Next Article in Journal
Estimation of the Total Nonstructural Carbohydrate Concentration in Apple Trees Using Hyperspectral Imaging
Previous Article in Journal
Shoot Dieback in Thornless Blackberries in Northern Spain Caused by Diaporthe rudis and Gnomoniopsis idaeicola
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 9
Issue 9
10.3390/horticulturae9090966
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effect of Ozone Stresses on Growth and Secondary Plant Metabolism of Brassica campestris L. ssp. chinensis

by
Young Jong Han
1,*,
Winston Beck
1,
Inga Mewis
2,
Nadja Förster
1 and
Christian Ulrichs
1
1
Faculty of Life Sciences, Division Urban Plant Ecophysiology, Humboldt-Universität zu Berlin, Lentzeallee 55-57, 14195 Berlin, Germany
2
Faculty of Life Sciences, Division Biosystems Engineering, Humboldt-Universität zu Berlin, Albrecht-Thaer-Weg 3, 14195 Berlin, Germany
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(9), 966; https://doi.org/10.3390/horticulturae9090966
Submission received: 25 July 2023 / Revised: 20 August 2023 / Accepted: 23 August 2023 / Published: 25 August 2023
(This article belongs to the Section Biotic and Abiotic Stress)
Browse Figures
Versions Notes

Abstract

:
Determining plant responses to hazardous air pollutants is critical in predicting food security programs and challenges in the future. This study aimed to determine the effects of various ozone levels on plant growth responses (leaf area, dry matter, and number of leaves) and biochemical quality (photopigments and glucosinolates) on Brassica campestris L. ssp. chinensis (Pak-Choi). The experiment was conducted within test chambers under different ozone concentrations (60, 150, and 240 ppb for 2 h/day). Leaf area and dry matter were negatively correlated with increasing ozone concentrations, but the number of leaves was not affected by ozone treatment. Lycopene and chlorophylls also showed the same tendency. Even if the ambient ozone concentration was only elevated for a short time, various glucosnilates (GLS) have been diversely affected. The total aliphatic GLS content was reduced. In contrast, the total indole GLS increased at the highest ozone concentration, and the aromatic GLS significantly increased and then decreased as the ozone concentration level increased. These results provide evidence of the strong effect of ozone stress on the plant quality of Pak-Choi with respect to certain secondary plant metabolites. These findings provide an understanding of elevated ozone effects in urban horticulture sites on the growth and metabolite profiling of Brassica plants.

1. Introduction

Rapid global climate change and air pollution are closely connected and represent a substantial part of environmental problems. The most important air pollutants that interact with and influence climates are aerosols and tropospheric ozone [1,2]. Tropospheric ozone causes damage to humans, animals, and plants if the concentration is high, and it has strong oxidation effects to corrode plastic, metal, textiles, and rubber products [3,4,5,6,7,8,9]. Human activities generate primary pollutants, such as HCs, Nox, and VOCs, which are involved in atmospheric chemical reactions that produce ozone as secondary pollutants [9,10,11]. In urban settings, ozone levels can reach over 300 ppb [12]. High levels of ozone concentrations can often be attributed to locally generated ozone because of heavy traffic and transported ozone precursors. Therefore, areas around the world have seen a gradual increase in ozone warnings [13,14].
A growing body of research provides an overview of the impacts of ozone; however, effects are dependent on the ozone level, duration, and type of plant, as the interaction between plants and ozone is known to positively or negatively affect plant growth and metabolisms [5,7,8].
Plant biochemical responses to ozone exposure have been mostly investigated by determining the effects of oxidative cell disruption [15]. At continuously high ozone conditions, the increased oxidative stress leads to a reduction in the transcription of genes encoding proteins involved in photosynthesis (chlorophyll and protein processing) and finally promotes degradation and early senescence symptoms in leaves [8,16,17]. Some researchers, however, reported that while not significant, there are positive effects of ozone on chlorophyll [18,19]. For agricultural crops, most of the research has been conducted looking at yield losses. In open chamber experiments with ambient ozone concentrations, yield reductions have been calculated. For the US, losses have been calculated to be about 5% of the total national production [20], while yield losses of up to 20% have been calculated for sensitive crops in the Mediterranean [21]. Plant quality parameters have often been overlooked in these studies.
Brassica campestris L. ssp. chinensis (Pak-Choi) is an important Brassica leafy vegetable crop and is widely cultivated in East Asia [22,23]. Research targeting secondary plant metabolism, especially when it comes to metabolites important to human health in horticultural products, is scarce. Brassica plants have a variety of secondary metabolites that are functional substances, such as ascorbic acid, glucosinolates (GLS), and polyphenols [24]. GLS are amino acid-derived secondary compounds important for plant defense, which are found mostly in Brassica plants. Elevated ozone also has GLS-reducing effects on Brassica plants [18,25,26]. In general, when Brassica plants are treated with ozone stress conditions continuously, the total GLS tends to reduce [27,28]. However, some previous studies have shown that the different GLS types in plants can significantly differ in responses [27,28,29].
This study investigates the response of different ozone concentrations on Pak-Choi, the most common Brassica crop. The aim of this study was to determine the responses of various ozone levels on Pak-Choi by assessing the plant growth and biochemical quality responses.

2. Materials and Methods

2.1. Plant Material and Experimental Setup

Test plants Brassica campestris L. ssp. chinensis (Pak-Choi) were grown in controlled environment growth chambers (Adaptis A 1000, Co., Conviron, Winnipeg, MB, Canada). Growth chamber control conditions were a 13 h photoperiod at temperature 23/20 °C (day/night/optimum) for 4 weeks, and plants were cultivated in 9 × 9 cm pots. Each test plant was given fertilizer by watering with diluted Yamazaki solution [30]. Afterward, test plants were transferred to an airtight ozone test chamber (airtight bio-chamber, 240 L volume; GMS GmbH, Berlin, Germany), where they were treated with different ozone concentrations for 6 days. Fifteen randomly selected pots were used as test plants in the growth chamber for each ozone treatment and repetitive test. The airtight ozone test chamber includes an ozone generator (MP 1000, A2Z Ozone, Inc. Louisville, KY, USA) and an ozone concentration monitor (BMT 930, BMT GMBH, Berlin, Germany) that allows real-time control and logging of the ozone concentration. The airtight ozone test chamber also includes two circulating fans to promote complete mixing of the air. This airtight ozone test chamber was installed in a controlled environment growth chamber to control the temperature and light regime. The airtight ozone test chamber was built according to modified materials and methods in [18,31]. Prior to ozone treatments, plants were watered to saturation and then placed in the airtight ozone test chamber. All treatment tests were performed in triplicate for each condition, and all measurements were performed at a minimum repetition of twelve times.
Leaf material was used to survey plant growth variables (leaf area, number of leaves, and dry matter). To analyze biochemical quality (photopigments and GLS), samples consisting of all leaves at the early vegetative plant growth stage test plants from youngest to oldest (excluding cotyledons) were frozen in liquid nitrogen immediately after harvesting then stored at −20 °C until analysis.

