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Sensitivity difference between skotomorphogenesis and photomorphogenesis of plants to antibiotics: A call for research
Chemosphere 242 (2020) 125261
Contents lists available at ScienceDirect
Chemosphere journal homepage: www.elsevier.com/locate/chemosphere
Discussion
Sensitivity difference between skotomorphogenesis and photomorphogenesis of plants to antibiotics: A call for research Yuan Luo a, b, Jie Liang a, b, *, Guangming Zeng a, b a b
College of Environmental Science and Engineering, Hunan University, Changsha 410082, China Key Laboratory of Environmental Biology and Pollution Control (Hunan University), Ministry of Education, Changsha 410082, China
g r a p h i c a l a b s t r a c t
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 August 2019 Received in revised form 28 October 2019 Accepted 29 October 2019 Available online 1 November 2019
Seedling establishment consists of the former stage (i.e. skotomorphogenesis) and the latter stage (i.e. photomorphogenesis). Due to specific developmental processes in plants, the two stages may have different sensitivities to antibiotics. Tetracycline (TC), for example, is a major-use antibiotic. Radicle length, the relatively sensitive endpoint in plant skotomorphogenesis, is less sensitive than all of the indices of cotyledon colour and pigments in plant photomorphogenesis to TC stress. In conclusion, we suggest that plant photomorphogenesis may be more sensitive than plant skotomorphogenesis to stresses of antibiotics, but which needs further studies. © 2019 Elsevier Ltd. All rights reserved.
Handling Editor: Willie Peijnenburg Keywords: Tetracycline Phytotoxicity Seedling establishment Skotomorphogenesis Photomorphogenesis
The process of seedling establishment begins with seed germination when the heterotrophic growth of emerging seedling
* Corresponding author. College of Environmental Science and Engineering, Hunan University, Changsha 410082, China. E-mail address: [email protected] (J. Liang). https://doi.org/10.1016/j.chemosphere.2019.125261 0045-6535/© 2019 Elsevier Ltd. All rights reserved.
depends on seed reserves, and it is completed when the seedling has gained photosynthetic ability and develops into to the autotrophic growth stage (Gommers and Monte, 2018). Based on the environmental conditions for morphogenesis, seedling establishment can be divided into two developmental stages, i.e. skotomorphogenesis and photomorphogenesis (Vinh et al., 2018). At the
2
Y. Luo et al. / Chemosphere 242 (2020) 125261
former stage, plants grow in the dark and the biggest change through observation is characterized by the rapid elongation of radicles. Subsequently, at the latter stage, plants need light for development and the most obvious change is characterized by the greening of cotyledons. In the last few years, the environmental risks caused by the continuous release of antibiotics have aroused wide attention for their assessment (Azanu et al., 2018; Kuppusamy et al., 2018; Pufal et al., 2019; Rede et al., 2019) and control (Jiang et al., 2018; Krzeminski et al., 2019; Liang et al., 2019). In plant skotomorphogenesis, radicle length was adopted as a relatively sensitive endpoint to evaluate the phytotoxicity of tetracycline (TC), a major-use antibiotic. A existing study showed that the radicle length of Chinese cabbage (Brassica rapa L.) was significantly inhibited by TC at 5 mM (Luo et al., 2019). However, so far there is a lack of research on the antibiotics affecting plant growth in photomorphogenesis rather than in skotomorphogenesis or after seedling establishment (Yu et al., 2017; Liu et al., 2018; McGinnis et al., 2019). Therefore, based on the adverse effect caused by TC stress on the skotomorphogenesis of plants, we are here to raise a question: Is photomorphogenesis more sensitive than skotomorphogenesis to