The effect of ozone and drought on the photosynthetic performance of canola

1. Introduction

In agriculture, crop growth, development and yields mainly depend on photosynthesis. Crop photosynthesis is limited by diverse environmental factors such as biotic and abiotic stresses (Munns et al. 2006; Chaves et al. 2009; Bilgin et al.2010), hence leading to reduced crop yields. Ozone (O3)is a secondary air pollutant and one of the abiotic stresses affecting agricultural crop production as it is highly reactive and reacts with a range of compounds associated with the cell wall and membranes (Roshchina 2003). Climate change studies indicate that the global background concentration of O3 has increased due to anthropogenic emission of its precursors (Porter et al. 2014). It has been shown that sensitive plant species show yield reduction when exposed to O3 concentrations above the threshold of 40 ppb (Christ et al. 2006). Ozone levels in southern Africa exceed air quality guidelines determined to protect agricultural crops(van Tienhoven et al. 2006). Laakso et al. (2013) concluded that crops may have adapted to elevated O3 levels in this region. However, they indicated that limited experimental studies exist on this issue to con firm whether local species may be tolerant to the high levels of O3.

Elevated O3 reduces photosynthetic efficiency and other physiological functions such as stomatal conductance and leaf area, which in turn negatively impact final yield (Gornall et al. 2010; Mills and Harmens 2011; Porter et al. 2014).Therefore, O3 effects on agricultural crops may become a major issue of concern in the future. The potential effect of O3 on agriculture has received much attention in developed countries but this issue has received little attention in the developing countries. As a consequence, findings of the northern hemisphere countries have been extrapolated in southern Africa, but given the differences in atmospheric and weather conditions these findings may not represent the local conditions. It is important to understand more detail O3 effects on crops under local conditions as well as to evaluate ways by which the agricultural sector can adapt to improve food security.

全国后备力量调整改革以来，民兵网军的编成与力量结构基本建立，初步形成了集网络攻防、信息保障、电磁频谱管理、舆情管控为一体的网军队伍。近年来，这些力量先后参加了G20安保、互联网大会、部队战役演习、抢险救灾等大项活动的信息通信保障和网络安防任务，展现了精湛的业务能力和过硬的战斗作风。但是民兵网军这支新质力量不同于应急维稳、抢险救灾等传统类型的民兵队伍，其人员编组、组训模式、战法运用等诸多方面都有其特殊性，反观当前省军区系统民兵网军队伍的建设与运用现状，距实战化的要求和走在前列的标准还有很大差距，概括起来主要反映在以下6个方面。

It has been found that the fast kinetics of OJIP, exhibited by all oxygenic photosynthetic plants upon illumination that follows dark-adaptation, is sensitive to stress caused by changes in different environmental conditions and can reflect the physiological status and response of plants under various stresses (van Heerden et al. 2003; Öz et al.2014). The JIP-test is an analysis of OJIP that quanti fies the in vivo vitality of photosystem II (PS II) and evaluates plant photosynthetic performance (Strasser et al. 2007; Öz et al.2014). The Chl a fluorescence transient and its analysis by the JIP-test was used here to evaluate the changes in growth and photosynthetic performance of canola.

Canola is a relatively new crop in South Africa and one of the major oilseed crops in the world. The production of oilseed rape will increase owing to the production of biofuel. According to the results of Zhu et al. (2016),canola is sensitive to drought during all stages of growth.The individual and combined effects of O3 and drought exposure can be influenced by a number of other factors such as O3 flux and antioxidant capacity, sensitivity to O3 and drought, time of day and vegetative season (Bohler et al. 2015). In the present study, particular parameters of Chl a fluorescence were used to determine the sensitivity of canola to elevated O3 and drought and combinations of them on the photosynthetic performance. The objectives were:(1) to expose canola plants performance to O3 (120 ppb)under well-watered (WW-O3) and water-stressed (WS-O3)conditions in open-top chambers (OTCs); (2) to quantify the biophysical and physiological responses to O3 in both cases.

2. Materials and methods

2.1. Plant materials and growth conditions

The experiment was conducted in OTCs located at the North-West University, Potchefstroom campus, South Africa(26°40´50´´S, 27°05´48´´E, 1 348 m above sea level). The design and operation of the specific OTC system used has previously been reported (Heyneke et al. 2012). Seedlings were grown under a 14-h/10-h day/night cycle with natural light conditions. The temperature and humidity inside the OTCs was monitored using a RHT03 humidity and temperature sensor with a single wire digital interface. It provides a voltage output that is linearly proportional to the Celsius temperature and relative humidity (RH).