2.2. Ozone Gas Treatments

The test plant’s age is sensitive to environmental change stresses [32,33]. Plants were randomly assigned to one of two test chambers. The ozone concentration treatments were based on the air quality guides for ozone index [34,35]. The ozone concentrations used in the experiments for the different treatments were 60, 150, and 240 ppb for 2 h/day.

2.3. Determination of Plant Growth Variables

The plant growth variables (such as leaf area, number of leaves, and dry matter) were determined after ozone tests. The leaf area and number of leaves were determined with a leaf area meter (3100 Area Meter, Co. LI-COR. Inc., Lincoln, NE, USA) for all leaves of test plants from youngest to oldest, excluding cotyledons. Dry matter was determined by drying the samples in a thermal dryer at 105 °C for 48 h until constant weight.

2.4. Determination of Photopigments

Total carotenoids, β-carotene, lutein, lycopene, and chlorophylls were determined according to modified methods in [36]. Fresh frozen samples (0.5 g) from each tested plant were put into glass centrifuge tubes (50 mL volume). The samples were homogenized with acetone–hexane (4/5, v/v; 15 mL) using an Ultra Turrax (T-25, IKA, Staufen, Germany). The supernatant liquid was transferred to a flask (25 mL volume) after centrifuged at 4000 rpm for 10 min at room temperature. Pellets were then washed with 2 mL of acetone–hexane and transferred into new 15 mL glass centrifuge tubes prior to centrifugation at 4000 rpm for 10 m at room temperature. This procedure was repeated once more, then a spectrophotometer (UV-Mini-1240, Shimadzu, Tokyo, Japan) was used to measure extinction and calculate photopigment contents (Table 1), total carotenoids (445 nm), β-carotene (450 nm), lutein (453 nm), lycopene (505 nm), and chlorophylls (663 and 645 nm) before transfer of liquid samples into glass cuvettes.

2.5. Determination of GLSs

GLSs were determined according to a modified method in [37]. Freeze-dried ground samples (20 mg) were extracted in 750 µL boiling methanol (70%), and sinalbin was added (1 mM; p-hydroxybenzyl GLS; internal standard). The tubes containing sample were centrifuged (10,000 rpm, 5 min, room temperature) before being transferred to an 80 °C thermomixer for 5 min, and then the supernatant was collected. This process was repeated twice, and 10 mL volume cartridges (BIORAD) were loaded with 500 µL DEAE Sephadex (suspended in 2 M acetic acid, v/v, 1/2) for desulfation. Columns were conditioned with 2 mL imidazole solution (6 M in 30% formic acid) and followed by 2 mL ultra-pure water. Methanolic GLS extracts were loaded onto columns and followed with 2 mL sodium acetate buffer (0.02 M, pH 4.0). A total of 75 µL of a cleaned-up thioglucosidase (sulfatase solution, Sigma-Aldrich, Inc., St. Louis, MO, USA) was added to the columns. After incubation overnight, the columns were washed using 1 mL ultra-pure water. Samples were stored in deep freezer at −80 °C until HPLC measurement. The GLSs were quantitatively and qualitatively analyzed using UHPLC system (UltiMate 3000 HPLC, Thermo Scientific, Waltham, MA, USA) (Table 2).

2.6. Statistical Calculations

The data were analyzed with the SAS program (9.4 version, SAS Institute Inc., Cary, NC, USA) for the significant difference [38]. The significant differences in variables were determined using ANOVA Tukey’s HSD test (p ≤ 0.05). Variability of the mean is indicated by the standard error in tables and figures.

3. Results

3.1. Effects of Ozone Concentrations on Growth Variables

The leaf area was not significantly different at 60 and 150 ppb ozone levels but was significantly reduced at 240 ppb ozone treatments (Figure 1a). However, the number of leaves was not affected (Figure 1b). Thus, dry matter was negatively correlated with increasing ozone concentrations (Figure 1c).

3.2. Effects of Ozone Concentrations on Photopigments

The photopigment contents were quantitatively increased at 60 and 150 ppb ozone treatments in comparison with the control. The lycopene, chlorophyll a, b, and total chlorophyll decreased significantly in the 240 ppb ozone treatment condition. However, none of the lutein, total carotenoids, and β-carotene analyzed were significantly changed through ozone treatment (Figure 2a–c).
The ANOVA elucidates that lycopene content for ozone exposure concentration was significantly increased at 60 and 150 ppb ozone exposure conditions, with no significant difference between control and 240 ppb exposure conditions. Chlorophyll a, b, and total chlorophyll showed the same tendency as lycopene (Figure 2d,e).

3.3. Effects of Ozone Concentrations on Glucosinolate Profile

This study identified a total of twelve GLS from the leaves of Pak-Choi, comprising aliphatic (seven), indole (four), and one aromatic GLS (Table 3). Elevated ozone levels decreased the content of the analyzed total aliphatic GLS in Pak-Choi. In contrast, most indole GLS increased through ozone treatment. The aromatic GLS increased and then decreased as the ozone concentration level increased (Table 4).

4. Discussion

4.1. Plant Growth Variables Affected by Ozone Concentration Treatments

In Triticum aestivum and Trifolium repens, ozone had a negative effect on the overall leaf area of individual plants [39]. In contrast, [40] found that in Betula pendula, plants that were exposed to ozone, instead of retaining damaged leaves, reacted by developing new leaves. These new leaves were smaller, which reduced the total leaf area. The decrease in leaf area in this study (Figure 1a) may be due to the effects of ozone-damaging mesophyll cells when absorbed by plants. In young leaves of Nicotiana tabacum, oxidative stress damage was much stronger and more intense than in old leaves [32]. Additionally, many researchers have reported that growth activity to ozone stress differs by plant species [5,41,42,43]. In other words, the test species plays an important role in the study of ozone impacts on plants; accordingly, genetic diversity among species and plant ontogenies within species should also be considered.
One of the plant responses to increased ozone levels is a decrease in biomass [44]. In Betula pendula, treatment with ozone between 70 and 100 ppb decreased yield by 27% compared to ambient air [7]. In Triticum aestivum, under high ozone levels, the quantity and quality of plants also deteriorated [4]. Several researchers reported that biomass in the mainstream plant was reduced under conditions of ozone stress [45,46]. Likewise, in Trifolium repens, the group treated with 120 ppb ozone had a 36% reduction in plant biomass in comparison to the control group, and Triticum aestivum was negatively impacted [39]. In Brassica napus L., total seed mass also decreased with increasing ozone exposure [47]. Ref. [5] reported that treatment with elevated ozone above ambient levels led to a reduction in plant biomass, which is similar to our results. Photosynthesis and respiration rates decrease when usable carbon is reduced due to ozone stress [48].

