition of early bolting can help stabilize the yield [4,5]. Bolting and flowering are promoted to shorten the breeding cycle and speed up the breeding process. The bolting of vegetables is regulated by various endogenous and exogenous hormones, such as auxin, gibberellin, brassinolide, and ethylene [6], promoting bolting, while paclobutrazol [7] can inhibit bolting. Gibberellin (GA3) plays an important role in the bolting of vegetables. GA3 can break dormancy and promote bud development [8]. It was found that GA3 strongly promoted the bolting of Chinese cabbage, and as the GA3 concentration increased, this effect was enhanced [9]. As the first plant hormone discovered and isolated, IAA has been extensively studied. In the same plant, different concentrations of auxin usually have different effects. There is synergism and antagonism between plant hormones. Luckwill first proposed the hypothesis of “hormone balance” [10], in which this equilibrium state controls the metabolism of various substances, thus regulating the growth and development of plants [11].

Leaf lettuce (Lactuca sativa L.) is a vegetable in the Compositae family. Because of its crisp taste, rich nutrients, low carbohydrate content, and high level of dietary fiber [12], this vegetable has become increasingly popular in recent years. However, there have been few studies on the relationship between exogenous hormones and bolting of leaf lettuce, and most treatments in previous studies used single hormones. Few studies have explored the effect of spraying exogenous hormones on the bolting of leaf lettuce. The application of exogenous hormones can regulate the breeding cycle and provide better strategies for breeding. Studies have shown that gibberellin can partially or completely replace low-temperature vernalization to induce bolting and flowering ahead of time [13,14]; as the earliest discovered and isolated plant hormone, auxin plays a role in flower initiation [15,16]. Therefore, it is important to further clarify the relationship between exogenous auxin and gibberellin and their synergistic effects on the bolting of leaf lettuce.

1 Materials and methods

1.1 Experimental details and treatments

1.1.1 Experimental details

The variety of leaf lettuce used in these experiments is the germplasm material GB-31 preserved in the laboratory. The experiments were carried out in a multispan greenhouse on the eastern side of the Beijing University of Agriculture from January to June 2018. The initial conditions included light/dark (14 h/10 h) and day temperature/night temperature (20 ± 2°C/13 ± 2°C). The relative humidity was 50–70%. When the plants grew to six leaves, the culture conditions were as follows: day temperature/night temperature (20/13°C); light/dark (14 h/10 h); relative humidity: 60%; and spraying.

The seeds of GB-31 were sown in a 5 × 10 hole plug tray. When the seedlings had four leaves and one heart, they were transplanted to a nutrient bowl with a diameter of 15 cm. The ratio of the matrix used was peat:vermiculite:perlite = 2:1:1. When the lettuce had six leaves, plants at the same growth stage and good growth conditions were selected for the experimental treatments.

1.1.2 Treatments

There were four treatments in the experiments: 40 mg/L IAA, 25 mg/L GA3, 40 mg/L IAA + 25 mg/L GA3, and water spray that was used as a control (CK). The stem length was measured every 3 days after treatment with 10 replicates per treatment. After the IAA treatment, the samples were observed at 0, 2, 4, 6, 8, 12, 18, and 24 days after spraying. After treatment with GA3 and IAA + GA3, the samples were observed at 0, 2, 4, 6, 8, 12, and 16 days after spraying. The control group was sampled and observed at 0, 2, 4, 6, 8, 12, 16, 18, and 24 days after spraying. The sampling site was the stem, selected from the upper part within 1 cm below the shoot apex. For endogenous hormone determination, three plants were randomly selected from each treatment group, and three replicates were used for each treatment.

1.2 Determination methods

1.2.1 Physiological Index

After adding exogenous hormones, 10 plants were randomly selected from each treatment group every 3 days, and the stem length was measured and recorded with a measuring tape. The stem length was measured from the cotyledon to the shoot apex. The routine paraffin sectioning method was used for cytological observation, and the safranin-fast, green-dyeing method was used. The slice thickness was 10 μm, and a fluorescence microscope was used to observe and take photos at a scale of 200 μm. Endogenous hormones were determined by enzyme-linked immunosorbent assay (ELISA). The ELISA kit was provided by China Agricultural University. The tested hormones were gibberellin (GA), auxin (IAA), abscisic acid (ABA), and brassinolide (BR).

1.2.2 Quantitative fluorescent PCR

To detect the expression of gibberellin biosynthesis- and transduction-related enzymes, we selected related genes for fluorescence quantitative PCR by reading the literature. 18 S ribosomal RNA was used as an internal reference gene, and a reaction system of 10 μL was as follows (Table 1).