the stress (Fig. 1)? We conducted a simple experiment to answer the question above. The plant, Chinese cabbage (Brassica rapa L.), and its culturing method were the same as those in a recent study (Luo et al., 2019). In the experiment, the radicle change was recorded and measured in plant skotomorphogenesis, and the cotyledon change was done in plant photomorphogenesis. We found that photomorphogenesis is more sensitive than skotomorphogenesis of Chinese cabbage to TC stress. After the first incubation in the dark for 48 h, the difference in radicle length between the control (0 mM) and TC treatments (1 and 5 mM) could be observed directly (Fig. 2a). The relative radicle lengths of 1 and 5 mM TC were 93.95% and 76.92% of the control respectively, but it was only for 5 mM TC with a significant difference (P < 0.01) (Fig. 2b). Next, the second incubation was performed under a light intensity of 80 mmol m2 s1 for 12 h, the colour of cotyledons was dark green, bright yellow with pale-green tinges, and bright yellow in the control and treatments, respectively (Fig. 3a). For relative gray value of green colour (RGVG) measured by ImageJ software (US NIH), it was 74.86% and 60.10% of the control with significant differences (P < 0.01) in the treatments, respectively (Fig. 3b). Further, the results of the composition of cotyledon pigments showed that the content of chlorophyll a (Ca) was 27.17% and merely 3.76% of the control in the treatments, respectively; 23.28% and merely 1.45% for chlorophyll b (Cb); and
Fig. 2. Changes of the radicle of Chinese cabbage (Brassica rapa L.) seeds exposed to tetracycline (TC). (a) The seeds after 48 h of the first incubation in the dark; (b) boxplot of radicle length (RL) (n ¼ 80 seeds). The solid and dash lines, lower and upper edges, bars and dots in or beyond the box represent median and mean values, 25th and 75th, 5th and 95th percentiles, and outliers (beyond 1.5 times the box height) of all data, respectively. The dots and curve at the right of the box illustrate the data and the normal distribution curve fitted to them. The mean values are marked with lowercase letters from large to small. For statistical results, boxes are not labelled with a same lower-case or upper-case letter, which indicate that there are significant differences among the mean values at P < 0.05 or P < 0.01.
63.58% and 29.11% for total carotenoids (Cxþc), respectively (Fig. 3b). For every kind of pigment, there were significant differences among the control and treatments (P < 0.01). Overall, the indices related to plant photomorphogenesis were more susceptible than the radicle length related to plant skotomorphogenesis to TC stress. In conclusion, considering the effectiveness of result and the accuracy of measurement, we recommend that Ca in plant photomorphogenesis can be adopted as an endpoint to evaluate the phytotoxicity of TC at environmentally related levels, i.e. high ng
Fig. 1. The underlying sensitivities of skotomorphogenesis and photomorphogenesis of Chinese cabbage (Brassica rapa L.) to tetracycline stress.
Y. Luo et al. / Chemosphere 242 (2020) 125261
3
Fig. 3. Changes of the cotyledon of Chinese cabbage (Brassica rapa L.) seeds exposed to tetracycline (TC). (a) The seeds after 12 h of the second incubation under a light intensity of 80 mmol m2 s1; (b) relative gray value of green colour (RGVG) (n ¼ 40 seeds) and pigment content (n ¼ 4 dishes) of the cotyledon. The mean values are marked with lowercase letters from large to small. For statistical results, boxes are not labelled with a same upper-case letter, which indicate that differences among the mean values are significant at P < 0.01. Ca, chlorophyll a; Cb, chlorophyll b; Cxþc, total carotenoids. The method for determining the pigment content is according to the study of Lichtenthaler and Wellburn (1983) and acetone 80% (v/v) is used as a solvent.