4.2. Photopigments Effected by Ozone Concentration Treatments

Many researchers have reported that under ozone stress, the photosynthesis capacity and photopigment contents decrease. In nine soybean cultivars, pigment contents in plants exposed to ozone were significantly reduced [49]. Ref. [50] reported that the chloroplasts in the ozone-affected leaves decreased both in number and size and eventually degraded. Among the organs of a plant, leaves are most influenced by ozone. The ozone-stressed plants show early defoliation and fast aging signs due to a reduction in the contents of photopigments [51]. In Brassica crops [47,52] and in Glycine max [49,53,54] under ozone stress, the photosynthetic rate and pigment contents decreased. In potatoes, elevated ozone reduced photosynthesis and promoted senescence [55]. Some researchers point out the reduction in stomatal conductivity [52], decreased activity and degradation of Rubisco due to chloroplast membrane damage [17,56,57], and reduction in chloroplasts [41] as the major causes of decreasing photosynthetic capacity in ozone-stressed plants. Such phenomena are accompanied by growth reduction in plants and are said to influence the aspects of anabolite distribution as well [55,58,59].
In contrast, Ref. [60] did not find a reduction in chlorophyll a when tobacco plants were exposed to 90 ppb ozone for 8 h/day. In Cucumis sativus, the chlorophyll a and total chlorophyll contents had no significant differences under 500 ppb for 3 h ozone exposure conditions [61]. In Pak-Choi, the β-carotene had no significant differences under 60 ppb with different exposure duration ozone treatments [62]. These results are similar to our research findings, where the photopigments had no significant differences in ozone stresses. The plant response to ozone depends on the development stage [19], nutritional status [63,64], and plant species [43,65]. Moreover, the plant response to oxidative damage is more sensitive in younger plant stages than in older plant growth stages [32,66]. Therefore, in our study, young plants were used with the expectation that they would be more sensitive to ozone. It might be that our treatments, even though the concentration was far above ambient concentrations, did not last long enough to trigger the degradation of photopigments or that responses to ozone stress differ by plant species.

4.3. Glucosinolate Profile Affected by Ozone Concentration Treatments

There is some research on the relationship between ozone and GLS. As of today, the changing GLS levels according to ozone cannot clearly be explained by a single factor but may be elucidated by coupling mainly to oxidative damage [65,67]. Ozone causes various oxidative interferences in cells, and the processing of ozone in the plant facilitates the oxidized burst and may induce a kind of reaction in plants similar to a pathogen infection response [15]. In addition, under elevated ozone levels, the GLS profile could be modulated by changes in salicylic acid (SA) and jasmonic acid (JA) contents via reactive oxygen species (ROS) within the cell disruption cycle, where this reaction functions as the defense signal of plants [6,15,25,67,68,69]. These signals in the Brassica plants induce specific GLS biosynthesis and emissions [70]. In Brassica napus faced with stress, the aromatic GLS was increased and the plant susceptibility to Pratylenchus neglectus decreased, thus significantly reducing nematodes [71]. Ref. [72] reported that Brassica napus showed the greatest increases in indole GLS after wounding, but aliphatic GLS was largely decreased. In addition, it seems that the environment has more considerable effects on the levels of indole GLS in comparison with aliphatic GLS [73], and these results are similar to our results. Thus, increasing physical damage was associated with increasing indole and aromatic GLS and decreasing aliphatic GLS contents. These phenomena are facilitated by the physical damage and the resulting accumulation of different bio-substances [72,74,75].
According to these results, in higher-ozone conditions, the total aliphatic GLS showed a diminishing trend in comparison with the control (Table 4). Similar effects have been noted in [28], where the GLS content showed a generally diminishing trend in ozone-treated rapeseed (176 ppb for 4 h) in comparison with the control group. In mustard, mostly decreasing GLS contents were reported due to elevated ozone [27]. However, reported observations demonstrate that GLS responses to ozone stress differ between species, and intraspecific variation exists within species [5,29,41]. In oilseed rape, 40 ppb ozone exposure condition was not enough to change the GLS profile significantly, but in broccoli, the same 40 ppb ozone significantly increased the aliphatic GLS profile [76]. However, in this study, the glucoerucin (aliphatic) in high-level ozone concentration exposure was increased significantly (Table 4). Ref. [77] reported that some GLSs could protect against physical damage. In mustard, an increase in isothiocyanates could be detected as a response to injury of the plant [77]. In this regard, results from many researchers show that some aliphatic GLS (isothiocyanates) are volatile; therefore, plants containing GLSs use them directly in their defense system [78,79].
In this study, it was shown that the total indole GLS increased as the ozone concentration increased, but the aromatic GLS showed a tendency to decrease after increasing with increasing ozone concentrations (Table 4). It has been hypothesized that the GLS reaction to ozone could be regulated by the activation status of organic acids in the oxidative cell disruption cycle and that both organic acids might be contributing to the GLS biosynthesis processes differently [15,29,74]. In oilseed, results from some reports indicate that directional aromatic GLS was increased during exogenous SA treatment [80,81]. In Arabidopsis, increasing aromatic GLS synthesis via genetic modification can enhance the SA-mediated defense system while also inhibiting the JA-mediated defense system [82]. On the other hand, In Arabidopsis, the amount of indole GLS was increased after treatment with methyl jasmonate, and in oilseeds, JA treatment caused an increase in indole GLS, but in both plants, other GLS types were relatively reduced [74,83,84]. The results of [85] indicated that SA and JA interact biochemically in GLS synthesis. According to advanced research results about interactions of GLS and organic acids, as well as our results, we can use the oxidative cell disruption cycle hypothesis [15,29] to explain the phenomenon. Due to this hypothesis, ozone stress can cause various reactions and responses among classes of GLS (indole and aromatic).

5. Conclusions

We have conducted research to study the growth and biochemical quality of Pak-Choi exposed to different ozone concentrations, similar to concentrations found in urban environments. There were no changes in growth variables in low-concentration ozone treatments, but leaf area and biomass were significantly decreased at a high ozone concentration of Pak-Choi. Lycopene and chlorophylls also showed the same results. The ozone concentration was only briefly elevated, but plant metabolisms were variously affected. This can be linked to cell destruction by plant ozonization and suggested as a direction for further studies on the mechanisms of ozone and plant interactions in increased ozone atmospheres in urban horticultural sites.

