JXB Advance Access originally published online on February 29, 2008
Journal of Experimental Botany 2008 59(4):951-963; doi:10.1093/jxb/ern022
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© 2008 The Author(s).
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RESEARCH PAPER |
Assessing the genetic relatedness of higher ozone sensitivity of modern wheat to its wild and cultivated progenitors/relatives
1State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, The Chinese Academy of Sciences, 20 Nanxincun, 100093 Beijing, PR China
2School of Crop Sciences, Shandong Agricultural University, No. 61, Daizong Avenue, 271018 Tai'an, PR China
3State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, The Chinese Academy of Sciences, 100101Beijing, PR China
* To whom correspondence should be addressed. E-mail: liyonggeng{at}ibcas.ac.cn; jianggm{at}126.com
Received 20 September 2007; Revised 30 November 2007 Accepted 16 January 2008
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Abstract |
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Modern wheat (Triticum aestivum L.) is one of the most ozone (O3)-sensitive crops. However, little is known about its genetic background of O3 sensitivity, which is fundamental for breeding O3-resistant cultivars. Wild and cultivated species of winter wheat including donors of the A, B and D genomes of T. aestivum were exposed to 100 ppb O3 or charcoal-filtered air in open top chambers for 21 d. Responses to O3 were assessed by visible O3 injury, gas exchange, chlorophyll fluorescence, relative growth rate, and biomass accumulation. Ozone significantly decreased light-saturated net photosynthetic rate (–37%) and instantaneous transpiration efficiency (–42%), but increased stomatal conductance (+11%) and intercellular CO2 concentration (+11%). Elevated O3 depressed ground fluorescence (–8%), maximum fluorescence (–26%), variable fluorescence (–31%), and maximum photochemical efficiency (–7%). Ozone also decreased relative growth rate and the allometric coefficient, which finally reduced total biomass accumulation (–54%), but to a greater extent in roots (–77%) than in the shoot (–44%). Winter wheat exhibited significant interspecies variation in the impacts of elevated O3 on photosynthesis and growth. Primitive cultivated wheat demonstrated the highest relative O3 tolerance followed by modern wheat and wild wheat showed the lowest. Among the genome donors of modern wheat, Aegilops tauschii (DD) behaved as the most O3-sensitive followed by T. monococcum (AA) and Triticum turgidum ssp. durum (AABB) appeared to be the most O3-tolerant. It was concluded that the higher O3 sensitivity of modern wheat was attributed to the increased O3 sensitivity of Aegilops tauschii (DD), but not to Triticum turgidum ssp. durum (AABB) during speciation.
Key words: Biomass, Chl a fluorescence, genome, ozone sensitivity, relative growth rate, stomatal conductance, winter wheat
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Introduction |
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Modern hexaploid wheat (Triticum aestivum L.) is recognized as one of the most ozone (O3)-sensitive crops (Heck et al., 1984; Soja and Soja, 1995a; Sellden and Pleijel, 1995; Farage and Long, 1999; Emberson et al., 2003; Wang et al., 2007a). There are also large variations in O3 sensitivity between cultivars of wheat (Barnes et al., 1990; Heagle et al., 2000; Biswas et al., 2008). It has been documented that more recent cultivars of spring wheat are more sensitive to O3 than older ones despite rising atmospheric O3 concentrations (Barnes et al., 1990; Velissariou et al., 1992; Pleijel et al., 2006). In a previous experiment (Biswas et al., 2008), it was found that higher O3 sensitivity in the more recent winter wheat cultivars was induced by higher O3 flux, larger reduction in anti-oxidative capacity, and lower levels of dark respiration, leading to higher oxidative damage to proteins and integrity of cellular membranes. Since O3 tolerance is a heritable trait (Damicone and Manning, 1987; Barnes et al., 1999; Reinert and Eason, 2000; Fiscus et al., 2005), knowledge on O3 sensitivity of donors of the A, B and D genomes of modern wheat may be critical for the genetic aspects of increased O3 sensitivity, as well as for breeding cultivars through chromosome-mediated gene transfer. Although effects of the A, B and D genomes of wheat on photosynthesis (Planchon and Fesquet, 1982; Haour-Lurton and Planchon, 1985) and its relation to abiotic stress tolerance (i.e. salt, cold, drought) have been well investigated (Limin et al., 1997; Shah et al., 1997; Chandrasekar et al., 2000; Colmer et al., 2006), there has been no study on the impacts of wheat genomes on O3 tolerance.