L1 to low mg L1 in waters and low mg kg1 to high mg kg1 in soils (Zhang et al., 2015; Deng et al., 2018; Kuppusamy et al., 2018). Although the sensitivity of plant photomorphogenesis to TC may be primarily dependent on its specific action site and translocation in plants, it deserves future studies, as well as the underlying mechanisms, that whether this conclusion can be still valid for other antibiotics and with universality. No conflict of interest exits in the submission of this manuscript. Acknowledgements This work was supported by the National Natural Science Foundation of China [51679082, 51479072, 51521006], the Hunan Science & Technology Innovation Program [2018RS3037] and the Hunan Natural Science Foundation for Distinguished Young Scholars [2019JJ20002]. References Azanu, D., Styrishave, B., Darko, G., Weisser, J.J., Abaidoo, R.C., 2018. Occurrence and risk assessment of antibiotics in water and lettuce in Ghana. Sci. Total Environ. 622e623, 293e305. Deng, Y., Li, B., Zhang, T., 2018. Bacteria that make a meal of sulfonamide antibiotics: blind spots and emerging opportunities. Environ. Sci. Technol. 52, 3854e3868. Gommers, C.M.M., Monte, E., 2018. Seedling establishment: a dimmer switchregulated process between dark and light signaling. Plant Physiol. 176, 1061e1074. Jiang, L., Yuan, X., Zeng, G., Wu, Z., Liang, J., Chen, X., Leng, L., Wang, H., Wang, H.,
2018. Metal-free efficient photocatalyst for stable visible-light photocatalytic degradation of refractory pollutant. Appl. Catal. B Environ. 221, 715e725. Krzeminski, P., Tomei, M.C., Karaolia, P., Langenhoff, A., Almeida, C.M.R., Felis, E., Gritten, F., Andersen, H.R., Fernandes, T., Manaia, C.M., Rizzo, L., FattaKassinos, D., 2019. Performance of secondary wastewater treatment methods for the removal of contaminants of emerging concern implicated in crop uptake and antibiotic resistance spread: a review. Sci. Total Environ. 648, 1052e1081. Kuppusamy, S., Kakarla, D., Venkateswarlu, K., Megharaj, M., Yoon, Y., Lee, Y.B., 2018. Veterinary antibiotics (VAs) contamination as a global agro-ecological issue: a critical view. Agric. Ecosyst. Environ. 257, 47e59. Liang, J., Fang, Y., Luo, Y., Zeng, G., Deng, J., Tan, X., Tang, N., Li, X., He, X., Feng, C., Ye, S., 2019. Magnetic nanoferromanganese oxides modified biochar derived from pine sawdust for adsorption of tetracycline hydrochloride. Environ. Sci. Pollut. Res. 26, 5892e5903. Lichtenthaler, H.K., Wellburn, A.R., 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 11, 591e592. Liu, X., Lv, Y., Xu, K., Xiao, X., Xi, B., Lu, S., 2018. Response of ginger growth to a tetracycline-contaminated environment and residues of antibiotic and antibiotic resistance genes. Chemosphere 201, 137e143. Luo, Y., Liang, J., Zeng, G., Li, X., Chen, M., Jiang, L., Xing, W., Tang, N., Fang, Y., Chen, X., 2019. Evaluation of tetracycline phytotoxicity by seed germination stage and radicle elongation stage tests: a comparison of two typical methods for analysis. Environ. Pollut. 251, 257e263. McGinnis, M., Sun, C., Dudley, S., Gan, J., 2019. Effect of low-dose, repeated exposure of contaminants of emerging concern on plant development and hormone homeostasis. Environ. Pollut. 252, 706e714. Pufal, G., Memmert, J., Leonhardt, S.D., Minden, V., 2019. Negative bottom-up effects of sulfadiazine, but not penicillin and tetracycline, in soil substitute on plants and higher trophic levels. Environ. Pollut. 245, 531e544. ~o, C., Sousa, S.R., DelerueRede, D., Santos, L.H.M.L., Ramos, S., Oliva-Teles, F., Anta Matos, C., 2019. Individual and mixture toxicity evaluation of three pharmaceuticals to the germination and growth of Lactuca sativa seeds. Sci. Total Environ. 673, 102e109.
4
Y. Luo et al. / Chemosphere 242 (2020) 125261
Vinh, N.P., Kathare, P.K., Huq, E., 2018. Phytochromes and phytochrome interacting factors. Plant Physiol. 176, 1025e1038. Yu, Q., Ahammed, G.J., Zhou, Y., Shi, K., Zhou, J., Yu, Y., Yu, J., Xia, X., 2017. Nitric oxide is involved in the oxytetracycline-induced suppression of root growth through inhibiting hydrogen peroxide accumulation in the root meristem. Sci. Rep.-UK.
7, 1e13. Zhang, Q., Ying, G., Pan, C., Liu, Y., Zhao, J., 2015. Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ. Sci. Technol. 49, 6772e6782.