Author Contributions

Y.J.H. conceived the original screening and research plans and performed all of the experiments; W.B. assisted substantially with writing the manuscript; I.M. and N.F. provided technical assistance; C.U. conceived and supervised the research; Y.J.H. wrote and edited the manuscript with contributions of all the authors. All authors have read and agreed to the published version of the manuscript.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The authors wish to thank Amir Gharibeshghi, Frau Susanne Meier, and our colleagues at the Urban Plant Ecophysiology, HU-Berlin. The article processing charge was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)–491192747 and the Open Access Publication Fund of Humboldt-Universität zu Berlin.

Conflicts of Interest

The authors declare that they have no conflict of interest.

References

  1. Unger, N. Global climate forcing by criteria air pollutants. Annu. Rev. Environ. Resour. 2012, 37, 1–24. [Google Scholar] [CrossRef]
  2. Bastl, K.; Kmenta, M.; Berger, U.W. Defining pollen seasons: Background and recommendations. Curr. Allergy Asthma Rep. 2018, 18, 73. [Google Scholar] [CrossRef]
  3. Hazari, M.S.; Stratford, K.M.; Krantz, Q.T.; King, C.; Krug, J.; Farraj, A.K.; Gilmour, M.I. Comparative cardiopulmonary effects of particulate matter-and ozone-enhanced smog atmospheres in mice. Environ. Sci. Technol. 2018, 52, 3071–3080. [Google Scholar] [CrossRef]
  4. Pandey, A.K.; Ghosh, A.; Agrawal, M.; Agrawal, S. Effect of elevated ozone and varying levels of soil nitrogen in two wheat (Triticum aestivum L.) cultivars: Growth, gas-exchange, antioxidant status, grain yield and quality. Ecotoxicol. Environ. Saf. 2018, 158, 59–68. [Google Scholar] [CrossRef]
  5. Singh, A.A.; Fatima, A.; Mishra, A.K.; Chaudhary, N.; Mukherjee, A.; Agrawal, M.; Agrawal, S.B. Assessment of ozone toxicity among 14 Indian wheat cultivars under field conditions: Growth and productivity. Environ. Monit. Assess. 2018, 190, 1–14. [Google Scholar] [CrossRef]
  6. Oksanen, E.; Pandey, V.; Pandey, A.; Keski-Saari, S.; Kontunen-Soppela, S.; Sharma, C. Impacts of increasing ozone on Indian plants. Environ. Pollut. 2013, 177, 189–200. [Google Scholar] [CrossRef]
  7. Leisner, C.P.; Ainsworth, E.A. Quantifying the effects of ozone on plant reproductive growth and development. Glob. Chang. Biol. 2012, 18, 606–616. [Google Scholar] [CrossRef]
  8. Booker, F.; Muntifering, R.; McGrath, M.; Burkey, K.; Decoteau, D.; Fiscus, E.; Manning, W.; Krupa, S.; Chappelka, A.; Grantz, D. The ozone component of global change: Potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. J. Integr. Plant Biol. 2009, 51, 337–351. [Google Scholar] [CrossRef]
  9. Crutzen, P.J.; Lelieveld, J. Human impacts on atmospheric chemistry. Annu. Rev. Earth Planet. Sci. 2001, 29, 17–45. [Google Scholar] [CrossRef]
  10. Jenkin, M.E.; Clemitshaw, K.C. Ozone and other secondary photochemical pollutants: Chemical processes governing their formation in the planetary boundary layer. Atmos. Environ. 2000, 34, 2499–2527. [Google Scholar] [CrossRef]
  11. Kley, D.; Kleinmann, M.; Sanderman, H.; Krupa, S. Photochemical oxidants: State of the science. Environ. Pollut. 1999, 100, 19–42. [Google Scholar] [CrossRef]
  12. Stathopoulou, E.; Mihalakakou, G.; Santamouris, M.; Bagiorgas, H. On the impact of temperature on tropospheric ozone concentration levels in urban environments. J. Earth Syst. Sci. 2008, 117, 227–236. [Google Scholar] [CrossRef]
  13. Jeon, W.-B.; Lee, S.-H.; Lee, H.; Park, C.; Kim, D.-H.; Park, S.-Y. A study on high ozone formation mechanism associated with change of NOx/VOCs ratio at a rural area in the Korean Peninsula. Atmos. Environ. 2014, 89, 10–21. [Google Scholar] [CrossRef]
  14. Ashmore, M. Assessing the future global impacts of ozone on vegetation. Plant Cell Environ. 2005, 28, 949–964. [Google Scholar] [CrossRef]
  15. Kangasjärvi, J.; Jaspers, P.; Kollist, H. Signalling and cell death in ozone-exposed plants. Plant Cell Environ. 2005, 28, 1021–1036. [Google Scholar] [CrossRef]
  16. Buchanan-Wollaston, V.; Morris, K. Senescence and cell death in Brassica napus and Arabidopsis. Program. Cell Death Anim. Plants 2000, 52, 163–174. [Google Scholar]
  17. Pell, E.J.; Schlagnhaufer, C.D.; Arteca, R.N. Ozone-induced oxidative stress: Mechanisms of action and reaction. Physiol. Plant. 1997, 100, 264–273. [Google Scholar] [CrossRef]
  18. Han, Y.J.; Gharibeshghi, A.; Mewis, I.; Förster, N.; Beck, W.; Ulrichs, C. Plant responses to ozone: Effects of different ozone exposure durations on plant growth and biochemical quality of Brassica campestris L. ssp. chinensis. Sci. Hortic. 2020, 262, 108921. [Google Scholar] [CrossRef]
  19. Pääkkönen, E.; Günthardt-Goerg, M.; Holopainen, T. Responses of Leaf Processes in a Sensitive Birch (Betula pendula Roth.) Clone to Ozone Combined with Drought. Ann. Bot. 1998, 82, 49–59. [Google Scholar] [CrossRef]
  20. Heck, W.W.; Taylor, O.C.; Tingey, D.T. Assessment of Crop Loss from Air Pollutants; Elsevier Applied Science: London, UK; New York, NY, USA, 1988. [Google Scholar]
  21. Schenone, G.; Botteschi, G.; Fumagalli, I.; Montinaro, F. Effects of ambient air pollution in open-top chambers on bean (Phaseolus vulgaris L.) I. Effects on growth and yield. New Phytol. 1992, 122, 689–697. [Google Scholar] [CrossRef]