The canola (Brassica napus L. cv. Rainbow) seeds were hand sown in 30-cm diameter pots and watered manually before the onset of O3 fumigation and water stress treatment to ensure that seeds germinate and grow healthy without any environmental stress. The growth medium used was a mixture of topsoil, river sand and vermiculite (2:1:1, v/v).A total of 25 g six-month slow release fertilizer, containing 17 nitrogen:11 phosphorus:10 potassium:2 magnesium oxide:TE (Osmocote® Pro, the Netherlands), was added to each pot.

2.2. Ozone fumigation

Fumigation of plants was started after 5 weeks of sowing with 120 ppb of O3 from 8:00 to 17:00 every day. Ozone levels inside the OTCs were continuously monitored at regular intervals by O3 monitor (Model 205 Ozone Monitor,2B Technologies Inc., USA) throughout the fumigation period.

Taking in consideration that the PItotal is a very sensitive parameter, our results revealed that PItotal in leaves changes over time. Since the photosynthetic process is affected by various environmental factors such as water stress and O3, it was expected that PItotal in the well-watered and nonfumigated plants will increase as the experiment continues over the weeks. However, it showed a downward trend over time in all treatments but in fumigated and well watered plants the decline was stronger. In Oxford clone experiment conducted in open-top chambers, Desotgiu et al. (2012) indicated that the PItotal in leaves changes over time according to development stage and ageing process. The PItotal decreased over time due to ageing but O3 fumigation enhanced this downward trend under well-watered conditions.

2.3. Water treatment

The plants inside each OTCs were subjected to two water regimes, WW and WS conditions by means of a unique irrigation system (Mills et al. 2005). The plants were receiving water via the glass fibre wicks that were projected into the water reservoirs. Wicks were cut at specific lengths(90 or 60 cm with a diameter of about 7 mm) and layered clockwise in a partial circle close to the perimeter of the pot.In the water-stressed treatment one glass fiber wick (90-cm)was placed at the mid-level of each pot, whereas in the wellwatered pots four wicks (two 90-cm and two 60-cm wicks)were placed at four levels within the pots to ensure suf ficient supply of water from the reservoir to the growth medium.Pots were placed into reservoirs which were connected to a drip irrigation system that re fill the water. The irrigation system was applied when the O3 fumigation was initiated on some plants (after 5 weeks of sowing), i.e., treatments of WW-O3 and WS-O3, while the potted plants without O3 fumigation were WW and WS treatments, respectively. The plants were irrigated on alternate days from the start to the end of the experiment.

2.4. Chlorophyll a fluorescence

The photosynthetic efficiency was investigated by means of Chl a fluorescence. The Chl a fluorescence transients were measured with a Handy PEA fluorimeter (Hansatech Instruments Ltd., UK) on dark adapted leaves. The leaves were dark-adapted for 1 h before measurements, to ensure that the primary quinone electron acceptor of PSII (QA) is fully oxidised, i.e., all the photosynthetic reaction centres are open. The transients in leaves were induced by red light(peak at 650 nm) of 3 000 μmol photons m−2 s−1 provided by an array of three light-emitting diodes, and recorded for 1 s with 12 bit resolution. The data acquisition was at every 10 μs (from 10 μs to 0.3 ms), every 0.1 ms (from 0.3 to 3 ms),every 1 ms (from 3 to 30 ms), every 10 ms (from 30 to 300 ms) and every 100 ms (from 300 ms to 1 s) (Strasser et al.2004; Tsimilli-Michael and Strasser 2013). The first reliable data are considered to be at 10 μs.

Data were analysed with Statistica 12 Software (Statsoft,Inc., US). Histograms and normal probability plot were used to test normal distribution of the data. In data sets with parametric distribution, significance differences between treatment means were determined using the Tukey’s Honest significant differences (HSD) in one-way analysis of variance(ANOVA). In data sets with non-parametric distribution,significant differences between treatment means were determined with Kruskal-Wallis test and the Dunn’s test for post-hoc comparisons.