Contents lists available at ScienceDirect
Chemosphere journal homepage: www.elsevier.com/locate/chemosphere
Discussion
Sensitivity difference between skotomorphogenesis and photomorphogenesis of plants to antibiotics: A call for research Yuan Luo a, b, Jie Liang a, b, *, Guangming Zeng a, b a b
College of Environmental Science and Engineering, Hunan University, Changsha 410082, China Key Laboratory of Environmental Biology and Pollution Control (Hunan University), Ministry of Education, Changsha 410082, China
g r a p h i c a l a b s t r a c t
a r t i c l e i n f o
a b s t r a c t
Article history: Received 27 August 2019 Received in revised form 28 October 2019 Accepted 29 October 2019 Available online 1 November 2019
Seedling establishment consists of the former stage (i.e. skotomorphogenesis) and the latter stage (i.e. photomorphogenesis). Due to specific developmental processes in plants, the two stages may have different sensitivities to antibiotics. Tetracycline (TC), for example, is a major-use antibiotic. Radicle length, the relatively sensitive endpoint in plant skotomorphogenesis, is less sensitive than all of the indices of cotyledon colour and pigments in plant photomorphogenesis to TC stress. In conclusion, we suggest that plant photomorphogenesis may be more sensitive than plant skotomorphogenesis to stresses of antibiotics, but which needs further studies. © 2019 Elsevier Ltd. All rights reserved.
Handling Editor: Willie Peijnenburg Keywords: Tetracycline Phytotoxicity Seedling establishment Skotomorphogenesis Photomorphogenesis
The process of seedling establishment begins with seed germination when the heterotrophic growth of emerging seedling
* Corresponding author. College of Environmental Science and Engineering, Hunan University, Changsha 410082, China. E-mail address: [email protected] (J. Liang). https://doi.org/10.1016/j.chemosphere.2019.125261 0045-6535/© 2019 Elsevier Ltd. All rights reserved.
depends on seed reserves, and it is completed when the seedling has gained photosynthetic ability and develops into to the autotrophic growth stage (Gommers and Monte, 2018). Based on the environmental conditions for morphogenesis, seedling establishment can be divided into two developmental stages, i.e. skotomorphogenesis and photomorphogenesis (Vinh et al., 2018). At the
2
Y. Luo et al. / Chemosphere 242 (2020) 125261
former stage, plants grow in the dark and the biggest change through observation is characterized by the rapid elongation of radicles. Subsequently, at the latter stage, plants need light for development and the most obvious change is characterized by the greening of cotyledons. In the last few years, the environmental risks caused by the continuous release of antibiotics have aroused wide attention for their assessment (Azanu et al., 2018; Kuppusamy et al., 2018; Pufal et al., 2019; Rede et al., 2019) and control (Jiang et al., 2018; Krzeminski et al., 2019; Liang et al., 2019). In plant skotomorphogenesis, radicle length was adopted as a relatively sensitive endpoint to evaluate the phytotoxicity of tetracycline (TC), a major-use antibiotic. A existing study showed that the radicle length of Chinese cabbage (Brassica rapa L.) was significantly inhibited by TC at 5 mM (Luo et al., 2019). However, so far there is a lack of research on the antibiotics affecting plant growth in photomorphogenesis rather than in skotomorphogenesis or after seedling establishment (Yu et al., 2017; Liu et al., 2018; McGinnis et al., 2019). Therefore, based on the adverse effect caused by TC stress on the skotomorphogenesis of plants, we are here to raise a question: Is photomorphogenesis more sensitive than skotomorphogenesis to the stress (Fig. 1)? We conducted a simple experiment to answer the question above. The