  22. Guo, J.; Zhang, Y.; Liu, W.; Zhao, J.; Yu, S.; Jia, H.; Zhang, C.; Li, Y. Incorporating in vitro bioaccessibility into human health risk assessment of heavy metals and metalloid (As) in soil and pak choi (Brassica chinensis L.) from greenhouse vegetable production fields in a megacity in Northwest China. Food Chem. 2022, 373, 131488. [Google Scholar] [CrossRef] [PubMed]
  23. Zhang, L.; Xiao, S.; Chen, Y.; Xu, H.; Li, Y.; Zhang, Y.; Luan, F. Ozone sensitivity of four Pakchoi cultivars with different leaf colors: Physiological and biochemical mechanisms. Photosynthetica 2017, 55, 478–490. [Google Scholar] [CrossRef]
  24. Podsędek, A. Natural antioxidants and antioxidant capacity of Brassica vegetables: A review. LWT-Food Sci. Technol. 2007, 40, 1–11. [Google Scholar] [CrossRef]
  25. Black, V.; Stewart, C.; Roberts, J.; Black, C. Ozone affects gas exchange, growth and reproductive development in Brassica campestris (Wisconsin Fast Plants). New Phytol. 2007, 176, 150–163. [Google Scholar] [CrossRef]
  26. De Bock, M.; de Beeck, M.O.; De Temmerman, L.; Guisez, Y.; Ceulemans, R.; Vandermeiren, K. Ozone dose–response relationships for spring oilseed rape and broccoli. Atmos. Environ. 2011, 45, 1759–1765. [Google Scholar] [CrossRef]
  27. Khaling, E.; Papazian, S.; Poelman, E.H.; Holopainen, J.K.; Albrectsen, B.R.; Blande, J.D. Ozone affects growth and development of Pieris brassicae on the wild host plant Brassica nigra. Environ. Pollut. 2015, 199, 119–129. [Google Scholar] [CrossRef] [PubMed]
  28. Gielen, B.; Vandermeiren, K.; Horemans, N.; D’haese, D.; Serneels, R.; Valcke, R. Chlorophyll a fluorescence imaging of ozone-stressed Brassica napus L. plants differing in glucosinolate concentrations. Plant Biol. 2006, 8, 698–705. [Google Scholar] [CrossRef] [PubMed]
  29. Himanen, S.J.; Nissinen, A.; Auriola, S.; Poppy, G.M.; Stewart, C.N.; Holopainen, J.K.; Nerg, A.-M. Constitutive and herbivore-inducible glucosinolate concentrations in oilseed rape (Brassica napus) leaves are not affected by Bt Cry1Ac insertion but change under elevated atmospheric CO2 and O3. Planta 2008, 227, 427–437. [Google Scholar] [CrossRef] [PubMed]
  30. Yamazaki, K. Hydroponics; Hakusa: Tokyo, Japan, 1978. [Google Scholar]
  31. Hörmann, V.; Brenske, K.-R.; Ulrichs, C. Assessment of filtration efficiency and physiological responses of selected plant species to indoor air pollutants (toluene and 2-ethylhexanol) under chamber conditions. Environ. Sci. Pollut. Res. 2018, 25, 447–458. [Google Scholar] [CrossRef]
  32. Martins, L.L.; Mourato, M.P.; Cardoso, A.I.; Pinto, A.P.; Mota, A.M.; de Lurdes, S.; Gonçalves, M.; de Varennes, A. Oxidative stress induced by cadmium in Nicotiana tabacum L.: Effects on growth parameters, oxidative damage and antioxidant responses in different plant parts. Acta Physiol. Plant. 2011, 33, 1375–1383. [Google Scholar] [CrossRef]
  33. Maas, E. Salt tolerance of plants. Appl. Agric. Res. 1986, 1, 12–25. [Google Scholar]
  34. AirNow. Air Quality Guide for Ozone. Available online: https://www.airnow.gov (accessed on 29 June 2016).
  35. World Health Organization. Air Quality Guidelines: Global Update 2005: Particulate Matter, Ozone, Nitrogen Dioxide, and Sulfur Dioxide; World Health Organization: Geneva, Switzerland, 2006; Available online: https://apps.who.int/iris/bitstream/handle/10665/69477/WHO_SDE_PHE_OEH_06.02_eng.pdf?sequence=1 (accessed on 17 June 2012).
  36. Goodwin, T.W.; Britton, G. Distribution and analysis of carotenoids. In Plant Pigment; Academic Press: London, UK, 1988; pp. 61–132. [Google Scholar]
  37. Mewis, I.; Appel, H.M.; Hom, A.; Raina, R.; Schultz, J.C. Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol. 2005, 138, 1149–1162. [Google Scholar] [CrossRef]
  38. SAS. Institute Inc. SAS/STAT 15.1 User’s Guide, SAS 9.4 and SAS Viya 3.4 Programming Documentation. Available online: https://documentation.sas.com/doc/en/pgmsascdc/9.4_3.4/statug/titlepage.htm (accessed on 30 March 2021).
  39. Menéndez, A.I.; Gundel, P.E.; Lores, L.M.; Martínez-Ghersa, M.A. Assessing the impacts of intra-and interspecific competition between Triticum aestivum and Trifolium repens on the species’ responses to ozone. Botany 2017, 95, 923–932. [Google Scholar] [CrossRef]
  40. Pääkkönen, E.; Paasisalo, S.; Holopainen, T.; Kärenlamp, L. Growth and stomatal responses of birch (Betula pendula Roth.) clones to ozone in open-air and chamber fumigations. New Phytol. 1993, 125, 615–623. [Google Scholar] [CrossRef]
  41. Feng, Z.; Pang, J.; Kobayashi, K.; Zhu, J.; Ort, D.R. Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open-air field conditions. Glob. Chang. Biol. 2011, 17, 580–591. [Google Scholar] [CrossRef]
  42. Ferdinand, J.; Fredericksen, T.; Kouterick, K.; Skelly, J. Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) seedlings. Environ. Pollut. 2000, 108, 297–302. [Google Scholar] [CrossRef]
  43. Saunier, A.; Blande, J.D. The effect of elevated ozone on floral chemistry of Brassicaceae species. Environ. Pollut. 2019, 255, 113257. [Google Scholar] [CrossRef]
  44. Wang, D.; Karnosky, D.F.; Bormann, F.H. Effects of ambient ozone on the productivity of Populus tremuloides Michx. grown under field conditions. Can. J. For. Res. 1986, 16, 47–55. [Google Scholar] [CrossRef]