Table 1

System for the quantitative determination of gene expression by real-time fluorescence

Material Volume (μL)
cDNA 1
Primer 1 1
Primer 2 1
SYBR Green 5
DEPC-treated ddH2O 2
Total Volume 10

The cDNA obtained by reverse transcription was subjected to quantitative fluorescent PCR with a 5-fold gradient dilution (1, 1/10, 1/100, 1/1,000, and 1/10,000). The reaction procedure was as follows: predenaturation at 95°C for 3 min; denaturation at 95°C for 20 s, annealing at 53°C for 20 s, and extension at 72°C for 20 s (40 cycles); finally, 65–95°C, with every rise of 0.5°C for 30 s; and the fluorescence value was detected and the dissolution curve was drawn. The reaction procedure of the internal reference gene was the same as that of the target gene, and each sample was assayed three times. The 2−△△Ct method was used for calculations [17].

1.2.3 Statistical analysis

Excel 2016 was used for data processing, the test data are expressed as the mean ± standard deviation, and the standard deviation was calculated by t-tests. SPSS 20.0 software was used to analyze the significance of differences, and OriginPro 9.0 software was used for mapping.

2 Results

2.1 Effects of exogenous auxin and gibberellin on lettuce bolting

Spraying the plants with gibberellin alone, auxin alone, or a combination of both could promote the stem elongation of lettuce, but the effect was different (Figure 1). Over time, the stem length of leaf lettuce was significantly different. After applying GA3 and a combination of GA3 and auxin, the stem length of leaf lettuce grew faster. On the third day, the stems treated with exogenous gibberellin or gibberellin and auxin showed obvious elongation, and the stem lengths reached 1.55 and 1.33 cm, respectively, which were significantly different from that of the control group. On the 6th day, there was a significant difference between the two groups, and the treatment with a combination of auxin and gibberellin resulted in longer stems than the treatment with GA3 alone. On the 12th day, the stem length of the group treated with GA3 alone was longer than that of the group treated with auxin and GA3. The application of auxin alone also promoted the stem elongation of lettuce, but the effect was slow. On the sixth day, the stem length of the group treated with auxin alone was 1.9 cm, which was 1.43 times longer than that of the control group. This difference was significant from the 15th day. In the control group, the stem length changed slowly. On Day 0, the stem length was 0.7 cm. On the 24th day, the stem length was only 4.3 cm, and the rate of stem elongation was much slower than that of the hormone treatment groups.

Figure 1 Stem length changes after treatment with GA3 or IAA.
Figure 1

Stem length changes after treatment with GA3 or IAA.

2.2 Microscopic observation of the shoot tip of lettuce treated with exogenous auxin and gibberellin

As shown in Figure 2, on the fourth day, the shoot tip became thinner, the growth point changed from conical to flat. The flower bud began to differentiate, and the growth point entered the stage of the hypertrophic growth. On the 6th day, a point-like protuberance was formed around the growth point, multiple involucres and primordia were differentiated and bent inward, and the scales of involucre entered the initial stage of differentiation. On the 12th day, the primordium of the involucre elongated upward and completely wrapped the growth point and entered the final stage of involucre differentiation. On the 16th day, irregular granular bulges were formed around the growth point, and floret primordium differentiation occurred. In the group treated with auxin alone, the flower bud differentiation rate was slow. On the 8th day, this group entered the hypertrophic growth stage. On the 18th day, a bulge was formed around the growth point, and the involucre primordium was formed. On the 24th day, the involucre primordium extended upward to wrap the growth point and entered the final stage of involucre differentiation. However, in the control group, on the 18th day, flower bud differentiation appeared, and the hypertrophic growth stage occurred.

Figure 2 Comparison of the flower bud differentiation of lettuce after treatment with GA3 or IAA. Note: A, B, C, and D represent the control group, exogenous IAA treatment group, exogenous GA3 treatment group, and combined IAA and GA3 treatment group, respectively. (a and b) Represent flower bud differentiation at 0, 2, 6, 8, 12, 16, and 24 days from left to right. (c and d) Represent flower bud differentiation at 0, 2, 4, 6, 8, 12, and 16 from left to right.
Figure 2

Comparison of the flower bud differentiation of lettuce after treatment with GA3 or IAA. Note: A, B, C, and D represent the control group, exogenous IAA treatment group, exogenous GA3 treatment group, and combined IAA and GA3 treatment group, respectively. (a and b) Represent flower bud differentiation at 0, 2, 6, 8, 12, 16, and 24 days from left to right. (c and d) Represent flower bud differentiation at 0, 2, 4, 6, 8, 12, and 16 from left to right.