Chl a fluorescence was measured after 1, 2, 3 and 4 weeks of O3 fumigation. Three plants in each chamber were selected for the readings in both well-watered and water-stressed treatments. Measurements were taken at five positions on each leaf, four leaves were assessed in each plant and 6 plants (three WW and three WS plants)were assessed in each chamber, giving 120 readings in each chamber (in total 120 readings×4 chambers). The data were transferred to a computer and all analyses were performed using the PEA Plus ver. 1.10 Program (Hansatech Instruments Ltd., UK). OJIP were analysed according to the JIP-test formulae (Strasser et al. 2004; Tsimilli-Michael and Strasser 2013) (Appendix A). The shape of the OJIP transient and its analysis by the JIP-test are efficient biophysical tools in the biophysical phenotyping of the photosynthetic apparatus of a plant under any stress (Strasser et al. 2007).

2.5. Stomatal conductance

Stomatal conductance was measured every week after the onset of fumigation on intact leaves with a porometer(Model AP4, Delta-T Devices, Cambridge, UK) between 9:00 and 14:00.

2.6. Statistical analysis

这两个问题是引导学生对文本人物进行评价的两种不同的提问方式，促进学生与文本进行深层次的对话。这些问题涉及学生的批判性思维，学生通过对文本的理解和判断，与文本进行思想交流。

3. Results

The average Chl a fluorescence transient for the four treatments (WW, WW-O3, WS, WS-O3) were plotted on logarithmic time scale (Fig. 1-A-D), expressed as Ft/F0 for clarity. We note that this normalisation was permitted since the differences of F0 values among treatments and over time were very minor and statistically not significant. In order to quantify and evaluate the differences between the transients,the JIP-test was applied for their analysis.

Fig. 2-A-F shows the performance indexes PItotal and PIABS and the parameters used for their de finition(Appendix A), i.e., the maximum quantum yield for primary photochemistry (φPo), the efficiency (ΨEo) with which a trapped exciton can move an electron into the electron transport chain further than QA–, the probability to reduce the end electron acceptors (δRo) and the reaction centre (RC)density on a chlorophyll basis (RC/ABS).

Under WW, PItotal was found to decrease over time in non-fumigated plants (Fig. 2-A), which can be attributed to physiological and biochemical changes within the plant because of leaf ageing. The decline in WW and fumigated plants was more pronounced. The average values of PItotal for the whole course of the experiment were by about 27%lower in WW-O3 than in WW. In water-stressed plants without and with fumigation (WS and WS-O3), PItotal increased from week 1 to 2 and then decreased until week 4 (Fig. 2-A). The difference between WS and WS-O3 of the average values of PItotal for the whole course (decrease of WS-O3 by about 3%) was statistically insignificant. These findings reveal that O3 affects well-watered but not water-stressed plants.

Fig. 1 Average chlorophyll a fluorescence transient of dark adapted canola leaves from non-fumigated and fumigated plants under well-watered (WW) and water-stressed (WS) conditions. A-D, week 1-4. The transients are plotted on a logarithmic time scale from 20 μs to 1 s and the steps O (at 20 μs), J (at 2 ms), I (at 30 ms), and P (at ≈300 ms) are labelled.

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Comparison of PItotal between WW and WS treatments revealed higher values in WW after week 1 and 3. There was no statistically significant difference between WW and WS in week 2 and 4; however, on average the PItotal was higher in WW treatment. The comparison between WW-O3 and WS-O3 showed higher PItotal values in WS-O3 per week,from week 2 to 4. In general, taking the average of all weeks,WW had the highest PItotal and the lowest WW-O3 (decrease by 27%), while in WS and WS-O3, it was lower than WW,14 and 17% decrease respectively.

Higher differences between O3-treated and control plants in the maximum yield of primary photochemistry of PS II(φPo=TR0/ABS) at predawn (dark conditions) was observed by Desotgiu et al. (2013). In contrast, minor differences in the maximum yield of primary photochemistry of PS II were observed in our present study, showing that φPo is the less sensitive parameter to the effect of O3 and drought. Similar findings have been also reported under dark chilling, drought and O3 (Strauss et al. 2006; Oukarroum et al. 2007; Bussotti et al. 2011). In well-watered plants, the δRo decreased in fumigated plants, causing a significant reduction of PItotal.The reduction in density of PSI and the compromised ability of the end acceptors of electrons (ferredoxine, NADP+)and RuBP to manage effectively the flux of electrons may cause an imbalance between the electrons sent through the electron transport chain to recipients which are beyond the PSI (Bussotti et al. 2011).

Ozone was found to increase the values of absorption(ABS)/RC over time under well-watered conditions(Fig. 3-A). The changes of ABS/RC are the inverse of the changes of RC/ABS values. The ABS/RC exhibit changes closely followed by changes of trapping (TR0)/RC (Fig. 3),as expected since φPo=TR0/ABS is almost insensitive. This indicates that ABS/RC stands for functional antenna size and not apparent antenna size (Strasser et al. 2004).

这话说起来轻巧，做起来确实有难度。这是一个手脑并用的过程：从动脑开始，想出一个可行的行动方案，然后动手引导宝宝去做。请注意我这里没用上“教”这个字。你教，宝宝没有体验，就没有感受，路摆在他面前，他也走不下去。

The drought stress affected stomatal conductance (WW vs. WS), which showed a decline in water stress plants by 44% than well-watered plants (Fig. 4). In addition, the mean values of well-watered and fumigated plants (WW-O3) were higher as compared to water-stressed and fumigated plants(WS-O3) (28% difference) (Fig. 4).

4. Discussion

Chl a fluorescence transient data were analysed by the JIP-test to quantify the PS II behaviour of canola leaves.The effect of elevated O3 on PS II activity was quantified by the values for PItotal and PIABS. PItotal is a combination of the following parameters: φPo, ΨEo, δRo and RC/ABS.PIABS combines three parameters: RC/ABS, φPo and ΨEo.Comparing the sensitivity of the PIABS and PItotal to O3 and drought, we found that PIABS as a measure of plant performance is less sensitive than the PItotal, since the δRo(the probability to reduce an end electron acceptor) is not contributing to it. In a review, Bussotti et al. (2011) compared the two performance indexes (PIABS and PItotal) and showed that in most cases PItotal is affected by O3 treatment more than PIABS.

Fig. 2 Performance indexes (A, PItotal; B, PIABS) and reaction centre (RC) density on a chlorophyll basis (RC/ABS) (C), the maximum quantum yield of primary photochemistry (φPo) (D), the efficiency (ΨEo) with which a trapped exciton can move an electron into the electron transport chain further than QA– (E), and the probability to reduce the end electron acceptors (δRo ) (F) of non-fumigated and fumigated plants with O3 under well-watered (WW, WW-O3 ) and water-stressed (WS, WS-O3) conditions. Each bar represents the mean value, and vertical error bar is SE and denotes 0.95 Confidence level. Capital letters indicate significant differences(P＜0.05) between treatments for the same week, whereas small letters indicate significant differences over time for each treatment(P＜0.05). W1-4, week 1-4.

制作一个收集气液用的收集筒，为便携式检测仪提供了一个半密闭的检测空间，该收集筒能有效防止被检测气体受周围环境气候影响，保持原有的浓度。检测时能隔离有害气体与操作员工的接触，检测过程中排放的气液不会散落在地面造成环境污染。这种检测方法能连续监测，同时提高检测的准确度，降低操作时的风险，减小环境污染。

Fig. 3 specific energy fluxes per reaction centre (RC) for non-fumigated and fumigated treatments under well-watered (WW,WW-O3) and water-stressed (WS, WS-O3) conditions: absorption flux (ABS/RC, A), trapping flux (TR0/RC, B), electron transport flux (ET0/RC, C), and electron flux for reducing end electron acceptors at PSI acceptor side (RE0/RC, D). Each bar represents the mean value, and vertical error bar is SE and denotes 0.95 Confidence level. Capital letters indicate significant differences(P＜0.05) between treatments for the same week, whereas small letters indicate significant differences over time for each treatment(P＜0.05). W1-4, week 1-4.

Fig. 4 Stomatal conductance of canola leaves from nonfumigated and fumigated plants under well-watered (WW,WW-O3) and water-stressed (WS, WS-O3) conditions. Each bar represents the mean value±SE (average of all weeks).

Concerning the parameters constructing PItotal, the maximum quantum yield for primary photochemistry (φPo)(Fig. 2-D) and the efficiency (ΨEo) (Fig. 2-E) were found to undergo only minor changes upon treatments and over time.Though the changes of ΨEo are slightly bigger than those of φPo, they are both much smaller than the changes of PItotal.The δRo showed the widest changes (Fig. 2-F), followed by RC density on a chlorophyll basis (RC/ABS) (Fig. 2-C),particularly in the well-watered treatments. PIABS (Fig. 2-B)is less sensitive than the PItotal since δRo is not contributing in its calculation (Appendix A).

世界各国对于税收优惠的主要三种方式有：税率式优惠、税基式优惠、税额式优惠，以上三种税收优惠政策不仅在影响范围有大小之分，影响深远度也有远近之分。由于发达国家税收优惠政策更加丰富，因此小微企业可选择的税收优惠政策更加多元化，同时也可以选择多种税收优惠政策将其自由组合，增加了小微企业对于税收优惠的自主选择性，对于促进小微企业快速发展十分有利。我国税收优惠政策以税率式优惠与税额式优惠作为重点，尚没有针对融资等方面的税收优惠政策，相较于发达国家的税收优惠政策则略显单一，对于小微企业税收优惠起到的作用不大，很难进一步提高小微企业的自主创新及其核心竞争力，难以维持这些企业的持续发展。

ABS/RC is a measure of the average absorption per active RC and concomitantly of the average amount of absorbing chlorophylls per active RC, i.e. of the apparent antenna size (Strasser et al. 2004). In addition, the changes of ABS/RC are the inverse of the changes of RC/ABS values. An increase of ABS/RC values means that a fraction of RCs is inactivated or the functional antenna has increased in size (Yusuf et al. 2010). However, we here found that ABS/RC increases whereas φPo undergoes slight changes and the TR0/RC closely follows the increase in ABS/RC.This indicates that the changes of ABS/RC are changes of functional antenna size, meaning that the functional antenna size was affected by O3 and drought.

We note that the probability to reduce an end electron acceptor (δRo=RE0/ET0) as well the RC density on a chl basis (RC/ABS) is sensitive to O3 even under waterstressed conditions, though much less than in wellwatered. Therefore, the more sensitive components of the photosynthetic electron transport chain appeared to have been the probability to reduce an end electron acceptor(δRo=RE0/ET0) as well the RC density on a chlorophyll basis (RC/ABS) under well-watered conditions, particularly in fumigated plants. The probability to move an electron beyond QA– (ΨEo=ET0/TR0) and the maximum quantum yield of primary photochemistry (φPo=TR0/ABS) were less affected. Pollastrini et al. (2013) reported that drought had more effect than O3 stress in reducing growth and carbon allocation in plant organs and in driving acclimation processes. In the current study, the effect of O3 was slight under drought conditions and this is related with the results on stomatal conductance which showed that it decreases in water-stressed plants compared to well-watered plants.

5. Conclusion

Based on the analysis of Chl a fluorescence in OTCs conditions, the effect of O3 was slight upon drought stress.Ozone caused an increase in the functional antenna size and a more pronounced decrease in the probability to reduce the end electron acceptors (δRo=RE0/ET0). Ozone and drought had negligible effect on the maximum quantum yield of primary photochemistry (φPo=TR0/ABS) and only slight effect on the probability of an electron to move beyond QA– (ΨEo=ET0/TR0). This study also supports the significance of the multiple turn-over region of the fluorescence transient (as revealed by the related parameter δRo=RE0/ET0) in the response of plants to O3 and drought stress. It can be concluded that O3 and drought stress altered the fluorescence induction and impaired photosynthetic systems in canola plants. The JIP-test is a good indicator to detect fluorescence induction and photosynthetic activity of the PS II RC complex of O3-treated canola plants. Considering the importance of this crop, the current findings do suggest that elevated O3 levels will have an effect on the production of oilseeds which will in turn impact the local economy.It is important to acknowledge that this effect could be cultivar dependent as a result it will be vital to gain a greater understanding of the canola cultivars responses to O3 in order to better predict crops response to changing atmospheric environment.

北京绿林认证有限公司是中国林产工业协会授权的首批第二方认定机构，已全面开展了无醛人造板及其制品的认定工作。在无醛认定基础上，北京绿林认证有限公司结合无醛人造板及其制品认定规则及人造板行业的实际情况，制定了无醛人造板及其制品的追溯体系，并开发了北京绿林认证有限公司专有的溯源平台。

Acknowledgements

This research was supported by the Cuomo Foundation through the partnership with the Intergovernmental Panel on Climate Change (IPCC) Scholarship Programme and by the Applied Centre for Climate and Earth Systems Science (ACCESS), South Africa. We are thankful to Dr.Merope Tsimilli-Michael (Cyprus) for her helpful explanations concerning the concepts and application of the JIP-test.Prof. Suria Ellis (North-West University, South Africa) for her assistance with the statistical analysis.

Appendix associated with this paper can be available on http://www.ChinaAgriSci.com/V2/En/appendix.htm

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