  45. Ottosson, S.; Wallin, G.; Skärby, L.; Karlsson, P.-E.; Medin, E.-L.; Räntfors, M.; Pleijel, H.; Selldén, G. Four years of ozone exposure at high or low phosphorus reduced biomass in Norway spruce. Trees 2003, 17, 299–307. [Google Scholar] [CrossRef]
  46. Karlsson, P.; Medin, E.; Selldén, G.; Wallin, G.; Ottosson, S.; Pleijel, H.; Skärby, L. Impact of ozone and reduced water supply on the biomass accumulation of Norway spruce saplings. Environ. Pollut. 2002, 119, 237–244. [Google Scholar] [CrossRef]
  47. Roberts, H.R.; Dodd, I.C.; Hayes, F.; Ashworth, K. Chronic tropospheric ozone exposure reduces seed yield and quality in spring and winter oilseed rape. Agric. For. Meteorol. 2022, 316, 108859. [Google Scholar] [CrossRef]
  48. Skärby, L.; Troeng, E.; Boström, C.-Å. Ozone uptake and effects on transpiration, net photosynthesis, and dark respiration in Scots pine. For. Sci. 1987, 33, 801–808. [Google Scholar]
  49. Zhang, W.; Wang, G.; Liu, X.; Feng, Z. Effects of elevated O3 exposure on seed yield, N concentration and photosynthesis of nine soybean cultivars (Glycine max (L.) Merr.) in Northeast China. Plant Sci. 2014, 226, 172–181. [Google Scholar] [CrossRef] [PubMed]
  50. Reig-Armiñana, J.; Calatayud, V.; Cerveró, J.; Garcıa-Breijo, F.; Ibars, A.; Sanz, M. Effects of ozone on the foliar histology of the mastic plant (Pistacia lentiscus L.). Environ. Pollut. 2004, 132, 321–331. [Google Scholar] [CrossRef] [PubMed]
  51. Greitner, C.S.; Pell, E.J.; Winner, W.E. Analysis of aspen foliage exposed to multiple stresses: Ozone, nitrogen deficiency and drought. New Phytol. 1994, 127, 579–589. [Google Scholar] [CrossRef]
  52. Singh, P.; Agrawal, M.; Agrawal, S.B. Evaluation of physiological, growth and yield responses of a tropical oil crop (Brassica campestris L. var. Kranti) under ambient ozone pollution at varying NPK levels. Environ. Pollut. 2009, 157, 871–880. [Google Scholar] [CrossRef]
  53. Betzelberger, A.M.; Gillespie, K.M.; Mcgrath, J.M.; Koester, R.P.; Nelson, R.L.; Ainsworth, E.A. Effects of chronic elevated ozone concentration on antioxidant capacity, photosynthesis and seed yield of 10 soybean cultivars. Plant Cell Environ. 2010, 33, 1569–1581. [Google Scholar] [CrossRef]
  54. Burkey, K.O.; Carter Jr, T.E. Foliar resistance to ozone injury in the genetic base of US and Canadian soybean and prediction of resistance in descendent cultivars using coefficient of parentage. Field Crops Res. 2009, 111, 207–217. [Google Scholar] [CrossRef]
  55. Vandermeiren, K.; Black, C.; Pleijel, H.; De Temmerman, L. Impact of rising tropospheric ozone on potato: Effects on photosynthesis, growth, productivity and yield quality. Plant Cell Environ. 2005, 28, 982–996. [Google Scholar] [CrossRef]
  56. Rao, M.V.; Paliyath, G.; Ormrod, D. Differential response of photosynthetic pigments, rubisco activity and rubisco protein of Arabidopsis thaliana exposed to UVB and ozone. Photochem. Photobiol. 1995, 62, 727–735. [Google Scholar] [CrossRef]
  57. Eckardt, N.; Pell, E. O3-induced degradation of Rubisco protein and loss of Rubisco mRNA in relation to leaf age in Solanum tuberosum L. New Phytol. 1994, 127, 741–748. [Google Scholar] [CrossRef]
  58. Skärby, L.; Ro-Poulsen, H.; Wellburn, F.A.; Sheppard, L.J. Impacts of ozone on forests: A European perspective. New Phytol. 1998, 139, 109–122. [Google Scholar] [CrossRef]
  59. Coleman, M.; Dickson, R.; Isebrands, J.; Karnosky, D. Root growth and physiology of potted and field-grown trembling aspen exposed to tropospheric ozone. Tree Physiol. 1996, 16, 145–152. [Google Scholar] [CrossRef] [PubMed]
  60. Saitanis, C.; Riga-Karandinos, A.; Karandinos, M. Effects of ozone on chlorophyll and quantum yield of tobacco (Nicotiana tabacum L.) varieties. Chemosphere 2001, 42, 945–953. [Google Scholar] [CrossRef] [PubMed]
  61. Agrawal, M.; Krizek, D.T.; Agrawal, S.B.; Kramer, G.F.; Lee, E.H.; Mirecki, R.M.; Rowland, R.A. Influence of inverse day/night temperature on ozone sensitivity and selected morphological and physiological responses of cucumber. J. Am. Soc. Hortic. Sci. 1993, 118, 649–654. [Google Scholar] [CrossRef]
  62. Han, Y.J.; Gharibeshghi, A.; Mewis, I.; Förster, N.; Beck, W.; Ulrichs, C. Effect of different durations of moderate ozone exposure on secondary metabolites of Brassica campestris L. ssp. chinensis. J. Hortic. Sci. Biotechnol. 2021, 96, 110–120. [Google Scholar] [CrossRef]
  63. Landolt, W.; Günthardt-Goerg, M.; Pfenninger, I.; Einig, W.; Hampp, R.; Maurer, S.; Matyssek, R. Effect of fertilization on ozone-induced changes in the metabolism of birch (Betula pendula) leaves. New Phytol. 1997, 137, 389–397. [Google Scholar] [CrossRef]
  64. Maurer, S.; Matyssek, R.; GuÈnthardt-Goerg, M.S.; Landolt, W.; Einig, W. Nutrition and the ozone sensitivity of birch (Betula pendula). Trees 1997, 12, 1–10. [Google Scholar] [CrossRef]
  65. Singh, A.A.; Ghosh, A.; Agrawal, M.; Agrawal, S.B. Secondary metabolites responses of plants exposed to ozone: An update. Environ. Sci. Pollut. Res. 2023, 30, 88281–88312. [Google Scholar] [CrossRef]
  66. Thwe, A.A.; Vercambre, G.; Gautier, H.; Pagès, L.; Jourdan, C.; Gay, F.; Kasemsap, P. Dynamic shoot and root growth at different developmental stages of tomato (Solanum lycopersicum Mill.) under acute ozone stress. Sci. Hortic. 2013, 150, 317–325. [Google Scholar] [CrossRef]