2.3 Changes in endogenous hormonal contents in lettuce stem after exogenous auxin and gibberellin application

2.3.1 Changes in the GA3 content in lettuce stems after exogenous auxin and gibberellin treatment

The GA3 content in the stem of leaf lettuce was 24.1 ng/g FW on Day 0. With the passage of treatment time, the content of GA3 in the stem of leaf lettuce decreased. The content of GA3 in the stems of the treatment group was slightly higher than that of the control group; the content of GA3 following exogenous spraying treatment was higher than that following the other treatments.

2.3.2 Changes in IAA content in lettuce stems treated with exogenous auxin and gibberellin

As shown in Figure 3, with the extension of treatment time, the IAA content in the stems of plants treated with hormones showed a similar pattern: the level first increased, followed by a decrease and another increase. The content of IAA reached a peak on the 6th day after treatment with exogenous GA3 and combined IAA and GA3 and was significantly different from that of the control group. At this time, the endogenous IAA concentration reached 51.17 and 56.20 ng/g FW, respectively, and then decreased; the IAA concentration in the stems of the group treated with auxin alone peaked on the 8th day and then decreased, and the IAA content in the early treatment group was higher; on the 12th day, the content of IAA in the control group was higher than that of the groups treated with exogenous hormones.

Figure 3 Changes in endogenous hormones in the stems of lettuce after treatment with GA3 or IAA.
Figure 3

Changes in endogenous hormones in the stems of lettuce after treatment with GA3 or IAA.

2.3.3 Changes in the ABA content in lettuce stems treated with exogenous auxin and gibberellin

As shown in Figure 3, the ABA content in the stems of leaf lettuce treated with IAA alone and combined IAA and GA3 was lower than that in the control group, and the ABA content in the stem decreased and was lower than that at 0 days. The content of endogenous ABA in stems increased after exogenous GA3 application. On the fourth day, the ABA content in the stems of the groups treated with GA3 alone or combined IAA and GA3 increased briefly and then decreased. After treatment with exogenous IAA, the ABA concentration decreased slowly and began to decline on the 8th day. From the 6th day, the ABA content in the control group was gradually higher than that in the groups treated with exogenous hormones.

2.3.4 Changes in BR content in lettuce stems treated with exogenous auxin and gibberellin

With the prolongation of treatment time, the BR content in the stems of the treatment group was higher than that of the control group in the early stage after the application of GA3 and combined IAA and GA3, and the highest values were found on day 4 and day 6, respectively, followed by a decrease. After treatment with IAA alone, the BR content in the stem increased slowly in the early stage and was lower than that after treatment with exogenous GA3 and the mixture of IAA and GA3; overall, the content of BR continued to increase and was significantly higher than that of other treatment groups after 12 days.

2.4 Effect of exogenous auxin and gibberellin on gene expression related to hormone signal transduction

Based on previous studies in our laboratory, the ARF1, ARF2, ARF4, ARF5, and ARF8 genes that may be related to bolting and flowering were selected to measure their relative expression in different treatments. On the 4th day, the relative expression of the ARF1 gene in the groups treated with exogenous IAA, GA3, and combined IAA and GA3 was lower than that of the control group, while the relative expression of the ARF1 gene was downregulated by GA3 alone or by a combination of IAA and GA3. On the 8th day, the relative expression of ARF1 in the groups treated with GA3 and combined IAA and GA3 was higher than that of the control group. On the 12th day, the relative expression of ARF1 decreased significantly in the group treated with IAA alone but increased in the group treated with GA3 and combined IAA and GA3. On the 18th day, the relative expression of ARF1 in IAA-treated plants continued to decrease and was only 0.016 times that in the control. For the ARF2 gene, the relative expression level in the groups treated with GA3 and combined IAA and GA3 was low in the early stage and increased rapidly on the 12th day, reaching a level that was 6.2 times and 24.2 times that of the control group, respectively. The expression level of IAA was higher on the 4th and 18th days. The relative expression of the ARF4 gene decreased on the 4th day, increased from the 6th day and was maintained at a high level. On the 4th day, the relative expression of the ARF5 gene in the treatment group was lower than that in the control group and then remained at a low level. On the 12th day, the relative expression of the ARF5 gene in the group treated with combined IAA and GA3 was significantly upregulated compared with the control. The relative expression of the ARF8 gene was upregulated on the 4th and 6th days, decreased on the 8th day, and was higher than that in the control group on the 12th day. After administration of IAA, the ARF8 gene was significantly upregulated on the 8th and 12th days and was downregulated on the 18th day. For the GID1 gene, the GA3 and combined IAA and GA3 treatments increased the expression from the 4th day and decreased it from the 8th day, but the relative expression remained at a relatively higher level. The relative expression level of GID1 after IAA treatment was almost the same as that of the control group on the fourth day, increased slightly on the eighth day, and remained at a higher level than that of the control group. The expression level of the RGL1 gene increased from the 4th day after the application of GA3 and combined IAA and GA3, peaked on the 8th day, and then decreased. The relative expression of IAA on the 12th and 18th days was 18.2 and 9.4 times higher than that of the control group, respectively, and the difference was significant (Figure 4).

Figure 4 Analysis of the mRNA expression levels of auxin and gibberellin signal transduction-related genes during leaflet lettuce development after treatment with GA3 or IAA. Note：**indicates a significant difference at P ≤ 0.01, and *indicates a significant difference at P ≤ 0.05.111.
Figure 4

Analysis of the mRNA expression levels of auxin and gibberellin signal transduction-related genes during leaflet lettuce development after treatment with GA3 or IAA. Note：**indicates a significant difference at P ≤ 0.01, and *indicates a significant difference at P ≤ 0.05.111.

3 Discussion

In the process of lettuce cultivation, lettuce shortening, stem elongation, and even bolting will affect the “leaf” harvest of lettuce, resulting in the decline of lettuce yield [18]. “GB-31,” as an easy bolting variety, is in line with the research direction of this experiment, so it is selected as the experimental material. Previous studies have shown that the concentrations of GA3 and auxin are positively correlated with bolting rate and bolting height. Therefore, it is speculated that spraying auxin and gibberellin will have a certain effect on lettuce bolting. ARF is an auxin-responsive factor and GID1 is a gibberellin receptor. The expression of the ARF gene and GID1 is helpful to further explore the bolting mechanism of leaf lettuce between auxin and gibberellin [19].

Gibberellin is an important plant hormone, which participates in many processes of regulating plant physiology [20]. One of the more prominent characteristics is to promote shoot tip elongation and plant height. Lettuce bolting is stimulated by environmental changes such as temperature and sunshine length. With the differentiation of flower buds, the stem begins to elongate rapidly and the plant becomes higher, which has a great relationship with this experimental treatment. In addition, through paraffin sectioning and whole plant photograph observation, it was found that spraying auxin promoted the lateral width of the stem. At the same stage of flower bud differentiation, the stems treated with auxin were thicker compared with other treatments, and the stems treated with combined gibberellin and auxin were thicker than those treated with gibberellin alone. Liu et al. found that after bolting lettuce with heat-treated leaves, the levels of GA3 and GA4 and the content of indole acetic acid (IAA) in stems increased sharply and remained stable. Further study found that the effect of GA3 and IAA mixed spraying was better than that of single spraying, and the bolting phenomenon occurred in 4 days. This finding is similar to the conclusion that GA3 and IAA combined application on flue-cured tobacco has a better effect on improving quality than a single application [11]. At the same time, this experiment found that the bolting time of IAA alone was relatively late, but it can promote the increase of endogenous GA3 content in the stem. It is speculated that the effect of mixed spraying is more obvious, which may be related to IAA promoting the increase of GA3 content and further promoting the elongation and growth of the stem.

Different hormones have different regulatory effects on plant bolting, some play a direct role, some play an indirect role, and then affect lettuce bolting by affecting the expression of other hormones [21,22]. As the earliest discovered plant hormone, auxin plays an important role in the whole process of plant growth and development. It is not only involved in regulating cell elongation, division and differentiation, and apical dominance but also involved in signal transduction and flower development. Previous studies have suggested that a low concentration of IAA promoted bolting, while a high concentration of IAA was not conducive to bolting [23,24]. In recent years, it has been found that a low concentration of IAA at an early stage promotes bolting and flowering, but a higher IAA concentration is required at the bolting stage [25]. In this study, although different treatments resulted in different times of bolting, the trend of change in the endogenous IAA content of the stems was similar, with higher concentrations at the beginning of bolting, lower concentrations in the early stage of bolting, and a gradual decrease after bolting. which is basically consistent with the previous research results, which further proves that IAA is involved in the bolting of lettuce.

ARF protein family is a key protein in response to auxin signal and plays an important role in the auxin signal transduction pathway. There are many members of the ARF family, and there are great functional differences among different ARF proteins. So far, 23 at ARF genes have been found in Arabidopsis. The ARF1 gene plays an important role in plant growth and vesicle transport [26], maintenance of some organelles [27,28], and antiviral defense. After exogenous IAA application, ARF1 gene expression in the stem remained at a high level in the early stage; treatment with GA3 or a combination of IAA and GA3 led to increases on the 8th day; however, the relative expression of the ARF1 gene in the IAA treatment group was much higher than that in the other two hormone treatment groups. It was speculated that exogenous IAA promoted ARF1 gene expression and that GA3 inhibited ARF1 gene expression. Yang Xiao [29] and others found that the ARF2 gene was expressed at high levels in tomato flower buds. In this study, the relative expression levels in the groups with the GA3 and combined IAA and GA3 treatments were lower in the early stage and increased rapidly on the 12th day, which was the final stage of involucre scale differentiation. The expression level in the group treated with IAA alone was higher on the 4th and 18th days. The expression of the ARF2 gene was upregulated on the 18th day after IAA treatment, which may have been due to preparation for floret primordium differentiation. In the Arabidopsis thaliana, the ARF4 gene is involved in flower development [30]. In this study, we found that the relative expression of the ARF4 gene was lower after the application of GA3 alone, IAA and GA3 combined, and IAA on the 8th day; that is, the expression of the ARF4 gene decreased at the beginning of flower bud differentiation. However, it increased gradually after bolting, which indicated that the ARF4 gene may play a role in promoting the late bolting stage [31]. In this study, when GA3 and IAA and GA3 were applied, the relative expression of the ARF8 gene was lower on the 4th to 8th days and the 12th day. After the application of exogenous IAA, the expression level was upregulated from Day 8 to Day 12 and downregulated on Day 18. The results showed that the ARF8 gene promoted bolting [32].

GID1 is a soluble protein-encoding gibberellin. It combines with GA to recognize DELLA in the nucleus, resulting in polyubiquitination of the DELLA protein, degradation of DELLA protein, and release of gene expression inhibited by DELLA [13]. In this study, compared with that of the control group, the expression of the GID1 gene was higher in the group sprayed with IAA, GA3 alone, and the mixture of IAA and GA3 at the beginning of bolting, indicating that the GID1 gene may promote bolting. After the three treatments, the expression of RGL1 increased gradually after bolting and then decreased slowly, with the highest concentration at the stage of bulb scale differentiation. It is speculated that the possible mechanism is that the degradation of DELLA makes a large number of gibberellin express, to induce the rapid growth of lettuce stems and bolting. The expression of RGL1 was lower in the early stage of bolting, and the relative expression of RGL1 was higher after bolting. These results indicated that RGL1 played an important role in flower development. In research on Arabidopsis thaliana, it was also found that RGL1 plays an important role in regulating flower bud differentiation and flower development [33,34].

In conclusion, based on the rapid elongation of stems and microscopic observation of flower bud differentiation, the combination of gibberellin and auxin has a synergistic effect. A combination of exogenous applications of gibberellin and auxin can promote leaf lettuce bolting. ARF8 and GID1 are involved in the bolting leaf lettuce. ARF1, ARF2, ARF4, and RGL1 may participate in flower development, but the relationship between the ARF5 gene and bolting and flowering is not clear.

# These authors contributed equally to this work

  1. Funding information: This work was financially supported by the National Natural Science Foundation of China (Grant No. 32072560), the 2018 Joint Funding Project of Beijing Natural Science Foundation-the Municipal Education Commission (KZ201810020027), and the Beijing Leafy Vegetables Innovation Team of Modern Agro-industry Technology Research System (BAIC07-2021).

  2. Conflict of interest: 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: 2021-04-15
Revised: 2022-01-24
Accepted: 2022-01-25
Published Online: 2022-04-29

© 2022 Yubo Wang et al., published by De Gruyter

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

Articles in the same Issue

  1. Biomedical Sciences
  2. Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
  3. The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
  4. Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
  5. LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
  6. Association study of CLDN14 variations in patients with kidney stones
  7. Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
  8. Regulation of miR-30b in cancer development, apoptosis, and drug resistance
  9. Informatic analysis of the pulmonary microecology in non-cystic fibrosis bronchiectasis at three different stages
  10. Swimming attenuates tumor growth in CT-26 tumor-bearing mice and suppresses angiogenesis by mediating the HIF-1α/VEGFA pathway
  11. Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
  12. Functional conservation and divergence in plant-specific GRF gene family revealed by sequences and expression analysis
  13. Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
  14. Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
  15. Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
  16. Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
  17. Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
  18. Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
  19. Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
  20. Nutrition intervention in the management of novel coronavirus pneumonia patients
  21. circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
  22. Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
  23. Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
  24. Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
  25. Comparison of axon extension: PTFE versus PLA formed by a 3D printer
  26. Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
  27. A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
  28. Study on the mechanism of inhibiting patulin production by fengycin
  29. SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
  30. Relationship between blood clots and COVID-19 vaccines: A literature review
  31. Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
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  35. Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
  36. Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
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  38. Genetic susceptibility to high myopia in Han Chinese population
  39. Potential biomarkers and molecular mechanisms in preeclampsia progression
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  43. Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
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  46. Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
  47. MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
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  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
  51. Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
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  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
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  66. Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
  67. Aberrant pulmonary immune response of obese mice to periodontal infection
  68. Bacteriospermia – A formidable player in male subfertility
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  71. Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
  72. Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
  73. Prognostic signature related to the immune environment of oral squamous cell carcinoma
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  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
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  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
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  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
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  171. Erratum
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  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
https://doi.org/10.1515/biol-2022-0043
Keywords for this article
lettuce; gibberellin; auxin; bolting; gene expression
Creative Commons
BY 4.0

Articles in the same Issue

  1. Biomedical Sciences
  2. Effects of direct oral anticoagulants dabigatran and rivaroxaban on the blood coagulation function in rabbits
  3. The mother of all battles: Viruses vs humans. Can humans avoid extinction in 50–100 years?
  4. Knockdown of G1P3 inhibits cell proliferation and enhances the cytotoxicity of dexamethasone in acute lymphoblastic leukemia
  5. LINC00665 regulates hepatocellular carcinoma by modulating mRNA via the m6A enzyme
  6. Association study of CLDN14 variations in patients with kidney stones
  7. Concanavalin A-induced autoimmune hepatitis model in mice: Mechanisms and future outlook
  8. Regulation of miR-30b in cancer development, apoptosis, and drug resistance
  9. Informatic analysis of the pulmonary microecology in non-cystic fibrosis bronchiectasis at three different stages
  10. Swimming attenuates tumor growth in CT-26 tumor-bearing mice and suppresses angiogenesis by mediating the HIF-1α/VEGFA pathway
  11. Characterization of intestinal microbiota and serum metabolites in patients with mild hepatic encephalopathy
  12. Functional conservation and divergence in plant-specific GRF gene family revealed by sequences and expression analysis
  13. Application of the FLP/LoxP-FRT recombination system to switch the eGFP expression in a model prokaryote
  14. Biomedical evaluation of antioxidant properties of lamb meat enriched with iodine and selenium
  15. Intravenous infusion of the exosomes derived from human umbilical cord mesenchymal stem cells enhance neurological recovery after traumatic brain injury via suppressing the NF-κB pathway
  16. Effect of dietary pattern on pregnant women with gestational diabetes mellitus and its clinical significance
  17. Potential regulatory mechanism of TNF-α/TNFR1/ANXA1 in glioma cells and its role in glioma cell proliferation
  18. Effect of the genetic mutant G71R in uridine diphosphate-glucuronosyltransferase 1A1 on the conjugation of bilirubin
  19. Quercetin inhibits cytotoxicity of PC12 cells induced by amyloid-beta 25–35 via stimulating estrogen receptor α, activating ERK1/2, and inhibiting apoptosis
  20. Nutrition intervention in the management of novel coronavirus pneumonia patients
  21. circ-CFH promotes the development of HCC by regulating cell proliferation, apoptosis, migration, invasion, and glycolysis through the miR-377-3p/RNF38 axis
  22. Bmi-1 directly upregulates glucose transporter 1 in human gastric adenocarcinoma
  23. Lacunar infarction aggravates the cognitive deficit in the elderly with white matter lesion
  24. Hydroxysafflor yellow A improved retinopathy via Nrf2/HO-1 pathway in rats
  25. Comparison of axon extension: PTFE versus PLA formed by a 3D printer
  26. Elevated IL-35 level and iTr35 subset increase the bacterial burden and lung lesions in Mycobacterium tuberculosis-infected mice
  27. A case report of CAT gene and HNF1β gene variations in a patient with early-onset diabetes
  28. Study on the mechanism of inhibiting patulin production by fengycin
  29. SOX4 promotes high-glucose-induced inflammation and angiogenesis of retinal endothelial cells by activating NF-κB signaling pathway
  30. Relationship between blood clots and COVID-19 vaccines: A literature review
  31. Analysis of genetic characteristics of 436 children with dysplasia and detailed analysis of rare karyotype
  32. Bioinformatics network analyses of growth differentiation factor 11
  33. NR4A1 inhibits the epithelial–mesenchymal transition of hepatic stellate cells: Involvement of TGF-β–Smad2/3/4–ZEB signaling
  34. Expression of Zeb1 in the differentiation of mouse embryonic stem cell
  35. Study on the genetic damage caused by cadmium sulfide quantum dots in human lymphocytes
  36. Association between single-nucleotide polymorphisms of NKX2.5 and congenital heart disease in Chinese population: A meta-analysis
  37. Assessment of the anesthetic effect of modified pentothal sodium solution on Sprague-Dawley rats
  38. Genetic susceptibility to high myopia in Han Chinese population
  39. Potential biomarkers and molecular mechanisms in preeclampsia progression
  40. Silencing circular RNA-friend leukemia virus integration 1 restrained malignancy of CC cells and oxaliplatin resistance by disturbing dyskeratosis congenita 1
  41. Endostar plus pembrolizumab combined with a platinum-based dual chemotherapy regime for advanced pulmonary large-cell neuroendocrine carcinoma as a first-line treatment: A case report
  42. The significance of PAK4 in signaling and clinicopathology: A review
  43. Sorafenib inhibits ovarian cancer cell proliferation and mobility and induces radiosensitivity by targeting the tumor cell epithelial–mesenchymal transition
  44. Characterization of rabbit polyclonal antibody against camel recombinant nanobodies
  45. Active legumain promotes invasion and migration of neuroblastoma by regulating epithelial-mesenchymal transition
  46. Effect of cell receptors in the pathogenesis of osteoarthritis: Current insights
  47. MT-12 inhibits the proliferation of bladder cells in vitro and in vivo by enhancing autophagy through mitochondrial dysfunction
  48. Study of hsa_circRNA_000121 and hsa_circRNA_004183 in papillary thyroid microcarcinoma
  49. BuyangHuanwu Decoction attenuates cerebral vasospasm caused by subarachnoid hemorrhage in rats via PI3K/AKT/eNOS axis
  50. Effects of the interaction of Notch and TLR4 pathways on inflammation and heart function in septic heart
  51. Monosodium iodoacetate-induced subchondral bone microstructure and inflammatory changes in an animal model of osteoarthritis
  52. A rare presentation of type II Abernethy malformation and nephrotic syndrome: Case report and review
  53. Rapid death due to pulmonary epithelioid haemangioendothelioma in several weeks: A case report
  54. Hepatoprotective role of peroxisome proliferator-activated receptor-α in non-cancerous hepatic tissues following transcatheter arterial embolization
  55. Correlation between peripheral blood lymphocyte subpopulations and primary systemic lupus erythematosus
  56. A novel SLC8A1-ALK fusion in lung adenocarcinoma confers sensitivity to alectinib: A case report
  57. β-Hydroxybutyrate upregulates FGF21 expression through inhibition of histone deacetylases in hepatocytes
  58. Identification of metabolic genes for the prediction of prognosis and tumor microenvironment infiltration in early-stage non-small cell lung cancer
  59. BTBD10 inhibits glioma tumorigenesis by downregulating cyclin D1 and p-Akt
  60. Mucormycosis co-infection in COVID-19 patients: An update
  61. Metagenomic next-generation sequencing in diagnosing Pneumocystis jirovecii pneumonia: A case report
  62. Long non-coding RNA HOXB-AS1 is a prognostic marker and promotes hepatocellular carcinoma cells’ proliferation and invasion
  63. Preparation and evaluation of LA-PEG-SPION, a targeted MRI contrast agent for liver cancer
  64. Proteomic analysis of the liver regulating lipid metabolism in Chaohu ducks using two-dimensional electrophoresis
  65. Nasopharyngeal tuberculosis: A case report
  66. Characterization and evaluation of anti-Salmonella enteritidis activity of indigenous probiotic lactobacilli in mice
  67. Aberrant pulmonary immune response of obese mice to periodontal infection
  68. Bacteriospermia – A formidable player in male subfertility
  69. In silico and in vivo analysis of TIPE1 expression in diffuse large B cell lymphoma
  70. Effects of KCa channels on biological behavior of trophoblasts
  71. Interleukin-17A influences the vulnerability rather than the size of established atherosclerotic plaques in apolipoprotein E-deficient mice
  72. Multiple organ failure and death caused by Staphylococcus aureus hip infection: A case report
  73. Prognostic signature related to the immune environment of oral squamous cell carcinoma
  74. Primary and metastatic squamous cell carcinoma of the thyroid gland: Two case reports
  75. Neuroprotective effects of crocin and crocin-loaded niosomes against the paraquat-induced oxidative brain damage in rats
  76. Role of MMP-2 and CD147 in kidney fibrosis
  77. Geometric basis of action potential of skeletal muscle cells and neurons
  78. Babesia microti-induced fulminant sepsis in an immunocompromised host: A case report and the case-specific literature review
  79. Role of cerebellar cortex in associative learning and memory in guinea pigs
  80. Application of metagenomic next-generation sequencing technique for diagnosing a specific case of necrotizing meningoencephalitis caused by human herpesvirus 2
  81. Case report: Quadruple primary malignant neoplasms including esophageal, ureteral, and lung in an elderly male
  82. Long non-coding RNA NEAT1 promotes angiogenesis in hepatoma carcinoma via the miR-125a-5p/VEGF pathway
  83. Osteogenic differentiation of periodontal membrane stem cells in inflammatory environments
  84. Knockdown of SHMT2 enhances the sensitivity of gastric cancer cells to radiotherapy through the Wnt/β-catenin pathway
  85. Continuous renal replacement therapy combined with double filtration plasmapheresis in the treatment of severe lupus complicated by serious bacterial infections in children: A case report
  86. Simultaneous triple primary malignancies, including bladder cancer, lymphoma, and lung cancer, in an elderly male: A case report
  87. Preclinical immunogenicity assessment of a cell-based inactivated whole-virion H5N1 influenza vaccine
  88. One case of iodine-125 therapy – A new minimally invasive treatment of intrahepatic cholangiocarcinoma
  89. S1P promotes corneal trigeminal neuron differentiation and corneal nerve repair via upregulating nerve growth factor expression in a mouse model
  90. Early cancer detection by a targeted methylation assay of circulating tumor DNA in plasma
  91. Calcifying nanoparticles initiate the calcification process of mesenchymal stem cells in vitro through the activation of the TGF-β1/Smad signaling pathway and promote the decay of echinococcosis
  92. Evaluation of prognostic markers in patients infected with SARS-CoV-2
  93. N6-Methyladenosine-related alternative splicing events play a role in bladder cancer
  94. Characterization of the structural, oxidative, and immunological features of testis tissue from Zucker diabetic fatty rats
  95. Effects of glucose and osmotic pressure on the proliferation and cell cycle of human chorionic trophoblast cells
  96. Investigation of genotype diversity of 7,804 norovirus sequences in humans and animals of China
  97. Characteristics and karyotype analysis of a patient with turner syndrome complicated with multiple-site tumors: A case report
  98. Aggravated renal fibrosis is positively associated with the activation of HMGB1-TLR2/4 signaling in STZ-induced diabetic mice
  99. Distribution characteristics of SARS-CoV-2 IgM/IgG in false-positive results detected by chemiluminescent immunoassay
  100. SRPX2 attenuated oxygen–glucose deprivation and reperfusion-induced injury in cardiomyocytes via alleviating endoplasmic reticulum stress-induced apoptosis through targeting PI3K/Akt/mTOR axis
  101. Aquaporin-8 overexpression is involved in vascular structure and function changes in placentas of gestational diabetes mellitus patients
  102. Relationship between CRP gene polymorphisms and ischemic stroke risk: A systematic review and meta-analysis
  103. Effects of growth hormone on lipid metabolism and sexual development in pubertal obese male rats
  104. Cloning and identification of the CTLA-4IgV gene and functional application of vaccine in Xinjiang sheep
  105. Antitumor activity of RUNX3: Upregulation of E-cadherin and downregulation of the epithelial–mesenchymal transition in clear-cell renal cell carcinoma
  106. PHF8 promotes osteogenic differentiation of BMSCs in old rat with osteoporosis by regulating Wnt/β-catenin pathway
  107. A review of the current state of the computer-aided diagnosis (CAD) systems for breast cancer diagnosis
  108. Bilateral dacryoadenitis in adult-onset Still’s disease: A case report
  109. A novel association between Bmi-1 protein expression and the SUVmax obtained by 18F-FDG PET/CT in patients with gastric adenocarcinoma
  110. The role of erythrocytes and erythroid progenitor cells in tumors
  111. Relationship between platelet activation markers and spontaneous abortion: A meta-analysis
  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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