plant, Chinese cabbage (Brassica rapa L.), and its culturing method were the same as those in a recent study (Luo et al., 2019). In the experiment, the radicle change was recorded and measured in plant skotomorphogenesis, and the cotyledon change was done in plant photomorphogenesis. We found that photomorphogenesis is more sensitive than skotomorphogenesis of Chinese cabbage to TC stress. After the first incubation in the dark for 48 h, the difference in radicle length between the control (0 mM) and TC treatments (1 and 5 mM) could be observed directly (Fig. 2a). The relative radicle lengths of 1 and 5 mM TC were 93.95% and 76.92% of the control respectively, but it was only for 5 mM TC with a significant difference (P < 0.01) (Fig. 2b). Next, the second incubation was performed under a light intensity of 80 mmol m2 s1 for 12 h, the colour of cotyledons was dark green, bright yellow with pale-green tinges, and bright yellow in the control and treatments, respectively (Fig. 3a). For relative gray value of green colour (RGVG) measured by ImageJ software (US NIH), it was 74.86% and 60.10% of the control with significant differences (P < 0.01) in the treatments, respectively (Fig. 3b). Further, the results of the composition of cotyledon pigments showed that the content of chlorophyll a (Ca) was 27.17% and merely 3.76% of the control in the treatments, respectively; 23.28% and merely 1.45% for chlorophyll b (Cb); and
Fig. 2. Changes of the radicle of Chinese cabbage (Brassica rapa L.) seeds exposed to tetracycline (TC). (a) The seeds after 48 h of the first incubation in the dark; (b) boxplot of radicle length (RL) (n ¼ 80 seeds). The solid and dash lines, lower and upper edges, bars and dots in or beyond the box represent median and mean values, 25th and 75th, 5th and 95th percentiles, and outliers (beyond 1.5 times the box height) of all data, respectively. The dots and curve at the right of the box illustrate the data and the normal distribution curve fitted to them. The mean values are marked with lowercase letters from large to small. For statistical results, boxes are not labelled with a same lower-case or upper-case letter, which indicate that there are significant differences among the mean values at P < 0.05 or P < 0.01.
63.58% and 29.11% for total carotenoids (Cxþc), respectively (Fig. 3b). For every kind of pigment, there were significant differences among the control and treatments (P < 0.01). Overall, the indices related to plant photomorphogenesis were more susceptible than the radicle length related to plant skotomorphogenesis to TC stress. In conclusion, considering the effectiveness of result and the accuracy of measurement, we recommend that Ca in plant photomorphogenesis can be adopted as an endpoint to evaluate the phytotoxicity of TC at environmentally related levels, i.e. high ng
Fig. 1. The underlying sensitivities of skotomorphogenesis and photomorphogenesis of Chinese cabbage (Brassica rapa L.) to tetracycline stress.
Y. Luo et al. / Chemosphere 242 (2020) 125261
3
Fig. 3. Changes of the cotyledon of Chinese cabbage (Brassica rapa L.) seeds exposed to tetracycline (TC). (a) The seeds after 12 h of the second incubation under a light intensity of 80 mmol m2 s1; (b) relative gray value of green colour (RGVG) (n ¼ 40 seeds) and pigment content (n ¼ 4 dishes) of the cotyledon. The mean values are marked with lowercase letters from large to small. For statistical results, boxes are not labelled with a same upper-case letter, which indicate that differences among the mean values are significant at P < 0.01. Ca, chlorophyll a; Cb, chlorophyll b; Cxþc, total carotenoids. The method for determining the pigment content is according to the study of Lichtenthaler and Wellburn (1983) and acetone 80% (v/v) is used as a solvent.
L1 to low mg L1 in waters and low mg kg1 to high mg kg1 in soils (Zhang et al., 2015; Deng et al., 2018; Kuppusamy et al., 2018). Although the sensitivity of plant photomorphogenesis to TC may be primarily dependent on its specific action site and translocation in plants, it deserves future studies, as well as the underlying mechanisms, that whether this conclusion can be still valid for other antibiotics and with universality. No conflict of interest exits in the submission of this manuscript. Acknowledgements This work was supported by the National Natural Science Foundation of China [51679082, 51479072, 51521006], the Hunan Science & Technology Innovation Program [2018RS3037] and the Hunan Natural Science Foundation for Distinguished Young Scholars [2019JJ20002]. References Azanu, D., Styrishave, B., Darko, G., Weisser, J.J., Abaidoo, R.C., 2018. Occurrence and risk assessment of antibiotics in water and lettuce in Ghana. Sci. Total Environ. 622e623, 293e305. Deng, Y., Li, B., Zhang, T., 2018. Bacteria that make a meal of sulfonamide antibiotics: blind spots and emerging opportunities. Environ. Sci. Technol. 52, 3854e3868. Gommers, C.M.M., Monte, E., 2018. Seedling establishment: a dimmer switchregulated process between dark and light signaling. Plant Physiol. 176, 1061e1074. Jiang, L., Yuan, X., Zeng, G., Wu, Z., Liang, J., Chen, X., Leng, L., Wang, H., Wang, H.,
2018. Metal-free efficient photocatalyst for stable visible-light photocatalytic degradation of refractory pollutant. Appl. Catal. B Environ. 221, 715e725. Krzeminski, P., Tomei, M.C., Karaolia, P., Langenhoff, A., Almeida, C.M.R., Felis, E., Gritten, F., Andersen, H.R., Fernandes, T., Manaia, C.M., Rizzo, L., FattaKassinos, D., 2019. Performance of secondary wastewater treatment methods for the removal of contaminants of emerging concern implicated in crop uptake and antibiotic resistance spread: a review. Sci. Total Environ. 648, 1052e1081. Kuppusamy, S., Kakarla, D., Venkateswarlu, K., Megharaj, M., Yoon, Y., Lee, Y.B., 2018. Veterinary antibiotics (VAs) contamination as a global agro-ecological issue: a critical view. Agric. Ecosyst. Environ. 257, 47e59. Liang, J., Fang, Y., Luo, Y., Zeng, G., Deng, J., Tan, X., Tang, N., Li, X., He, X., Feng, C., Ye, S., 2019. Magnetic nanoferromanganese oxides modified biochar derived from pine sawdust for adsorption of tetracycline hydrochloride. Environ. Sci. Pollut. Res. 26, 5892e5903. Lichtenthaler, H.K., Wellburn, A.R., 1983. Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem. Soc. Trans. 11, 591e592. Liu, X., Lv, Y., Xu, K., Xiao, X., Xi, B., Lu, S., 2018. Response of ginger growth to a tetracycline-contaminated environment and residues of antibiotic and antibiotic resistance genes. Chemosphere 201, 137e143. Luo, Y., Liang, J., Zeng, G., Li, X., Chen, M., Jiang, L., Xing, W., Tang, N., Fang, Y., Chen, X., 2019. Evaluation of tetracycline phytotoxicity by seed germination stage and radicle elongation stage tests: a comparison of two typical methods for analysis. Environ. Pollut. 251, 257e263. McGinnis, M., Sun, C., Dudley, S., Gan, J., 2019. Effect of low-dose, repeated exposure of contaminants of emerging concern on plant development and hormone homeostasis. Environ. Pollut. 252, 706e714. Pufal, G., Memmert, J., Leonhardt, S.D., Minden, V., 2019. Negative bottom-up effects of sulfadiazine, but not penicillin and tetracycline, in soil substitute on plants and higher trophic levels. Environ. Pollut. 245, 531e544. ~o, C., Sousa, S.R., DelerueRede, D., Santos, L.H.M.L., Ramos, S., Oliva-Teles, F., Anta Matos, C., 2019. Individual and mixture toxicity evaluation of three pharmaceuticals to the germination and growth of Lactuca sativa seeds. Sci. Total Environ. 673, 102e109.
4
Y. Luo et al. / Chemosphere 242 (2020) 125261
Vinh, N.P., Kathare, P.K., Huq, E., 2018. Phytochromes and phytochrome interacting factors. Plant Physiol. 176, 1025e1038. Yu, Q., Ahammed, G.J., Zhou, Y., Shi, K., Zhou, J., Yu, Y., Yu, J., Xia, X., 2017. Nitric oxide is involved in the oxytetracycline-induced suppression of root growth through inhibiting hydrogen peroxide accumulation in the root meristem. Sci. Rep.-UK.
7, 1e13. Zhang, Q., Ying, G., Pan, C., Liu, Y., Zhao, J., 2015. Comprehensive evaluation of antibiotics emission and fate in the river basins of China: source analysis, multimedia modeling, and linkage to bacterial resistance. Environ. Sci. Technol. 49, 6772e6782.