  67. Lee, J.G.; Kwak, M.J.; Jeong, S.G.; Woo, S.Y. Indivisual and interactive effects of elevated ozone and temperature on plant responses. Horticulturae 2020, 8, 211. [Google Scholar] [CrossRef]
  68. Baier, M.; Kandlbinder, A.; Golldack, D.; Dietz, K.J. Oxidative stress and ozone: Perception, signalling and response. Plant Cell Environ. 2005, 28, 1012–1020. [Google Scholar] [CrossRef]
  69. Rao, M.V.; Davis, K.R. The physiology of ozone induced cell death. Planta 2001, 213, 682–690. [Google Scholar] [CrossRef] [PubMed]
  70. Hopkins, R.J.; Van Dam, N.M.; Loon, J.v. Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 2009, 54, 57–83. [Google Scholar] [CrossRef] [PubMed]
  71. Potter, M.; Vanstone, V.; Davies, K.; Kirkegaard, J.; Rathjen, A. Reduced susceptibility of Brassica napus to Pratylenchus neglectus in plants with elevated root levels of 2-phenylethyl glucosinolate. J. Nematol. 1999, 31, 291. [Google Scholar]
  72. Koritsas, V.; Lewis, J.; Fenwick, G. Glucosinolate responses of oilseed rape, mustard and kale to mechanical wounding and infestation by cabbage stem flea beetle (Psylliodes chrysocephala). Ann. Appl. Biol. 1991, 118, 209–221. [Google Scholar] [CrossRef]
  73. Verkerk, R.; Schreiner, M.; Krumbein, A.; Ciska, E.; Holst, B.; Rowland, I.; De Schrijver, R.; Hansen, M.; Gerhäuser, C.; Mithen, R. Glucosinolates in Brassica vegetables: The influence of the food supply chain on intake, bioavailability and human health. Mol. Nutr. Food Res. 2009, 53, S219. [Google Scholar] [CrossRef]
  74. Mikkelsen, M.D.; Petersen, B.L.; Glawischnig, E.; Jensen, A.B.; Andreasson, E.; Halkier, B.A. Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol. 2003, 131, 298–308. [Google Scholar] [CrossRef] [PubMed]
  75. Kliebenstein, D.J.; Kroymann, J.; Brown, P.; Figuth, A.; Pedersen, D.; Gershenzon, J.; Mitchell-Olds, T. Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 2001, 126, 811–825. [Google Scholar] [CrossRef]
  76. Vandermeiren, K.; De Bock, M.; Horemans, N.; Guisez, Y.; Ceulemans, R.; De Temmerman, L. Ozone effects on yield quality of spring oilseed rape and broccoli. Atmos. Environ. 2012, 47, 76–83. [Google Scholar] [CrossRef]
  77. Mithen, R.F. Glucosinolates and their degradation products. Advances in Botanical Research. 2001, 35, 213–232. [Google Scholar]
  78. Bradburne, R.P.; Mithen, R. Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica. Proc. R. Soc. London. Ser. B Biol. Sci. 2000, 267, 89–95. [Google Scholar] [CrossRef] [PubMed]
  79. Brown, P.D. Control of soil-borne plant pests using glucosinolate-containing plants. Adv. Agron. 1997, 61, 167–231. [Google Scholar]
  80. Cole, R. Abiotic induction of changes to glucosinolate profiles in Brassica species and increased resistance to the specialist aphid Brevicoryne brassicae. In Proceedings of the 9th International Symposium on Insect-Plant Relationships; Springer Netherlands: Dordrecht, The Netherlands, 1996; pp. 228–230. [Google Scholar]
  81. Kiddle, G.A.; Doughty, K.J.; Wallsgrove, R.M. Salicylic acid-induced accumulation of glucosinolates in oilseed rape (Brassica napus L.) leaves. J. Exp. Bot. 1994, 45, 1343–1346. [Google Scholar] [CrossRef]
  82. Brader, G.; Mikkelsen, M.D.; Halkier, B.A.; Tapio Palva, E. Altering glucosinolate profiles modulates disease resistance in plants. Plant J. 2006, 46, 758–767. [Google Scholar] [CrossRef]
  83. Loivamäki, M.; Holopainen, J.K.; Nerg, A.-M. Chemical changes induced by methyl jasmonate in oilseed rape grown in the laboratory and in the field. J. Agric. Food Chem. 2004, 52, 7607–7613. [Google Scholar] [CrossRef]
  84. Doughty, K.J.; Kiddle, G.A.; Pye, B.J.; Wallsgrove, R.M.; Pickett, J.A. Selective induction of glucosinolates in oilseed rape leaves by methyl jasmonate. Phytochemistry 1995, 38, 347–350. [Google Scholar] [CrossRef]
  85. Cipollini, D.; Enright, S.; Traw, M.; Bergelson, J. Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol. Ecol. 2004, 13, 1643–1653. [Google Scholar] [CrossRef]
Horticulturae 09 00966 g001
Figure 1. Effects of different ozone concentrations on growth variables of Brassica campestris L. ssp. chinensis. Data are presented for (a) leaf area, (b) number of leaves, and (c) dry matter. Con.: control. Bars represent mean ± SE values (n = 45). Significant differences between various ozone treatments are shown with different small letters (p ≤ 0.05) using Tukey’s HSD test.
Figure 1. Effects of different ozone concentrations on growth variables of Brassica campestris L. ssp. chinensis. Data are presented for (a) leaf area, (b) number of leaves, and (c) dry matter. Con.: control. Bars represent mean ± SE values (n = 45). Significant differences between various ozone treatments are shown with different small letters (p ≤ 0.05) using Tukey’s HSD test.
Horticulturae 09 00966 g001
Horticulturae 09 00966 g002
Figure 2. Effect of different ozone concentrations on photopigments of Brassica campestris L. ssp. Chinensis. Data are presented for (a) lutein, (b) total carotenoids, (c) β-carotene, (d) lycopene, and (e) chlorophyll a, b, and total chlorophyll (e). Chl.: chlorophyll; Con.: control; DW: dry weight. Bars represent mean values ± SE (n = 12). Significant differences between ozone concentrations are shown with different small letters (p ≤ 0.05) according to Tukey’s HSD test.