The genome of an organism comprises a set of chromosomes, containing all of its genes and associated DNA. The wheat group (the genera Aegilops and Triticum) constitutes an alloploidy series containing diploid, tetraploid, and hexploid species with a basic chromosome set of x=7 (Belay et al., 1994). For instance, T. aestivum is hexaploid wheat which contains three diploid genomes (2n=6x=42, AABBDD). One predecessor of modern wheat is tetraploid durum wheat, T. turgidum ssp. durum with two diploid genomes (2n=4x=28, AABB) (Zohary and Hopf, 2000; Singh, 2005). The A genome shares a high degree of homology with the diploid genomes of T. urartu (AA), a species closely related to einkorn wheat, T. monococcum (AA), which was domesticated around 12 000 years ago (Zohary and Hopf, 2000; Singh, 2005). The origin of the B genome is still a matter of debate in the present literature (Levy and Feldman, 2004). It has been reported that the B genome might be derived from Aegilops speltoides, although its donor has still not been definitively identified (Levy and Feldman, 2004; Rudnoy et al., 2004). However, the hexaploid wheat, T. aestivum (AABBDD) is believed to have originated by hybridization between the early domesticated tetraploid durum wheat, T. turgidum ssp. durum (AABB) as a cytoplasm donor and the wild diploid wheat, A. tauschii (2n=2x=14, DD) as a donor of the D genome about 8000 years ago (Feldman, 2001; Matsuoka and Nasuda, 2004).
Plant sensitivity to O3 is typically assessed by the decline in growth and/or by visible symptoms, although it has often been reported that there is only a weak correlation between visible injury and growth (Reiling and Davison, 1992; Soja and Soja, 1995b). However, relative growth rate and allometric coefficient, i.e. the ratio between mean relative growth rate of root to shoot can provide a simple integration of the effects of O3 stress (Reiling and Davison, 1992; Andersen, 2003). It has also been reported that O3 sensitivity of spring wheat as determined by relative growth rate at the vegetative stage is proportional to O3-induced yield reduction (Pleijel et al., 2006). Gas exchange and chlorophyll fluorescence, on the other hand, offer a useful and non-destructive tool for in vivo stress detection (Owens, 1994; Maxwell and Johnson, 2000) and the mechanisms involved in O3-induced growth reduction (Guidi et al., 1997; Cardoso-Vilhena et al., 2004).
Despite the fact that O3 tolerance is a heritable trait (Damicone and Manning, 1987; Barnes et al., 1999; Fiscus et al., 2005) and the fact that genotypic variation in O3 sensitivity exists in wheat, with increased O3 sensitivity of recent cultivars compared with older ones (Barnes et al., 1990; Velissariou et al., 1992; Pleijel et al., 2006), little attention has been paid to the genetic variations in O3 sensitivity of their donor species. Besides, wild and primitive cultivated species are commonly used as crossing materials with immediate progenitors of wheat (Valkoun, 2001) to introduce economically useful genes as well as to enhance genetic diversity of wheat (Kawahara, 2002; Xiong et al., 2006). Determination of O3 sensitivity of wild and cultivated progenitors of modern wheat is especially critical to quantify the magnitude of genetic control of O3 tolerance and its further exploitation. Therefore, O3 sensitivity of wild and cultivated winter wheat species including donors of the A, B and D genomes of modern wheat were examined in terms of visible symptoms, growth, gas exchange, and fluorescence parameters. It was hypothesized that increased O3 sensitivity of modern wheat might be related to its wild and cultivated progenitors/relatives. Our findings may provide sufficient genetic basis of the increased O3 sensitivity of modern wheat, which is fundamental for breeding O3-resistant wheat cultivars.
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Materials and methods |
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Plant establishment and O3 fumigation
Twelve wild and cultivated species/cultivars including donors of the A, B and D genomes of modern wheat belonging to diploid (AA and DD), tetraploid (AABB and AAGG), and hexaploid (AABBDD) wheat were evaluated for O3 tolerance (Table 1). Seeds of selected winter wheat species/cultivars were obtained from the School of Crop Sciences, Shandong Agricultural University, Tai'an, PR China. On 2 March 2006, three germinated seeds were sown in each of 60 plastic pots (6 cm in diameter, 9 cm in height) per genotype in a temperature-controlled double-glazed greenhouse. Pots were filled with field clay loam soil containing organic C, total N, total P, and total K at the rate of 1.24%, 0.045%, 296 mg kg–1 and 14.7 g kg–1, respectively. No chemical fertilizer was applied either as basal or topdressing. Seedlings were thinned to one per pot on the seventh day after planting (DAP). On 8 DAP, 15 pots per genotype were moved to each of four open-top chambers (OTC, 1.2 m in diameter, 1.6 m in height) placed in the same greenhouse. The OTCs were ventilated continuously (24 h d–1) with air passing through activated charcoal filters attached to fan boxes. All seedlings were allowed to grow till 14 DAP to adapt to chamber environments before O3 exposure. During this adaptation period, all plants received charcoal-filtered air with an O3 concentration of less than 5 ppb. The gas-dispensing system of the OTCs was constructed following the methodology described by Uprety (1998). The chambers were illuminated by natural daylight supplemented by fluorescence light (360 W) providing a photosynthetic photon flux density (PPFD) of approximately 260 µmol m–2 s–1 at plant canopy height, yielding a 14 h photoperiod. The maximum PPFD in the chambers was approximately 690 µmol m–2 s–1. The temperature in the OTCs was 16/28 °C night/day and relative humidity was 65–90% during the experimental period. Plants were watered to soil field capacity every 2 d to avoid water stress throughout the experiment and the hard soil crust formed after irrigation was broken to ensure better aeration in the soil.
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On 15 DAP, O3 was added to the charcoal-filtered air-stream entering two of the chambers to maintain an O3 concentration of 100±7 ppb for 7 h d–1 (10.00 h to 17.00 h) for 21 d. The other two chambers were set up the same way but without O3 addition. In the present study, a high target O3 treatment was chosen since O3 concentrations exceed potentially damaging levels (>120 ppb) for many h in some peri-urban areas of China during the summer months (Zheng et al., 1998; Wang et al., 2007b). The treatments (+O3, elevated O3; CF, charcoal-filtered control) were assigned randomly to the chambers and replicated twice. O3 was generated by electrical discharge using charcoal-filtered ambient oxygen (Balaguer et al., 1995) with an O3 generator (CF-KG1, Beijing Sumsun EP Hi-Tech., Co. Ltd. China) and bubbled through distilled water before entering the two high O3 chambers. Ambient air was used since it has been reported that the small amount of HNO3 vapour or N2O produced during generation of O3 using ambient air is typically undetectable and does not interact with O3 (Neighbour et al., 1990; Taylor et al., 1993; Balaguer et al., 1995; Mortensen and Jorgensen, 1996). Water traps were used to remove harmful compounds other than O3 (Balaguer et al., 1995). Manual mass flow controllers were used to regulate the flow of O3-enriched air to the OTCs. O3 concentrations in the OTCs were continuously monitored at approximately 10 cm above the plant canopy using an O3 analyser (APOA-360, Horiba, Ltd, Japan), which was cross-calibrated with another O3 monitor (ML 9810B, Eco-Tech, USA). In order to minimize chamber effects and environmental heterogeneity, plants and associated treatment were rotated between the chambers and plants were also randomized within the chambers every three days throughout the experiment.
Visible O3 injury
Visible injury was assessed on the whole plant or leaf level (the third youngest leaf of the main stem) after 21 d of O3 exposure on 35 DAP, when the plants had a total of 5–6 fully expanded leaves. The percentage of damaged area (mottled or necrotic) on the leaves was assessed for five plants per species/cultivar sampled from control and O3 fumigated chambers.
Leaf gas exchange measurement
On day 19 of O3 fumigation, four plants per species/cultivar were sampled from each chamber per treatment for leaf gas exchange measurements. The most recently fully expanded leaf (i.e. after emergence of ligules) without visible symptoms of damage on the main stem was used for measurement with an open gas exchange system (Li- 6400, Li-Cor, Inc., Lincoln, NE, USA). The system was calibrated prior to measurement. During measurement, relative humidity was maintained at 70% and leaf temperature was set at 25 °C in the leaf chamber. The flow rate was set at 700 µmol s–1 and CO2 concentration in the leaf chamber was maintained at 386 µmol mol–1. PPFD was maintained at 1500 µmol m–2 s–1using the internal light source of the leaf chamber. Data obtained as part of the gas exchange measurements included area-based light-saturated net photosynthetic rate (Asat), stomatal conductance (gs), the ratio between intercellular CO2 concentration (Ci) and ambient CO2 concentration (Ca), and leaf-level photosynthetic water use efficiency, or instantaneous transpiration efficiency (ITE), which was calculated as assimilation/transpiration.
Chlorophyll fluorescence measurement
On day 20 of O3 fumigation, four plants per species/cultivar were sampled from each chamber and taken into an adjacent laboratory for dark adaptation (40 min) to ensure maximal oxidization of the primary quinone acceptor (QA). The same plants were not used for fluorescence measurement to avoid plants with reduced ozone exposure during gas exchange measurement and any leaf injury resulting from leaf chamber. Modulated chlorophyll fluorescence measurements were made in the middle of the intact youngest fully expanded leaves without visible O3 injury using a PAM-2000 (Heinz Walz, Germany). The room temperature was maintained at 25 °C during measurements. The minimum fluorescence, F0, was determined with modulated light which was sufficiently low (<1 µmol m–2 s–1), so as not to induce any significant variable fluorescence. The maximum fluorescence, Fm, was determined using a 0.8 s saturating pulse at 8000 µmol m–2 s–1. Data obtained after recording fluorescence key parameters included minimum fluorescence (F0), maximum fluorescence (Fm), variable fluorescence, Fv=Fm–F0, and maximum photochemical efficiency in the dark-adapted state, Fv/Fm (Krause and Weis, 1991).
Determination of growth and resource allocation
Plants were sampled for growth analysis before O3 fumigation (on 15 DAP) and after 21 d of O3 exposure (on 35 DAP). Four plants per species/cultivar were harvested from each chamber and partitioned into shoot and root before being dried to constant weight at 72 °C. The difference in dry weight between the pre-fumigation and final harvest was used to calculate relative growth rate of whole plants and plant parts over 21 d. Mean plant relative growth rate (RGR), relative growth rate of shoot (RGRs), relative growth rate of root (RGRr), and allometric coefficient (K=RGRr/RGRs) were calculated as described by Hunt (1990).
Statistical analysis
The experiment consisted of two randomized blocks of two treatments with 15 plants per replicate. Statistical analyses of data were performed using analysis of variance (ANOVA) in the General Linear Model procedure of SPSS (Ver. 13, SPSS, Chicago, IL, USA). The main effects of wheat type, wheat species, and wheat genotype in O3 and CF air were analysed using one-way ANOVA on the measured variables. To control the Type I error across the entire set of pair-wise comparisons, the Tukey–Kramer method was used to assess differences among treatment means. Regression analysis was carried out to investigate the relationships between physiological and growth parameters. Differences between treatments were considered significant at P < 0.05.
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Results |
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Visible O3 injury
Elevated O3 developed visible O3 injury on mature leaves of all wheat species, whereas control plants showed no visible symptoms of O3 damage. No visible symptoms were observed on the youngest fully expanded leaves. All species exposed to high O3 showed the start of premature leaf senescence (Leaf 1) after one week of O3 fumigation (data not shown). There was a significant (P < 0.001) interspecies variation in O3 injury developed on the third youngest leaf of the main stem (48–72%) after the end of O3 fumigation (Table 2). The lowest visible symptoms were observed both in T. turgidum ssp. durum and T. dicoccum, whereas wild species (A. tauschii, T. boeoticum) showed the highest. Significantly differences in visible O3 symptoms were noted between the cultivars. Visible O3 symptoms were found to be significantly positively correlated with gs in O3-exposed plants, but negatively correlated with RGR and total biomass relative to control (Fig. 1).
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Gas exchange
Ozone significantly (P < 0.05) decreased Asat and ITE, but increased gs and Ci/Ca. There was considerable interspecies variation in gas exchange characteristics in CF air or O3-treated plants (Table 3). The highest Asat and gs were observed in wild wheat, followed by modern wheat and the lowest was in primitive cultivated wheat in CF air (data not shown). Significantly higher Asat and ITE were observed in modern than in primitive cultivated or wild wheat of O3-exposed plants. Wild wheat had higher gs and Ci/Ca than modern or primitive cultivated wheat at high O3. The highest relative reduction in Asat was observed in Triticosecale wittmack, while T. dicoccum showed the lowest. Almost all wheat species displayed non-significant relative increases in gs, while T. turgidum ssp. durum and Triticosecale wittmack showed a relative decrease in gs. In addition, A. tauschii showed no change in gs in O3 relative to the control. The highest and lowest relative increases in Ci/Ca were observed in T. boeoticum and T. timopheevii, respectively. T. turgidum ssp. durum had the lowest relative loss of ITE, while T. boeoticum had the highest. Wheat cultivars also showed significant variation in gas exchange traits in both CF air and elevated O3. Among donor species of T. aestivum, the highest relative loss in Asat and ITE was noted in A. tauschii, followed by T. monococcum and the least was in T. turgidum ssp. durum. There were strong negative relationships between gs in ozone-exposed plants and reduction in total mass, RGR and Fv in O3 relative to control (Fig. 2).
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Chlorophyll fluorescence
Ozone significantly (P < 0.001) decreased dark-adapted ground fluorescence (F0), maximum fluorescence (Fm), variable fluorescence (Fv) and maximum photochemical efficiency (Fv/Fm). Large interspecies variation in chlorophyll fluorescence was observed in CF and ozonated plants (Table 4). Modern and primitive cultivated wheats had higher F0, Fm, and Fv than wild wheat both in CF air and elevated O3 (data not shown). Higher Fv/Fm was observed in modern wheat rather than in wild wheat or primitive cultivated wheat in CF air. There was no significant interspecies variation in Fv/Fm in O3-treated plants. The highest relative reduction in F0, Fm, and Fv was observed in A. tauschii, while T. polonicum showed the lowest. The highest and lowest relative reduction in Fv/Fm was observed in Triticosecale wittmack and in T. turgidum ssp. durum, respectively (Table 2). Significant cultivar differences were also noted in F0, Fm, and Fv both in CF air and elevated O3. Among donor species of modern wheat, the highest relative decrease in Fv was observed in A. tauschii, followed by T. monococcum and the least was in T. turgidum ssp. durum. Both A. tauschii and T. monococcum had higher relative loss in Fv/Fm than T. turgidum ssp. durum. Fv in ozone-exposed plants was significantly positively correlated with relative reduction in total mass and RGR, but negatively (r = –0.54, P=0.069) with relative reduction in K. It also positively correlated with the relative reduction in shoot mass, RGRs and Asat (Fig. 3).
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Growth and resource allocation
Ozone significantly (P < 0.001) decreased RGR, RGRs, RGRr, and K in wheat species (Table 5). There was significant interspecies difference in growth and resource allocation in control plants. Generally higher RGR, RGRs, and RGRr were observed in wild wheat rather than in modern wheat or in primitive cultivated wheat. Modern and primitive cultivated wheats had higher K than wild wheat. Significant variation (P < 0.05) was observed between wheat types showing higher RGR and RGRs in primitive cultivated wheat than in modern or wild wheat (data not shown) at elevated O3. There was significant variation in RGR, RGRs, RGRr and K in wheat cultivars exposed to CF air, but not to elevated O3. Among genome donors of modern wheat, the highest relative decrease in RGR, RGRs, RGRr, and K was observed in A. tauschii, followed by T. monococcum and the least was in T. turgidum ssp. durum. RGR in CF control plants was significantly negatively correlated with relative reduction in RGR and RGRs, but positively (r=0.52, P=0.083) with the relative reduction in K (Fig. 4).
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Dry matter accumulation and partitioning
Ozone significantly (P < 0.001) decreased shoot, root, root/shoot ratio, and total mass in wheat species, with the greater effect being in roots than in shoots (Table 6). Considerable interspecies variation in dry matter accumulation and partitioning were observed in both control and O3-treated plants. The highest shoot, root, and total masses were observed in modern wheat, followed by primitive cultivated wheat and the lowest in wild wheat both in CF air and elevated O3 (data not shown). Significantly higher root/shoot ratio was noted in modern wheat than in wild or primitive cultivated wheat in CF air. Modern and wild wheats showed higher root/shoot ratios than primitive cultivated wheat at elevated O3. Nevertheless, T. turgidum ssp. durum showed the lowest relative reduction in shoot, root, and total mass, while T. boeoticum showed the highest. The lowest relative reduction in root/shoot ratio was found in T. boeoticum, while T. timopheevii showed the highest. Wheat cultivars showed significant variation in shoot, root, root/shoot ratio, and total mass both in CF air and elevated O3. Among donor species of modern wheat, the highest relative decrease in shoot, root, and total mass was observed in A. tauschii, followed by T. monococcum and the least was in T. turgidum ssp. durum. Higher relative reduction in root/shoot ratio was noted both in T. monococcum and T. turgidum ssp. durum than in A. tauschii.
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Discussion |
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Interspecies differences in the development of visible symptoms of O3 damage in winter wheat
The similar trend of premature leaf senescence (Leaf 1) and the extent of visible symptoms on the third youngest leaves after 7 d and 21 d of O3 fumigation, respectively, revealed that all species were sensitive to O3. There was significant (P < 0.001) interspecies variation in the extent of visible O3 injury in winter wheat ranging from 48% to 72%. The extent of visible O3 injury was found to be correlated with gs in O3-exposed plants. This can be explained because O3 uptake is proportional to gs and O3 produces reactive oxygen species which can severely compromise the integrity of metabolically important membranes (Long and Naidu, 2002; Biswas et al., 2008). These results indicated that higher O3 uptake through increased gs finally led to a greater development of visible injury as well as greater growth reduction. These results are consistent with the findings of Barnes et al. (1990) who obtained a significant negative relationship between visible injury and mean RGR or Fv of spring wheat cultivars exposed to 90 ppb O3. This can be explained by loss of chlorophyll and the oxidative stress induced by O3 as a close relationship between the extent of visible O3 injury and reduction in Fv/Fm has been documented in bean genotypes (Guidi et al., 2000).
Photosynthetic and growth responses of winter wheat species to O3
Overall, O3 significantly depressed Asat and ITE, but increased gs and Ci/Ca. These results are in general agreement with the findings of McKee et al. (1995), Mulholland et al. (1997), and Farage and Long (1999). The effects of O3 on gs have been found to be highly variable, as an increase, decrease, and no change in gs have all been reported in spring wheat and other crops grown at elevated O3 (Darrall, 1989; Mulholland et al., 1997; Farage and Long, 1999; McKee et al., 2000). Our results suggested that O3 depressed photosynthesis by impairing the activity of mesophyll cells as indicated by higher Ci/Ca. Elevated O3 also significantly (P < 0.001) decreased F0, Fm, Fv, and Fv/Fm. A slight O3-induced reduction in F0 (–8%) was observed, which was accompanied by higher reductions in Fm (–26%) and Fv (–31%). These results are consistent with the previous reports on winter wheat exposed to 80 ppb O3 (Khan, 2005). The results indicated that overall thermal dissipation by the xanthophyll cycle was minimum, which resulted in higher O3-impairment of Fv/Fm (–7%) mediated electron transport or O3-induced photoinhibition (Guidi et al., 1997; Cardoso-Vilhena et al., 2004; Fiscus et al., 2005). In general, O3 significantly decreased RGR, RGRs, RGRr, and K in winter wheat species, which led to a major decrease in shoot, root, root/shoot ratio, and total mass at final harvest. The marked O3-induced reduction in K indicated that shoot growth was maintained at the expense of root growth in winter wheat at high O3. These results are very consistent with the previous reports on a number of crop species (Andersen, 2003; Grantz et al., 2006).
Interspecies differences in the impact of elevated O3 on photosynthesis and growth
Winter wheat species showed significant (P < 0.01) differences in gas exchange and fluorescence signals in response to O3. Interspecies variation in the impacts of elevated O3 on Asat or ITE might be mediated by significant variation (P < 0.05) in gs in ozonated plants. For instance, wild species demonstrated higher O3 flux as shown by increased gs in O3-treated plants resulting in higher relative reduction in Asat than modern or primitive cultivated species. It can be further explained by higher O3-impairment of mesophyll cells in wild species than in modern or primitive cultivated species as documented by increased Ci/Ca. Nevertheless, the highest relative loss in Asat was observed in Triticosecale wittmack, which exhibited a decrease in gs (–9%) and an increase in Ci/Ca (13%) relative to control. On the other hand, the lowest relative loss in Asat was observed in T. dicoccum showing a relative increase in gs (37%) and Ci/Ca (11%). These results therefore suggested that loss of photosynthetic capacity in winter wheat due to high O3 was largely related to species-specific physiological characteristics. As a result, there was no consistent trend among relative changes in Asat, gs, Ci/Ca, and ITE in winter wheat species.
As for chlorophyll fluorescence, modern or primitive cultivated species displayed higher F0, Fm, and Fv at elevated O3 as well as lower relative reduction in respective parameters than wild species. This indicates that O3-caused impairment of PSII-mediated electron transport was higher in wild species than in modern or primitive cultivated species. Although O3 significantly altered the fast kinetics of fluorescence, there was no significant interspecies difference in the impacts of elevated O3 on Fv/Fm in winter wheat. It is conceivable because O3 causes slight, but significant decrease in Fv/Fm (Reichenauer et al., 1998; Cardoso-Vilhena et al., 2004). A wild species, A. tauschii appeared as the most sensitive to O3 as shown by the highest relative reduction in F0 (–32%), Fm (–43%), and Fv (–46%), while a primitive cultivated species, T. polonicum behaved as O3-tolerant as documented by the lowest corresponding changes, which were +5%, –17%, and –23%, respectively. However, among fluorescence parameters, Fv appeared as the most sensitive and reliable parameter in detecting O3 stress as Fv in ozonated plants significantly correlated with Asat, RGR, RGRs, K, shoot and total mass in winter wheat species.
Generally, there was no interspecies variation in the impact of O3 on RGR and K. However, when data were analysed based on wheat type, there were significant differences (P < 0.05) in the effects of O3 on RGR, RGRs and K (P=0.116) showing higher RGR and RGRs in O3 in modern wheat or primitive cultivated wheat than in wild wheat. Higher K was noted in modern or wild wheat than in primitive cultivated wheat at elevated O3. Relative loss in RGR and RGRs indicated that primitive cultivated species appeared as the most resistant to O3, followed by modern and wild species behaving as the most sensitive to O3. Higher O3 tolerance in primitive cultivated species might be attributed to lower gs in O3-exposed plants as there was a significant relationship between gs in O3 and relative reduction in RGR. As O3 uptake is proportional to gs (Long and Naidu, 2002; Danielsson et al., 2003; Pleijel et al., 2006), lower gs resulted in lower O3 uptake into the mesophyll tissue of primitive cultivated species and hence lower O3 induced losses in Asat and RGR (McKee et al., 1997; Biswas et al., 2008). This can also be attributed to the slow-growth rate of primitive cultivated species in CF air since RGR in control plants negatively correlated with relative reduction in RGR. In addition, there was a considerable positive relationship (r=0.52, P=0.083) between RGR in CF air and relative reduction in K. This suggests that wheat species with slow-growth rate in CF air showed a larger O3-induced reduction in K, which could be a mechanism of higher O3 resistance (Grantz et al., 2006).
Higher O3-induced loss in Asat through impaired activity of mesophyll cells and photochemistry finally resulted in the highest relative loss in biomass accumulation in wild species, followed by modern wheat and the lowest in primitive cultivated species. However, gs in O3-exposed plants can explain about 69% variation in total dry matter accumulation, as there was a significant relationship (r = –0.69**) between gs in O3 and relative loss in total mass (Biswas et al., 2008). Although wild species had the highest relative loss in total mass, they displayed the lowest relative reduction in root/shoot ratio. This could be an adaptive mechanism of wild species at elevated O3 (Grantz et al., 2006). In particular, T. turgidum ssp. durum appeared as the most O3-tolerant, while A. tauschii appeared as the most O3-sensitive as indicated by the lowest and highest relative loss in shoot, root, and total mass in O3, respectively.
Comparison of O3 tolerance between modern wheat and its donor species
As noted above, the probable donors of the A, B and D genome of modern wheat (AABBDD) are (i) T. turgidum ssp. durum (AABB), (ii) T. monococcum L. (AA), and (iii) Aegilops tauschii (DD) (Feldman, 2001; Levy and Feldman, 2004; Matsuoka and Nasuda, 2004; Rudnoy et al., 2004). It is evident from the present study that among the three genome donors of modern wheat, the highest relative reduction in Asat was observed in A. tauschii (–55%) followed by T. monococcum (–42%), and the least was observed in T. turgidum ssp. durum (–26%). The highest relative reduction in ITE was observed in A. tauschii (–48%), while the lowest was in T. turgidum ssp. durum (–36%). These results indicated that the addition of the B genome into the A genome of T. monococcum (i.e., the origin of T. turgidum ssp. durum) reduced the negative impacts of O3 on photosynthesis. On the other hand, the addition of the D genome into the AB genome of T. turgidum ssp. durum (i.e., the origin of T. aestivum) enhanced the negative effects of O3 on photosynthesis in winter wheat. Although there is no report on the effects of O3 on B and D genomes, evidence of adverse effects of the D genome on photosynthesis has been reported elsewhere (Planchon and Fesquet, 1982; Haour-Lurton and Planchon, 1985). As for chlorophyll fluorescence, A. tauschii showed the highest O3-induced impairment of PSII activity as the highest relative reduction in F0 (–32%), Fm (–43%), and Fv (–46%) was noted. T. monococcum had higher Fm (–26%) and Fv (–30%), while T. turgidum ssp. durum showed the lowest Fm (–23%) and Fv (–25%) in O3 relative to control. Lower relative loss in Fv/Fm was observed in T. turgidum ssp. durum (–5%) than in A. tauschii (–6%) and T. monococcum (–6%). This further indicated that the addition of the B genome into the A genome of T. monococcum decreased deleterious O3 impacts of the A genome on Fm, Fv, and Fv/Fm. Relative loss in F0, Fm, Fv, and Fv/Fm in T. aestivum was –4%, –25%, –30%, and –7%, respectively. This also suggests that the addition of D genome resulted in higher O3-induced impairment of photochemistry in T. aestivum than its predecessor, T. turgidum ssp. durum.
The negative effect of the D genome on photosynthesis was also apparent on growth and resource allocation in O3-treated plants. The highest relative loss in RGR, RGRs, RGRr, and K in A. tauschii was –63%, –59%, –81%, and –65%, respectively. T. monococcum had an intermediate response, while the lowest relative loss in those variables in T. turgidum ssp. durum was –34%, –23%, –63%, and –25%, respectively. Besides, the corresponding values in T. aestivum were –51%, –38%, –81%, and –44%, respectively. This suggests that addition of the D genome into the AB genome of T. turgidum ssp. durum resulted in higher O3 sensitivity in modern wheat compared to its predecessors. It can be further reinforced by the similar trends of O3-induced dry matter accumulation and partitioning in T. aestivum and its donor species. For example, the highest relative loss in shoot (–65%), root (–80%), and total mass (–69%) was observed in A. tauschii, followed by T. monococcum and the lowest relative reduction in shoot (–25%), root (–65%), and total mass (–36%) was observed in T. turgidum ssp. durum. On the other hand, relative reduction in shoot, root, and total mass in T. aestivum was –44%, –78%, and –57%, respectively. Our results therefore further demonstrated that higher O3 tolerance in T. turgidum ssp. durum and higher O3 sensitivity in T. aestivum were attributed to the addition of B and D genomes, respectively. However, more investigations are necessary to make a definite conclusion on the increased O3 sensitivity of the D genome in wheat.
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Acknowledgements |
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We wish to thank anonymous reviewers for their valuable suggestions on an early version of the manuscript. The work was co-financed by the Innovative Group Grant of the National Science Foundation of China (No. 30521002), the National Basic Research Program of China (2007CB106804), Key Project of the Chinese Academy of Sciences (KZCZ2-XB2-01), and Beijing National Science Foundation (No. 8062017).
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