Figure 2. Effect of different ozone concentrations on photopigments of Brassica campestris L. ssp. Chinensis. Data are presented for (a) lutein, (b) total carotenoids, (c) β-carotene, (d) lycopene, and (e) chlorophyll a, b, and total chlorophyll (e). Chl.: chlorophyll; Con.: control; DW: dry weight. Bars represent mean values ± SE (n = 12). Significant differences between ozone concentrations are shown with different small letters (p ≤ 0.05) according to Tukey’s HSD test.
Horticulturae 09 00966 g002
Table 1. Formulas for determination of photopigment contents.
Table 1. Formulas for determination of photopigment contents.
Photopigment.Formula
Lutein(E445 × Volume)/Fresh weight (g)
Total carotenoids(E450 × Volume × 4)/Fresh weight (g)
β-carotene(E453 × Volume)/Fresh weight (g)
Lycopene(E505 × Volume)/Fresh weight (g)
Chlorophyll a{(10.1 × E663) − (10.1 × E645) × Volume}/Fresh weight (g)
Chlorophyll b{(16.4 × E645) − (2.57 × E663) × Volume}/Fresh weight (g)
Table 2. UHPLC conditions.
Table 2. UHPLC conditions.
ParameterOptimized Condition
Column2.7 µm, 2.1 × 100 mm, Agilent, USA
Oven temperature25 °C
Injection10 µL
Flow rate0.4 mL min−1
Gradient program0–2 min: 0–0.5% B
2–15 min: 0.5–100% B
15–16 min: 100% B
16–17 min: 100–0.5% B
17–21 min: 0.5% B
EluentsA: ultra-pure waterB: acetonitrile 100%
Table 3. Identified glucosinolates of Brassica campestris L. ssp. chinensis from UHPLC.
Table 3. Identified glucosinolates of Brassica campestris L. ssp. chinensis from UHPLC.
Molecular FormulaCompound IdentityCompound ClassRetention Time [min]
C11H19NO10S2Progoitrin (2-Hydroxy-3-Butenylglucosinolate)Aliphatic2.21
C11H19NO9S2Gluconapin (3-Butenylglucosinolate)Aliphatic6.89
C11H20NO9S3−Glucoibervirin (3-Methylthiopropylglucosinolate)Aliphatic7.82
C12H21NO10S2Gluconapoleiferin (2-Hydroxy-4-Pentenylglucosinolate)Aliphatic6.12
C12H21NO9S2Glucobrassicanapin (4-Pentenylglucosinolate)Aliphatic8.49
C12H22NO9S3−Glucoerucin (4-Methylthiobutylglucosinolate)Aliphatic8.79
C13H25NO10S3Glucoalyssin (5-Methylsulfinylpentylglucosinolate)Aliphatic6.38
C15H20NO9S2−Gluconasturtiin (2-Phenylethylglucosinolate)Aromatic10.20
C16H20N2O10S24-Hydroxyglucobrassicin (4-Hydroxy-3-Indolylmethylglucosinolate)Indole7.38
C16H20N2O9S2Glucobrassicin (3-Indolylmethylglucosinolate)Indole9.42
C17H22N2O10S24-Methoxyglucobrassicin (4-Methoxy-3-Indolylmethylglucosinolate)Indole10.30
C17H22N2O10S2Neoglucobrassicin (1-Methoxy-3-Indolylmethylglucosinolate)Indole11.76
Table 4. Effects of different ozone treatments (ppb) on GLS contents (µmol g−1 DW) of Brassica campestris L. ssp. chinensis.
Table 4. Effects of different ozone treatments (ppb) on GLS contents (µmol g−1 DW) of Brassica campestris L. ssp. chinensis.
Aliphatic GLS
2H3B2H4P5MGS3BGS3MGS4PGS4MGSTotal
Con.1.65 ± 0.01 a0.54 ± 0.05 a0.04 ± 0.00 a1.51 ± 0.05 a0.13 ± 0.01 a4.96 ± 0.10 a0.06 ± 0.01 c8.89 ± 0.19 a
601.28 ± 0.01 b0.41 ± 0.01 b0.04 ± 0.00 a1.15 ± 0.02 b0.14 ± 0.01 a3.75 ± 0.06 b0.19 ± 0.00 b6.94 ± 0.10 b
1501.11 ± 0.02 c0.32 ± 0.01 bc0.02 ± 0.00 c1.12 ± 0.02 b0.12 ± 0.00 a3.37 ± 0.05 c0.26 ± 0.01 a6.43 ± 0.11 b
2401.14 ± 0.01 c0.22 ± 0.00 c0.03 ± 0.00 b1.52 ± 0.01 a0.14 ± 0.00 a3.40 ± 0.02 c0.24 ± 0.00 a6.69 ± 0.03 b
Indole GLSAromatic GLS
4H3I3IGS4M3I1M3ITotal2PGS
Con.0.01 ± 0.00 a0.07 ± 0.00 c0.67 ± 0.04 b0.23 ± 0.03 a0.98 ± 0.07 b1.11 ± 0.01 d
600.03 ± 0.00 a0.06 ± 0.00 c0.56 ± 0.02 b0.20 ± 0.00 a0.84 ± 0.02 b1.53 ± 0.03 c
1500.01 ± 0.01 a0.11 ± 0.00 b0.64 ± 0.02 b0.25 ± 0.01 a1.02 ± 0.03 b2.22 ± 0.06 a
2400.01 ± 0.00 a0.23 ± 0.00 a1.27 ± 0.02 a0.20 ± 0.00 a1.71 ± 0.02 a1.96 ± 0.01 b
2H3B: 2-Hydroxy-3-Butenyl-GLS; 2H4P: 2-Hydroxy-4-Pentenyl-GLS; 5MGS: 5-Methylsulfinylpentyl-GLS; 3BGS: 3-Butenyl-GLS; 3MGS: 3-Methylthiopropyl-GLS; 4PGS: 4-Pentenyl-GLS; 4MGS: 4-Methylthiobutyl-GLS; 4H3I: 4-Hydroxy-3-Indolylmethyl-GLS; 3IGS: 3-Indolylmethyl-GLS; 4M3I: 4-Methoxy-3-Indolylmethy-GLS; 1M3I: 1-Methoxy-3-Indolymethyl-GLS; 2PGS: 2-Phenylethyl-GLS. Con.: control, DW: dry weight. Values represent mean ± SE (n = 12). Significant differences between different ozone treatments are indicated with different small letters (p ≤ 0.05) using Tukey’s HSD test.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Han, Y.J.; Beck, W.; Mewis, I.; Förster, N.; Ulrichs, C. Effect of Ozone Stresses on Growth and Secondary Plant Metabolism of Brassica campestris L. ssp. chinensis. Horticulturae 2023, 9, 966. https://doi.org/10.3390/horticulturae9090966

AMA Style

Han YJ, Beck W, Mewis I, Förster N, Ulrichs C. Effect of Ozone Stresses on Growth and Secondary Plant Metabolism of Brassica campestris L. ssp. chinensis. Horticulturae. 2023; 9(9):966. https://doi.org/10.3390/horticulturae9090966

Chicago/Turabian Style

Han, Young Jong, Winston Beck, Inga Mewis, Nadja Förster, and Christian Ulrichs. 2023. "Effect of Ozone Stresses on Growth and Secondary Plant Metabolism of Brassica campestris L. ssp. chinensis" Horticulturae 9, no. 9: 966. https://doi.org/10.3390/horticulturae9090966

APA Style

Han, Y. J., Beck, W., Mewis, I., Förster, N., & Ulrichs, C. (2023). Effect of Ozone Stresses on Growth and Secondary Plant Metabolism of Brassica campestris L. ssp. chinensis. Horticulturae, 9(9), 966. https://doi.org/10.3390/horticulturae9090966

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop