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Intraspecific variation in sensitivity to ultraviolet-B radiation in maize grown under field conditions. I. Growth and morphological aspects
Field Crops Research 59 (1998) 81±89
Intraspeci®c variation in sensitivity to ultraviolet-B radiation in maize grown under ®eld conditions. I. Growth and morphological aspects Correia C.M.*, Areal E.L.V., Torres-Pereira M.S., Torres-Pereira J.M.G. Section of Biological and Environmental Engineering, University of TraÂs-os-Montes and Alto Douro, 5000 Vila Real, Portugal Received 23 December 1997; received in revised form 17 April 1998; accepted 25 April 1998
Abstract This study was conducted to determine the growth and morphological effects of UV-B on 8 cultivars of maize (Zea mays L.) in a Mediterranean climate. Dry weight, leaf area, leaf area duration (LAD), ear length, mean relative growth rate (RGR), and mean net assimilation rate (NAR) were signi®cantly reduced by UV-B treatment in some cultivars. Plant height and number of leaves were not affected. Changes in partitioning of biomass and premature leaf senescence were also recorded. Considerable variation in UV-B sensitivity exists within cultivars. DK 498 was the most sensitive and REG.VR the least sensitive. These genotypic differences suggest that future attempts at breeding for increased tolerance to UV-B radiation might be successful. # 1998 Elsevier Science B.V. All rights reserved. Keywords: UV-B radiation; Maize; Growth analysis; Sensitivity ranking
1. Introduction The stratospheric ozone layer constitutes a protective atmospheric ®lter against biologically harmful solar UV radiation. Anthropogenic emissions of chloro¯uorocarbons and nitrogen oxides result in depletion of the ozone layer (Rowland, 1990). As a consequence, increased levels of ultraviolet-B radiation have been measured in the Southern (Frederick et al., 1994) as well in the Northern Hemisphere (Seckmeyer et al., 1994) in both high and temperate latitudes (Madronich and de Gruijl, 1994). Although UV-B represents only a small part of the solar radiation reaching the surface of the earth, its
*Corresponding author. Fax: +351 593 20480; e-mail: [email protected] 0378-4290/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0378-4290(98)00102-6
impact on the biological processes can be very important. Ultraviolet-B radiation is known to negatively in¯uence plant growth and development in higher plants (Caldwell, 1981; Teramura, 1983; Rozema et al., 1990; Runeckles and Krupa, 1994; Correia, 1995), although neutral and positive effects were also reported (Krupa and Kickert, 1989; Sullivan et al., 1992; Tosserams and Rozema, 1995). Since Zea mays L. is the third most important worldwide crop, after wheat and rice, and very few studies concerning its response to UV radiation have been done, it is of interest to gain information about its response to enhanced UV-B radiation. In the present study we examined such in¯uences on 8 cultivars of maize under ®eld growing conditions in the Mediterranean region. Our objectives were to characterize the range of growth and morphological responses to UV-B and elaborate a sensitivity ranking of maize cultivars.
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2. Material and methods This study was conducted at the University of TraÂsos-Montes and Alto Douro, Vila Real, Portugal (418 190 N, 78 440 W; 450 m elevation), between 25 June and 2 October 1996. The normal sowing date in this region of Northern Portugal is in the middle of May, but this was delayed by dif®culties associated with the experimental installation. The optimal harvest date extends to the middle of September because the rain season begins in early Autumn. For these reasons it was impossible to reach commercial maturation or even physiological maturation. Therefore, we present data from the biological yield only. A split-plot design was employed. The UV-B treatment was assigned to the mainplot and cultivar to the subplot. The experiment used 3 replicates. Five plants within each replicate were sampled for growth analysis. The experimental ®eld was divided into high UV-B treatment (UV) and ambient UV-B treatment, as a control (C). High UV-B treatment was supplied by preburned Philips sun lamps (TL 40 W/12), and began immediately after plants emerged. Radiation transmitted by the UV tubes was ®ltered using 0.1 mm cellulose acetate foil (Ultraphan, Weil am Rhein, Germany), which eliminates radiation below 290 nm. The ®lters were replaced twice a week to maintain uniform optical properties. Lamps were in frames that were adjusted weekly to a distance to provide a mean supplement of 0.65 wmÿ2 (unweighted) of UV-B radiation at plant apices for 8 h daily over the middle of the photoperiod. The difference betwen ambient and high UV-B levels was about 30%. For reference, the mean daily unweighted ambient UV-B levels in Portugal during clear days in mid summer are above 70 KJ mÿ2. The homogeneity of the UV-B irradiance was measured after sunset (i.e. in the absence of ambient UV-B radiation) with an IL 1400 A radiometer (International Light, Newburyport, USA) with a photodetector (SEL 240) calibrated according to the National Institute of Standards and Technology (USA). We used a constant lamp output throughout the daily treatment period, which may cause a UV-B enhancement in early morning and late afternoon. The coef®cient of variation in the UV-B/PAR ratio during the 8 h of photoperiod was 13%. If we consider only the 4 h around the solar noon, the coef®cient of variation was 3.4%. The
variation in UV-B irradiance received at plant apices resulting from variability in plant height was less than 10%. The UV-B treatment was suspended on cloudy days (16 days) to prevent abnormally high UV-B to PAR ratios. Non-burning UV-B lamps were used above the control treatment area to create shade, as in the UV-B radiated experimental groups. In this way, the visible light environment under control and UV-B frames was similar. Shading from the lamps and lamp supports was estimated with a ceptometer (Decagon Sun¯eck Ceptometer, Pullman, WA, USA). During a clear day, with maximum shading (i.e. with low zenith angle), the plant apices received about 90% of the photosynthetically active radiation (PAR) found above the frames. Obviously, less shading is expected with increasing zenith angle. With this system a small increase in UV-A radiation under the UV-B frames was observed. However, under the high PAR levels in the ®eld, the additional UV-A irradiances would be considered neutral in effect and their careful control unnecessary (Middleton and Teramura, 1994). Seeds of 8 cultivars of maize (Zea mays L.) were used (Table 1). Two of them were open-pollinated cultivars: REG.VR is a cultivar of upland habitat, grown near Vila Real; REG.VS is a cultivar of lowland habitat grown in the Entre Douro e Minho region, which has a genetic af®nity to the Portuguese hybrid Braga. The seed bed was prepared by conventional tillage. The treatments received 200 kg N haÿ1 as ammonium nitrate, 90 kg P2O5 haÿ1 as superphosphate and 180 kg K2O haÿ1 as potassium cloride. Half of the N and all of the P2O5 and K2O were applied broadcast and incorporated prior to sowing, and the remainder of the N was sidedressed as a band around 40±50 cm of the Table 1 Characteristics of maize cultivars (H-hybrid; OPC-open-pollinated) Cultivar
FAO Cycle
Type
Origin
Anjou 37 Teodora Avantage REG. VR DK 498 Braga Polo REG. VS
200 200 200 200 300 300 300 200
H H H OPC H H H OPC
France France Germany Portugal USA Portugal Germany Portugal
C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
plant height. Maize was oversown at a within-row spacing of 0.15 m spaced 0.75 m apart, and thinned to a ®nal density of 89000 plants haÿ1. Rainfall was supplemented with furrow irrigation as necessary to ensure that the crops did not suffer water stress. Weeds were controlled manually. At the end of the experiment, the plants were harvested and the following parameters were measured: leaf area (LICOR 3100, Lincoln, NE, USA), number of total green leaves, number of green leaves below the ear (NLBE), ear length, plant height and dry weight of each aboveground plant organ (after drying in a force-draft oven at 708C to a constant weight). Based on the data of leaf area and dry weight at the initial check (7 days after emergence) and ®nal harvest, the mean relative growth rate (RGR), mean net assimilation rate (NAR), leaf area ratio (LAR), speci®c leaf area (SLA), leaf weight ratio (LWR) and leaf area duration (LAD) were calculated using the equations shown in Hunt (1978). A UV-B sensitivity index (Lydon et al., 1986) was determined by adding the percentage changes in plant dry weight, plant height and leaf area (percentage change(control-treatment)/control100).
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All data were analyzed by analysis of variance to test the main effects of UV-B radiation. Signi®cantly different means were separated using the LSD test. 3. Results Enhanced UV-B irradiation signi®cantly reduced many components of the growth and morphology of maize plants (Table 2). Across all cultivars, the UV-B treatment was found to reduce signi®cantly total aerial plant dry weight (p0.01), total leaf area (p0.029), the number of leaves below the ear (p0.052), the ear length (p0.022),the leaf size (p0.036) and LAD (p0.027). Plant height and the number of leaves were not signi®cantly affected by UV-B treatment. When the responses of cultivars were examined individually, only 3 cultivars (DK 498, Braga and REG.VS) exhibited signi®cant (p<0.1) reductions in the parameters measured. However, in general, behaviour was the same as in the other cultivars. Due to unequal variances among cultivars, treatment effects of a similar relative magnitude were not always similar in terms of the level of statistical signi®cance. Only
Fig. 1. Partition of dry matter at the harvest as affected by enhanced UV-B radiation. Numbers on treatments indicate different cultivars (the order is the same as descending order in Table 2).
UV C
UV C
UV C
UV C
UV C
UV C
UV C
UV C
UV C
Anjou 37
Teodora
Avantage
REG.VR
DK 498
Braga
Polo
REG.VS
Total
b
Significant at p0.1. Significant at p0.05.
a
Treatment
Cultivar
120.9 (30.6) 156.7 (35.2) ÿ22.8% 122.5 (8.4) 161.3 (26.1) ÿ24.0% 131.0 (19.8) 162.3 (3.2) ÿ19.3% 151.6 (17.4) 183.7 (5.9) ÿ17.4% 123.5 (5.3) 169.6 (18.6) ÿ27.2%a 118.2 (17.9) 169.6 (28.1) ÿ30.3%b 158.7 (6.7) 176.9 (11.2) ÿ10.3% 141.8 (13.2) 173.5 (3.9) ÿ18.3% 133.5 (5.8) 169.2 (6.2) ÿ21.1%b
Plant weight g plant-1 0.282 (0.003) 0.315 (0.003) ÿ10.4% 0.274 (0.002) 0.312 (0.002) ÿ12.1% 0.316 (0.003) 0.352 (0.002) ÿ10.2% 0.266 (0.001) 0.254 (0.002) 4.5% 0.357 (0.001) 0.447 (0.005) ÿ20.1%b 3.90 (0.004) 4.80 (0.006) ÿ18.6%b 0.365 (0.001) 0.406 (0.005) ÿ10.0% 0.255 (0.003) 0.349 (0.001) ÿ26.9%b 0.313 (0.012) 0.364 (0.018) ÿ14.0%b
Leaf area m2 plant-1 216.4 (2.3) 209.8 (10.6) 3.2% 222.9 (11.4) 221.3 (6.3) 0.8% 251.5 (11.8) 246.3 (11.9) 2.1% 216.3 (4.7) 203.5 (5.9) 6.3% 238.1 (7.1) 256.8 (8.7) ÿ7.3% 233.8 (19.2) 227.6 (18.1) 2.7% 258.7 (5.9) 249.0 (19.3) 3.9% 208.5 (6.0) 221.3 (6.7) ÿ5.8% 230.8 (4.6) 229.4 (5.2) 0.6%
Plant height cm 11.1 (0.1) 11.6 (0.2) ÿ4.5% 11.3 (0.5) 11.3 (0.3) 0% 10.9 (0.1) 11.3 (0.3) ÿ3.4% 10.7 (0.3) 9.7 (0.2) 10.0%a 12.0 (0.6) 12.7 (0.5) ÿ5.3% 13.2 (0.4) 13.2 (0.4) 0% 11.8 (0.4) 12.3 (0.7) ÿ4.5% 9.6 (0.3) 11.0 (0.5) ÿ12.6%b 11.3 (0.2) 11.6 (0.2) ÿ2.7%
Number of leaves 2.0 (0.1) 2.4 (0.1) ÿ17.2% 1.5 (0.4) 2.0 (0.1) ÿ25.0%a 1.7 (0.2) 1.6 (0.1) 1.7% 1.5 (0.1) 1.3 (0.2) 12.8% 1.7 (0.3) 2.2 (0.4) ÿ23.1%a 1.9 (0.4) 2.5 (0.2) ÿ24.2%b 1.9 (0.3) 2.5 (0.1) ÿ24.4% 1.7 (0.1) 1.8 (0.2) ÿ4.7% 1.7 (0.1) 2.0 (0.1) ÿ15.5%a
NLBE 17.1 (0.8) 17.9 (0.6) ÿ4.8% 17.9 (0.1) 19.3 (1.2) ÿ7.0% 20.4 (0.8) 21.7 (0.3) ÿ6.3% 17.3 (1.0) 19.3 (0.2) ÿ10.6%b 19.3 (0.4) 21.2 (0.4) ÿ8.8%a 19.6 (1.1) 20.7 (1.1) ÿ5.2% 22.4 (1.1) 21.4 (1.2) 4.4% 15.3 (0.7) 17.1 (0.6) ÿ10.3%a 18.7 (0.5) 19.8 (0.4) ÿ5.9%b
Ear length cm 254.2 (23.3) 271.0 (19.3) ÿ6.2% 243.8 (11.9) 278.6 (13.3) ÿ12.5% 289.3 (24.4) 310.6 (5.3) ÿ6.9% 250.4 (12.4) 260.7 (12.1) ÿ4.0% 298.8 (14.9) 352.2 (24.9) ÿ15.2%a 295.0 (19.3) 361.2 (40.4) ÿ18.3%b 311.0 (13.9) 327.4 (23.0) ÿ5.0% 262.7 (20.4) 316.5 (6.9) ÿ17.0% 275.6 (7.3) 309.8 (9.6) ÿ11.0%b
Leaf size cm2
0.291 (0.003) 0.320 (0.003) ÿ9.0% 0.284 (0.002) 0.318 (0.002) ÿ10.7% 0.321 (0.003) 0.353 (0.001) ÿ9.1% 0.274 (0.001) 0.263 (0.001) 4.3% 0.371 (0.001) 0.454 (0.004) ÿ18.2%b 0.402 (0.003) 0.482 (0.006) ÿ16.6%b 0.379 (0.001) 0.416 (0.005) ÿ9.0% 0.264 (0.003) 0.349 (0.001) ÿ24.4%b 0.323 (0.001) 0.369 (0.002) ÿ12.5%b
LAD m2 day
Table 2 Effects of UV-B radiation on several plant parameters of maize cultivars. Mean values with standard errors. The percentages indicate the changes in plants grown with enhanced UV-B compared to the control plants
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C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
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Table 3 Effects of UV-B radiation on growth analysis parameters. Mean values with standard errors. The percentages indicate the changes in plants grown with enhanced UV-B compared to the control plants Cultivar
Treatment
RGR mg g-1 day-1
Anjou 37
UV C
Teodora
UV C
Avantage
UV C
REG.VR
UV C
DK 498
UV C
Braga
UV C
Polo
UV C
REG.VS
UV C
Total
UV C
68.9 (2.8) 72.4 (2.6) ÿ4.8% 68.0 (0.7) 72.8 (3.2) ÿ6.6%b 68.5 (1.7) 71.4 (0.2) ÿ4.1% 74.9 (1.2) 76.1 (1.3) ÿ1.6% 63.9 (0.5) 66.9 (1.3) ÿ4.5% 63.2 (1.5) 66.8 (1.9) ÿ5.4% 68.5 (0.5) 69.5 (0.7) ÿ1.4% 70.4 (1.1) 73.1 (0.2) ÿ3.7% 68.3 (0.8) 71.1 (0.8) ÿ3.9%b
NAR g m-2 day-1 40.2 (6.7) 48.0 (7.3) ÿ16.1% 42.5 (0.7) 50.3 (6.0) ÿ15.5% 39.9 (3.0) 45.8 (2.5) ÿ12.9% 54.6 (5.0) 70.5 (4.7) ÿ22.6%c 33.0 (0.6) 36.7 (1.1) ÿ10.0% 28.9 (2.2) 34.2 (2.1) ÿ15.4% 41.8 (0.9) 42.6 (2.7) ÿ1.9% 54.1 (0.9) 49.6 (2.2) 9.2% 41.9 (2.0) 47.2 (2.5) ÿ11.3%b
LAR m2 kg-1 2.6 (0.4) 2.2 (0.3) 18.2%a 2.4 (0.1) 2.0 (0.3) 20.0% 2.6 (0.1) 2.3 (0.1) 13.0% 1.9 (0.2) 1.4 (0.1) 35.7%a 2.9 (0.1) 2.7 (0.1) 7.4% 3.4 (0.2) 3.0 (0.2) 13.3%a 2.4 (0.1) 2.3 (0.2) 4.3% 1.9 (0.1) 2.1 (0.1) ÿ9.5% 2.5 (0.1) 2.2 (0.1) 13.6%c
LWR g kg-1 190.0 (15.1) 172.5 (15.6) 10.1% 165.5 (6.9) 156.3 (7.0) 5.9% 188.8 (6.8) 180.6 (5.0) 4.5% 139.0 (9.6) 115.4 (5.8) 20.5%a 206.8 (1.4) 194.7 (0.8) 6.2% 233.5 (11.7) 203.2 (9.6) 14.9%b 174.5 (5.6) 173.2 (12.4) 0.8% 146.9 (11.1) 154.4 (5.3) ÿ4.9% 180.6 (6.7) 168.8 (5.9) 7.0%
SLA m2 kg-1 13.4 (1.0) 12.4 (0.7) 8.1% 14.3 (0.6) 12.9 (1.0) 10.9%a 13.5 (0.7) 12.3 (0.5) 9.8% 13.4 (0.6) 12.3 (0.5) 8.9% 14.2 (0.1) 13.9 (0.4) 2.2% 14.9 (1.2) 14.8 (0.4) 0.7% 13.6 (0.7) 13.4 (0.1) 1.5% 13.1 (0.3) 13.3 (0.4) ÿ1.5% 13.8 (0.2) 13.2 (0.2) 4.5%
a
Significant at p0.1. Significant at p0.05. c Significant at p0.01. b
REG.VR and Polo, particularly the ®rst, exhibited signi®cant increase (p<0.1) in some growth parameters in response to UV-B radiation. Almost all cultivars showed reductions in leaf weight, stem weight (stem tassels) and ear weight (data not shown). Although cultivar differences existed in response to UV-B radiation, reductions in total dry weight were accompanied by changes in the partitioning of the biomass into component organs. In UV-B-treated plants a greater proportion of biomass was partitioned to leaves and stems, namely, in REG.VR, DK 498 and Braga, and a lesser proportion to ears (Fig. 1). This could decrease the harvest index of these cultivars. Growth analysis also revealed signi®cant reductions in RGR and NAR, but at the same time, a noticeable
increase in LAR in UV treated plants due to increase in LWR and SLA, although this was not statistically signi®cant (Table 3). Signi®cant correlations were found between plant dry weight and plant parameters, but some differences were observed between treatments (Table 4). In UVB-treated plants, plant dry weight is affected primarily by NAR and to a lesser extent by plant height and leaf area, indicating that some positive relationships exist between physiological and morphological sensitivity to UV-B and biomass reductions. In the control plants the importance of NAR and plant height is decreased, but the importance of leaf area is increased. LAD and ear length also had signi®cant positive correlations with dry weight. Speci®c leaf area was negatively correlated with biological yield, especially in UV-B
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C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
Table 4 Correlation analysis between several plant parameters and total plant dry weight Parameter
UV
C
Leaf area Plant height Ear length NAR LAD SLA
0.362a 0.406a 0.322 0.659c 0.326 ÿ0.741c
0.426b 0.352a 0.384a 0.453b 0.402a ÿ0.366a
a
Significant at p0.1. Significant at p0.05. c Significant at p0.001. b
treated plants, which indicates that leaf thickness per se has an important relationship with radiation use ef®ciency. Relative sensitivities of the cultivars varied according to which response variable was used in the ranking but were consistently most or least affected by the UVB in terms of dry matter production, plant height and leaf area (Barnes et al., 1993). The cultivars REG.VR and Polo were the least affected by UV-B whereas, DK 498, Braga and REG.VS were the most affected. The calculated UV-B sensitivity index (SI) ranged from ÿ6.6 for the least affected cultivar (REG.VR) to ÿ54.6 for the most affected (DK 498)(Table 5). Using this combined response, cultivars with an SI greater than ÿ20 were arbitrarily classi®ed as insensitive while those with an index value of less than ÿ40 were considered as sensitive. Cultivars with sensitivity Table 5 Ranking of the maize cultivars with respect to a UV-B sensitivity index. The sensitivity index was determined by adding the percentage changes in plant dry weight, plant height and leaf area Cultivar Insensitive REG.VR Polo Intermediate Avantage Anjou 37 Teodora Sensitive Braga REG.VS DK 498
Sensitivity index ÿ6.6 ÿ16.4 ÿ27.4 ÿ30.0 ÿ35.3 ÿ46.2 ÿ51.0 ÿ54.6
indices between ÿ20 and ÿ40 were considered to be of intermediate sensitivity. 4. Discussion Ultraviolet-B radiation had a signi®cant inhibitory effect on the growth and biological yield of several of the maize cultivars used in this study. This agrees with other works (Santos et al., 1993; van Staaij, 1994; Correia, 1995) where maize was found to be sensitive to UV-B. However, considerable variation in UV-B sensitivity exists between maize cultivars. These responses showed both similarities to and differences from what has been described for other species, both cultivated (Biggs et al., 1981; Teramura and Murali, 1986; Reed et al., 1992; Barnes et al., 1993) and native taxa (Caldwell et al., 1982; Sullivan et al., 1992). Reduction in plant dry weight may be explained by alterations in morphological and physiological processes. Decreases in leaf area, leaf area duration, ear length and, namely, in net assimilation rate, contribute to lower biomass accumulation in UV-B-treated plants. Thus, lower biological yields result from both inferior source and sink capacities. Decrease in RGR and NAR suggest that the growth reduction of the plants exposed to UV-B radiation was mainly due to the reduction in the ef®ciency of dry matter production per unit of leaf area, namely, net photosynthetic rate. Several researchers have reported that the exposure to UV-B radiation caused a reduction in the net photosynthetic rate of crop plants (Teramura, 1983; Strid et al., 1990; Ziska et al., 1993; Correia, 1995). This reduction may be closely related to the inhibition of photosynthetic electron transport, the inhibition of photosynthetic enzymes, increases in stomatal and mesophyll resistance and ultrastructural changes in chloroplasts (Brandle et al., 1977; Pfundel et al., 1991; Nedunchezhian and Kulandaivelu, 1991; Jordan et al., 1992; Eichhorn et al., 1993; Musil and Wand, 1993; Grammatikopoulos et al., 1994; He et al., 1994). Maize UV plants may compensate for a lower NAR by increasing LAR, which suggests changes in the structural characteristics of the plants. A bigger LAR represents a greater investment of photosynthates in leaf area than in plant biomass and is due to an increase of LWR and SLA, which indicates larger biomass partition leaves and altered leaf morphology,
C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
respectively. The general trend towards increased SLA under UV-B treatment indicates that UV-B radiation decreases leaf thickness, as reported in other studies (van Staaij et al., 1993; Santos et al., 1993; Musil and Wand, 1994). This decrease may be important in plant dry weight reduction because decreased photosynthesis rates have been correlated with an increase in SLA, contributing to lower RGRs (Poorter, 1989). Plant height did not change after 3 months of UV-B treatment. This is in agreement with some reports (Cen and Bornman, 1990; van Staaij, 1994; Correia, 1995), but contradicts other studies (Tevini and Teramura, 1989; Krizek et al., 1993; Yakimchuk and Hoddinott, 1994). However, caution is needed in interpreting these results, because height differences may occur at one phenological stage but not at another. In a previous report (Correia, 1995) and in this study (data not shown) we have seen signi®cant differences in plant height at the vegetative stage but no differences were observed at the reproductive or maturation stage. The greater sensitivity at the early development stage to UV-B radiation has also been reported in some studies (Murali and Teramura, 1986; Naidu et al., 1993; Musil and Wand, 1994) and is attributed to lower concentrations of UV-B-absorbing compounds in young leaves (Teramura, 1983). Such growth reduction may potentially allow repair mechanisms such as photoreactivation and excision repair to be more effective in ameliorating UV-induced damage (Teramura and Sullivan, 1987). The decrease in the number of green leaves below the ear in UV-B plants indicates an early senescence of older foliage, also observed by other researchers (Sisson and Caldwell, 1977; Teramura and Sullivan, 1987; Naidu et al., 1993). Premature leaf senescence would alter the canopy carbon gain and nutrient relations. In fact, when the activity of lower leaves decreased, the supply of carbohydrates to the roots was limited (Palmer et al., 1973; Fairey and Daynard, 1978) and so root activity was reduced. Accordingly, absorption of nutrients, namely, nitrogen, was reduced too. As a consequence, increase in the decomposition of the nitrogen compounds of leaves and the photosynthetic rate was depressed. For these reasons leaf senescence may indirectly alter biomass production. Our study did not reveal any association between cultivar sensitivity and the geographic origin of the seed, as in the study of Barnes et al. (1993). Sensitivity
87
was the same between hybrids and open-pollinated cultivars, despite REG.VR being the most tolerant cultivar. REG.VR is the most tolerant cultivar in this study because, with regard to both leaf area and plant height parameters, performance was increased by UVB treatment. On the other hand, DK 498 and REG.VS are the most sensitive cultivars because the response of the 3 parameters used in the ranking changed in the same direction. In almost all cultivars, plant height responses minimize the effects of UV-B radiation. The evidence of signi®cant variation in UV-B sensitivity among maize cultivars is due to inherent genotypic differences and suggests that future efforts at breeding for increased tolerance to UV-B radiation might be possible. As maize is the third major crop in the world more ®eld studies are needed in order to elucidate which mechanisms are involved in the observed growth reductions due to enhanced UV-B radiation and also what can be done to minimize these negative effects.
References Barnes, P.W., Maggard, S., Holman, S.R., Vergara, B.S., 1993. Intraspecific variation in sensitivity to UV-B radiation in rice. Crop Sci. 33(5), 1041±1046. Biggs, R.H., Kossuth, S.V., Teramura, A.H., 1981. Response of 19 cultivars of soybeans to ultraviolet-B irradiance. Physiol. Plant. 53, 19±26. Brandle, J.R., Campbell, W.F., Sisson, W.B., Caldwell, M.M., 1977. Net photosynthesis, electron transport capacity and ultrastructure of Pisum sativum L. exposed to ultraviolet-B radiation. Plant Physiol. 60, 165±168. Caldwell, M.M., 1981. Physiological plant ecology I ± Responses to the physical environment, plant response to solar ultraviolet radiation. In: Encyclopedia of Plant Physiology, New Series, vol. 12 A. Springer, Berlin, pp. 169±197. Caldwell, M.M., Robberecht, R., Nowak, R.S., Billings, W.D., 1982. Differential photosynthetic inhibition by ultraviolet radiation in species from the Arctic±Alpine life zone. Arc. Alp. Res. 14, 195±202. Cen, Y.P., Bornman, J.F., 1990. The response of bean plants to UVB radiation under different irradiances of background visible light. J. Exp. Botany 41, 1489±1495. Correia, C.M., 1995. ConsequeÃncias do Aumento dos NõÂveis de Radiac,aÄo Ultravioleta-B na Produtividade AgrõÂcola. Estudos em Zea mays L. cv. LG5. Master thesis, UTAD, Vila Real, 98 pp. Eichhorn, M., Dohler, G., Augsten, H., 1993. Impact of UV-B radiation on photosynthetic electron transport of Wolffia arrhiza (L.) Wimm.. Photosynthetica 29(4), 613±618.
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Fairey, N.A., Daynard, T.B., 1978. Assimilate distribution and utilization in maize. Can. J. Plant Sci. 58, 719±730. Frederick, J.E., Diaz, S.B., Smolskaia, J., Esposito, W., Lucas, T., Booth, C.R., 1994. Ultraviolet solar radiation in the high latitudes of South America. Photochem. Photobiol. 60, 362± 365. He, J., Huang, L.K., Whitecross, M.I., 1994. Chloroplast ultrastructure changes in Pisum sativum associated with supplementary ultraviolet (UV-B) radiation. Plant, Cell and Environment 17, 771±775. Hunt, R., 1978. Growth analysis of individual plants. In: Arnold, E. (Ed.), Plant Growth Analysis. London. Jordan, B.R., He, J., Chow, W.S., Anderson, J.M., 1992. Changes in mRNA levels and polypeptide subunits of Ribulose-1,5bisphosphate carboxylase in response to supplementary ultraviolet-B radiation. Plant, Cell and Environment 15, 91±98. Krizek, D.T., Kramer, G.F., Upadhyaya, A., Mirecki, R.M., 1993. UV-B response of cucumber seedlings grown under metal halide and high pressure sodium/deluxe lamps. Physiol. Plant. 88, 350±358. Krupa, S.V., Kickert, R.N., 1989. The greenhouse effect: The impact of ultraviolet-B (UV-B) radiation, carbon dioxide (CO2) and ozone (O3) on vegetation. Environ. Pollution 61, 263±293. Lydon, J., Teramura, A.H., Summers, E.G., 1986. Effects of ultraviolet-B radiation on the growth and productivity of field grown soybean. In: Worrest, R.C., Caldwell, M.M. (Eds.), Stratospheric Ozone Reduction, Solar Ultraviolet Radiation and Plant Life. Springer, Berlin. Madronich, S., de Gruijl, 1994. Stratospheric ozone depletion between 1979 and 1992: Implications for biologically active ultraviolet-B radiation and non-melanoma skin cancer incidence. Photochem. Photobiol. 59, 541±546. Middleton, E.M., Teramura, A.H., 1994. Understanding photosynthesis, pigment and growth responses induced by UV-A irradiances. Photochem. Photobiol. 60, 38±45. Murali, N.S., Teramura, A.H., 1986. Effects of supplemental ultraviolet-B radiation on the growth and physiology of fieldgrown soybean. Environ. Exp. Botany 26(3), 233±242. Musil, C.F., Wand, S.J.E., 1993. Responses of Sclerophyllous ericaceae to enhanced levels of ultraviolet-B radiation. Environ. Exper. Botany 33(2), 233±242. Musil, C.F., Wand, S.J.E., 1994. Differential stimulation of an aridenvironment winter ephemeral Dimorphotheca pluvialis (L.) Moench by ultraviolet-B radiation under nutrient limitation. Plant, Cell and Environment 17, 245±255. Naidu, S.L., Sullivan, J.H., Teramura, A.H., DeLucia, E.H., 1993. The effects of ultraviolet-B radiation on photosynthesis of different needle age classes in field-grown loblolly pine. Tree Physiology 12, 151±162. Nedunchezhian, N., Kulandaivelu, G., 1991. Effect of UV-B enhanced radiation on Ribulose-1,5-biphosphate carboxylase in leaves of Vigna sinensis (L.). Photosynthetica 25, 431±435. Palmer, A.F.E., Heichel, G.H., Musgrave, R.B., 1973. Patterns of translocation, respiratory loss, and redistribution of 14C in maize labeled after flowering. Crop. Sci. 13, 371±376. Pfundel, E.E., Pan, R.S., Dilley, R.A., 1991. Inhibition of violoxanthin deepoxidation by ultraviolet-B radiation in
isolated chloroplasts and intact leaves. Plant Physiol. 98, 1372±1380. Poorter, H., 1989. Interspecific variation in RGR, In: Lambers, H., Cambridge, M.L., Konings, H., Pons, T.L. (Eds.), On Ecological Causes and Physiological Consequences ± Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB Academic Publishing, The Hague, Netherlands. Reed, H.E., Teramura, A.H., Kenworthy, W.J., 1992. Ancestral U.S. soybean cultivars characterized for tolerance to ultraviolet-B radiation. Crop Sci. 32, 1214±1219. Rowland, F.S., 1990. Stratospheric ozone depletion by chlorofluorocarbons. Ambio 19, 281±292. Rozema, J., Lenssen, G.M., van Staaij, J.W.M., 1990. The combined effect of increased atmospheric CO2 and UV-B radiation on some agricultural and salt marsh species. In: Goudriaan, J., van Keulen, H., van Laar, H.H. (Eds.), The Greenhouse Effect and Primary Productivity in European Agroecosystems. Pudoc, Wageningen, pp. 68±71. Runeckles, V.C., Krupa, S.V., 1994. The impact of UV-B radiation and ozone on terrestrial vegetation. Environ. Pollution 83, 191± 213. Santos, I., Almeida, J.M., Salema, R., 1993. Plants of Zea mays L. developed under enhanced UV-B radiation. I. Some ultrastructural and biochemical aspects. J. Plant Physiol. 141, 450± 456. Seckmeyer, G., Mayer, B., Erb, R., Bernhard, G., 1994. UV-B in Germany higher in 1993 than in 1992. Geophys. Res. Lett. 21, 577±580. Sisson, W.B., Caldwell, M.M., 1977. Atmospheric ozone depletion: Reduction of photosynthesis and growth of a sensitive higher plant exposed to enhanced UV-B radiation. J. Exp. Bot. 28, 691±705. Strid, A., Chow, W.S., Anderson, J.M., 1990. Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochimica et Biophysica Acta 1020, 260±268. Sullivan, J.H., Teramura, A.H., Ziska, L.H., 1992. Variation in UVB sensitivity in plants from a 3000 m elevational gradient in Hawaii. Amer. J. Botany 79, 737±743. Teramura, A.H., 1983. Effects of ultraviolet-B radiation on the growth and yield of crop plants. Physiol. Plant. 58, 415±427. Teramura, A.H., Murali, N.S., 1986. Intraspecific differences in growth and yield of soybean exposed to ultraviolet-B radiation under greenhouse and field conditions. Environ. Exp. Bottany 26, 89±95. Teramura, A.H., Sullivan, J.H., 1987. Soybean growth responses to enhanced levels of ultraviolet-B radiation under greenhouse conditions. Amer. J. Botany 74(7), 975±979. Tevini, M., Teramura, A.H., 1989. UV-B effects on terrestrial plants. Photochem. Photobiol. 50(4), 479±487. Tosserams, M., Rozema, J., 1995. Effects of ultraviolet-B radiation (UV-B) on growth and physiology of the dune grassland species Calamagrostis epigeios. Environ. Pollution 89, 209±214. van Staaij, J.W.M., Lenssen, G.M., Stroetenga, M., Rozema, J., 1993. The combined effect of elevated CO2 levels and UV-B radiation on growth characteristics of Elymus athericus. Vegetatio, 104/105, 433±439.
C.M. Correia et al. / Field Crops Research 59 (1998) 81±89 van Staaij, J.W.M., 1994. Enhanced solar ultraviolet-B radiation: Consequences for plant growth. Doctoral thesis, Vrije Universiteit Amsterdam, 130 pp. Yakimchuk, R., Hoddinott, J., 1994. The influence of ultraviolet-B light and carbon dioxide enrichment on the growth and physiology of seedlings of three conifer species. Can. J. For. Res. 24, 1±8.
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Ziska, L.H., Teramura, A.H., Sullivan, J.H., McCoy, A., 1993. Influence of ultraviolet-B (UV-B) radiation on photosynthetic and growth characteristics in field-grown Cassava (Manihot esculentum Crantz). Plant, Cell and Environment 16, 73±79. Grammatikopoulos et al., 1994.
Intraspeci®c variation in sensitivity to ultraviolet-B radiation in maize grown under ®eld conditions. I. Growth and morphological aspects Correia C.M.*, Areal E.L.V., Torres-Pereira M.S., Torres-Pereira J.M.G. Section of Biological and Environmental Engineering, University of TraÂs-os-Montes and Alto Douro, 5000 Vila Real, Portugal Received 23 December 1997; received in revised form 17 April 1998; accepted 25 April 1998
Abstract This study was conducted to determine the growth and morphological effects of UV-B on 8 cultivars of maize (Zea mays L.) in a Mediterranean climate. Dry weight, leaf area, leaf area duration (LAD), ear length, mean relative growth rate (RGR), and mean net assimilation rate (NAR) were signi®cantly reduced by UV-B treatment in some cultivars. Plant height and number of leaves were not affected. Changes in partitioning of biomass and premature leaf senescence were also recorded. Considerable variation in UV-B sensitivity exists within cultivars. DK 498 was the most sensitive and REG.VR the least sensitive. These genotypic differences suggest that future attempts at breeding for increased tolerance to UV-B radiation might be successful. # 1998 Elsevier Science B.V. All rights reserved. Keywords: UV-B radiation; Maize; Growth analysis; Sensitivity ranking
1. Introduction The stratospheric ozone layer constitutes a protective atmospheric ®lter against biologically harmful solar UV radiation. Anthropogenic emissions of chloro¯uorocarbons and nitrogen oxides result in depletion of the ozone layer (Rowland, 1990). As a consequence, increased levels of ultraviolet-B radiation have been measured in the Southern (Frederick et al., 1994) as well in the Northern Hemisphere (Seckmeyer et al., 1994) in both high and temperate latitudes (Madronich and de Gruijl, 1994). Although UV-B represents only a small part of the solar radiation reaching the surface of the earth, its
*Corresponding author. Fax: +351 593 20480; e-mail: [email protected] 0378-4290/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved. PII S0378-4290(98)00102-6
impact on the biological processes can be very important. Ultraviolet-B radiation is known to negatively in¯uence plant growth and development in higher plants (Caldwell, 1981; Teramura, 1983; Rozema et al., 1990; Runeckles and Krupa, 1994; Correia, 1995), although neutral and positive effects were also reported (Krupa and Kickert, 1989; Sullivan et al., 1992; Tosserams and Rozema, 1995). Since Zea mays L. is the third most important worldwide crop, after wheat and rice, and very few studies concerning its response to UV radiation have been done, it is of interest to gain information about its response to enhanced UV-B radiation. In the present study we examined such in¯uences on 8 cultivars of maize under ®eld growing conditions in the Mediterranean region. Our objectives were to characterize the range of growth and morphological responses to UV-B and elaborate a sensitivity ranking of maize cultivars.
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2. Material and methods This study was conducted at the University of TraÂsos-Montes and Alto Douro, Vila Real, Portugal (418 190 N, 78 440 W; 450 m elevation), between 25 June and 2 October 1996. The normal sowing date in this region of Northern Portugal is in the middle of May, but this was delayed by dif®culties associated with the experimental installation. The optimal harvest date extends to the middle of September because the rain season begins in early Autumn. For these reasons it was impossible to reach commercial maturation or even physiological maturation. Therefore, we present data from the biological yield only. A split-plot design was employed. The UV-B treatment was assigned to the mainplot and cultivar to the subplot. The experiment used 3 replicates. Five plants within each replicate were sampled for growth analysis. The experimental ®eld was divided into high UV-B treatment (UV) and ambient UV-B treatment, as a control (C). High UV-B treatment was supplied by preburned Philips sun lamps (TL 40 W/12), and began immediately after plants emerged. Radiation transmitted by the UV tubes was ®ltered using 0.1 mm cellulose acetate foil (Ultraphan, Weil am Rhein, Germany), which eliminates radiation below 290 nm. The ®lters were replaced twice a week to maintain uniform optical properties. Lamps were in frames that were adjusted weekly to a distance to provide a mean supplement of 0.65 wmÿ2 (unweighted) of UV-B radiation at plant apices for 8 h daily over the middle of the photoperiod. The difference betwen ambient and high UV-B levels was about 30%. For reference, the mean daily unweighted ambient UV-B levels in Portugal during clear days in mid summer are above 70 KJ mÿ2. The homogeneity of the UV-B irradiance was measured after sunset (i.e. in the absence of ambient UV-B radiation) with an IL 1400 A radiometer (International Light, Newburyport, USA) with a photodetector (SEL 240) calibrated according to the National Institute of Standards and Technology (USA). We used a constant lamp output throughout the daily treatment period, which may cause a UV-B enhancement in early morning and late afternoon. The coef®cient of variation in the UV-B/PAR ratio during the 8 h of photoperiod was 13%. If we consider only the 4 h around the solar noon, the coef®cient of variation was 3.4%. The
variation in UV-B irradiance received at plant apices resulting from variability in plant height was less than 10%. The UV-B treatment was suspended on cloudy days (16 days) to prevent abnormally high UV-B to PAR ratios. Non-burning UV-B lamps were used above the control treatment area to create shade, as in the UV-B radiated experimental groups. In this way, the visible light environment under control and UV-B frames was similar. Shading from the lamps and lamp supports was estimated with a ceptometer (Decagon Sun¯eck Ceptometer, Pullman, WA, USA). During a clear day, with maximum shading (i.e. with low zenith angle), the plant apices received about 90% of the photosynthetically active radiation (PAR) found above the frames. Obviously, less shading is expected with increasing zenith angle. With this system a small increase in UV-A radiation under the UV-B frames was observed. However, under the high PAR levels in the ®eld, the additional UV-A irradiances would be considered neutral in effect and their careful control unnecessary (Middleton and Teramura, 1994). Seeds of 8 cultivars of maize (Zea mays L.) were used (Table 1). Two of them were open-pollinated cultivars: REG.VR is a cultivar of upland habitat, grown near Vila Real; REG.VS is a cultivar of lowland habitat grown in the Entre Douro e Minho region, which has a genetic af®nity to the Portuguese hybrid Braga. The seed bed was prepared by conventional tillage. The treatments received 200 kg N haÿ1 as ammonium nitrate, 90 kg P2O5 haÿ1 as superphosphate and 180 kg K2O haÿ1 as potassium cloride. Half of the N and all of the P2O5 and K2O were applied broadcast and incorporated prior to sowing, and the remainder of the N was sidedressed as a band around 40±50 cm of the Table 1 Characteristics of maize cultivars (H-hybrid; OPC-open-pollinated) Cultivar
FAO Cycle
Type
Origin
Anjou 37 Teodora Avantage REG. VR DK 498 Braga Polo REG. VS
200 200 200 200 300 300 300 200
H H H OPC H H H OPC
France France Germany Portugal USA Portugal Germany Portugal
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plant height. Maize was oversown at a within-row spacing of 0.15 m spaced 0.75 m apart, and thinned to a ®nal density of 89000 plants haÿ1. Rainfall was supplemented with furrow irrigation as necessary to ensure that the crops did not suffer water stress. Weeds were controlled manually. At the end of the experiment, the plants were harvested and the following parameters were measured: leaf area (LICOR 3100, Lincoln, NE, USA), number of total green leaves, number of green leaves below the ear (NLBE), ear length, plant height and dry weight of each aboveground plant organ (after drying in a force-draft oven at 708C to a constant weight). Based on the data of leaf area and dry weight at the initial check (7 days after emergence) and ®nal harvest, the mean relative growth rate (RGR), mean net assimilation rate (NAR), leaf area ratio (LAR), speci®c leaf area (SLA), leaf weight ratio (LWR) and leaf area duration (LAD) were calculated using the equations shown in Hunt (1978). A UV-B sensitivity index (Lydon et al., 1986) was determined by adding the percentage changes in plant dry weight, plant height and leaf area (percentage change(control-treatment)/control100).
83
All data were analyzed by analysis of variance to test the main effects of UV-B radiation. Signi®cantly different means were separated using the LSD test. 3. Results Enhanced UV-B irradiation signi®cantly reduced many components of the growth and morphology of maize plants (Table 2). Across all cultivars, the UV-B treatment was found to reduce signi®cantly total aerial plant dry weight (p0.01), total leaf area (p0.029), the number of leaves below the ear (p0.052), the ear length (p0.022),the leaf size (p0.036) and LAD (p0.027). Plant height and the number of leaves were not signi®cantly affected by UV-B treatment. When the responses of cultivars were examined individually, only 3 cultivars (DK 498, Braga and REG.VS) exhibited signi®cant (p<0.1) reductions in the parameters measured. However, in general, behaviour was the same as in the other cultivars. Due to unequal variances among cultivars, treatment effects of a similar relative magnitude were not always similar in terms of the level of statistical signi®cance. Only
Fig. 1. Partition of dry matter at the harvest as affected by enhanced UV-B radiation. Numbers on treatments indicate different cultivars (the order is the same as descending order in Table 2).
UV C
UV C
UV C
UV C
UV C
UV C
UV C
UV C
UV C
Anjou 37
Teodora
Avantage
REG.VR
DK 498
Braga
Polo
REG.VS
Total
b
Significant at p0.1. Significant at p0.05.
a
Treatment
Cultivar
120.9 (30.6) 156.7 (35.2) ÿ22.8% 122.5 (8.4) 161.3 (26.1) ÿ24.0% 131.0 (19.8) 162.3 (3.2) ÿ19.3% 151.6 (17.4) 183.7 (5.9) ÿ17.4% 123.5 (5.3) 169.6 (18.6) ÿ27.2%a 118.2 (17.9) 169.6 (28.1) ÿ30.3%b 158.7 (6.7) 176.9 (11.2) ÿ10.3% 141.8 (13.2) 173.5 (3.9) ÿ18.3% 133.5 (5.8) 169.2 (6.2) ÿ21.1%b
Plant weight g plant-1 0.282 (0.003) 0.315 (0.003) ÿ10.4% 0.274 (0.002) 0.312 (0.002) ÿ12.1% 0.316 (0.003) 0.352 (0.002) ÿ10.2% 0.266 (0.001) 0.254 (0.002) 4.5% 0.357 (0.001) 0.447 (0.005) ÿ20.1%b 3.90 (0.004) 4.80 (0.006) ÿ18.6%b 0.365 (0.001) 0.406 (0.005) ÿ10.0% 0.255 (0.003) 0.349 (0.001) ÿ26.9%b 0.313 (0.012) 0.364 (0.018) ÿ14.0%b
Leaf area m2 plant-1 216.4 (2.3) 209.8 (10.6) 3.2% 222.9 (11.4) 221.3 (6.3) 0.8% 251.5 (11.8) 246.3 (11.9) 2.1% 216.3 (4.7) 203.5 (5.9) 6.3% 238.1 (7.1) 256.8 (8.7) ÿ7.3% 233.8 (19.2) 227.6 (18.1) 2.7% 258.7 (5.9) 249.0 (19.3) 3.9% 208.5 (6.0) 221.3 (6.7) ÿ5.8% 230.8 (4.6) 229.4 (5.2) 0.6%
Plant height cm 11.1 (0.1) 11.6 (0.2) ÿ4.5% 11.3 (0.5) 11.3 (0.3) 0% 10.9 (0.1) 11.3 (0.3) ÿ3.4% 10.7 (0.3) 9.7 (0.2) 10.0%a 12.0 (0.6) 12.7 (0.5) ÿ5.3% 13.2 (0.4) 13.2 (0.4) 0% 11.8 (0.4) 12.3 (0.7) ÿ4.5% 9.6 (0.3) 11.0 (0.5) ÿ12.6%b 11.3 (0.2) 11.6 (0.2) ÿ2.7%
Number of leaves 2.0 (0.1) 2.4 (0.1) ÿ17.2% 1.5 (0.4) 2.0 (0.1) ÿ25.0%a 1.7 (0.2) 1.6 (0.1) 1.7% 1.5 (0.1) 1.3 (0.2) 12.8% 1.7 (0.3) 2.2 (0.4) ÿ23.1%a 1.9 (0.4) 2.5 (0.2) ÿ24.2%b 1.9 (0.3) 2.5 (0.1) ÿ24.4% 1.7 (0.1) 1.8 (0.2) ÿ4.7% 1.7 (0.1) 2.0 (0.1) ÿ15.5%a
NLBE 17.1 (0.8) 17.9 (0.6) ÿ4.8% 17.9 (0.1) 19.3 (1.2) ÿ7.0% 20.4 (0.8) 21.7 (0.3) ÿ6.3% 17.3 (1.0) 19.3 (0.2) ÿ10.6%b 19.3 (0.4) 21.2 (0.4) ÿ8.8%a 19.6 (1.1) 20.7 (1.1) ÿ5.2% 22.4 (1.1) 21.4 (1.2) 4.4% 15.3 (0.7) 17.1 (0.6) ÿ10.3%a 18.7 (0.5) 19.8 (0.4) ÿ5.9%b
Ear length cm 254.2 (23.3) 271.0 (19.3) ÿ6.2% 243.8 (11.9) 278.6 (13.3) ÿ12.5% 289.3 (24.4) 310.6 (5.3) ÿ6.9% 250.4 (12.4) 260.7 (12.1) ÿ4.0% 298.8 (14.9) 352.2 (24.9) ÿ15.2%a 295.0 (19.3) 361.2 (40.4) ÿ18.3%b 311.0 (13.9) 327.4 (23.0) ÿ5.0% 262.7 (20.4) 316.5 (6.9) ÿ17.0% 275.6 (7.3) 309.8 (9.6) ÿ11.0%b
Leaf size cm2
0.291 (0.003) 0.320 (0.003) ÿ9.0% 0.284 (0.002) 0.318 (0.002) ÿ10.7% 0.321 (0.003) 0.353 (0.001) ÿ9.1% 0.274 (0.001) 0.263 (0.001) 4.3% 0.371 (0.001) 0.454 (0.004) ÿ18.2%b 0.402 (0.003) 0.482 (0.006) ÿ16.6%b 0.379 (0.001) 0.416 (0.005) ÿ9.0% 0.264 (0.003) 0.349 (0.001) ÿ24.4%b 0.323 (0.001) 0.369 (0.002) ÿ12.5%b
LAD m2 day
Table 2 Effects of UV-B radiation on several plant parameters of maize cultivars. Mean values with standard errors. The percentages indicate the changes in plants grown with enhanced UV-B compared to the control plants
84 C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
85
Table 3 Effects of UV-B radiation on growth analysis parameters. Mean values with standard errors. The percentages indicate the changes in plants grown with enhanced UV-B compared to the control plants Cultivar
Treatment
RGR mg g-1 day-1
Anjou 37
UV C
Teodora
UV C
Avantage
UV C
REG.VR
UV C
DK 498
UV C
Braga
UV C
Polo
UV C
REG.VS
UV C
Total
UV C
68.9 (2.8) 72.4 (2.6) ÿ4.8% 68.0 (0.7) 72.8 (3.2) ÿ6.6%b 68.5 (1.7) 71.4 (0.2) ÿ4.1% 74.9 (1.2) 76.1 (1.3) ÿ1.6% 63.9 (0.5) 66.9 (1.3) ÿ4.5% 63.2 (1.5) 66.8 (1.9) ÿ5.4% 68.5 (0.5) 69.5 (0.7) ÿ1.4% 70.4 (1.1) 73.1 (0.2) ÿ3.7% 68.3 (0.8) 71.1 (0.8) ÿ3.9%b
NAR g m-2 day-1 40.2 (6.7) 48.0 (7.3) ÿ16.1% 42.5 (0.7) 50.3 (6.0) ÿ15.5% 39.9 (3.0) 45.8 (2.5) ÿ12.9% 54.6 (5.0) 70.5 (4.7) ÿ22.6%c 33.0 (0.6) 36.7 (1.1) ÿ10.0% 28.9 (2.2) 34.2 (2.1) ÿ15.4% 41.8 (0.9) 42.6 (2.7) ÿ1.9% 54.1 (0.9) 49.6 (2.2) 9.2% 41.9 (2.0) 47.2 (2.5) ÿ11.3%b
LAR m2 kg-1 2.6 (0.4) 2.2 (0.3) 18.2%a 2.4 (0.1) 2.0 (0.3) 20.0% 2.6 (0.1) 2.3 (0.1) 13.0% 1.9 (0.2) 1.4 (0.1) 35.7%a 2.9 (0.1) 2.7 (0.1) 7.4% 3.4 (0.2) 3.0 (0.2) 13.3%a 2.4 (0.1) 2.3 (0.2) 4.3% 1.9 (0.1) 2.1 (0.1) ÿ9.5% 2.5 (0.1) 2.2 (0.1) 13.6%c
LWR g kg-1 190.0 (15.1) 172.5 (15.6) 10.1% 165.5 (6.9) 156.3 (7.0) 5.9% 188.8 (6.8) 180.6 (5.0) 4.5% 139.0 (9.6) 115.4 (5.8) 20.5%a 206.8 (1.4) 194.7 (0.8) 6.2% 233.5 (11.7) 203.2 (9.6) 14.9%b 174.5 (5.6) 173.2 (12.4) 0.8% 146.9 (11.1) 154.4 (5.3) ÿ4.9% 180.6 (6.7) 168.8 (5.9) 7.0%
SLA m2 kg-1 13.4 (1.0) 12.4 (0.7) 8.1% 14.3 (0.6) 12.9 (1.0) 10.9%a 13.5 (0.7) 12.3 (0.5) 9.8% 13.4 (0.6) 12.3 (0.5) 8.9% 14.2 (0.1) 13.9 (0.4) 2.2% 14.9 (1.2) 14.8 (0.4) 0.7% 13.6 (0.7) 13.4 (0.1) 1.5% 13.1 (0.3) 13.3 (0.4) ÿ1.5% 13.8 (0.2) 13.2 (0.2) 4.5%
a
Significant at p0.1. Significant at p0.05. c Significant at p0.01. b
REG.VR and Polo, particularly the ®rst, exhibited signi®cant increase (p<0.1) in some growth parameters in response to UV-B radiation. Almost all cultivars showed reductions in leaf weight, stem weight (stem tassels) and ear weight (data not shown). Although cultivar differences existed in response to UV-B radiation, reductions in total dry weight were accompanied by changes in the partitioning of the biomass into component organs. In UV-B-treated plants a greater proportion of biomass was partitioned to leaves and stems, namely, in REG.VR, DK 498 and Braga, and a lesser proportion to ears (Fig. 1). This could decrease the harvest index of these cultivars. Growth analysis also revealed signi®cant reductions in RGR and NAR, but at the same time, a noticeable
increase in LAR in UV treated plants due to increase in LWR and SLA, although this was not statistically signi®cant (Table 3). Signi®cant correlations were found between plant dry weight and plant parameters, but some differences were observed between treatments (Table 4). In UVB-treated plants, plant dry weight is affected primarily by NAR and to a lesser extent by plant height and leaf area, indicating that some positive relationships exist between physiological and morphological sensitivity to UV-B and biomass reductions. In the control plants the importance of NAR and plant height is decreased, but the importance of leaf area is increased. LAD and ear length also had signi®cant positive correlations with dry weight. Speci®c leaf area was negatively correlated with biological yield, especially in UV-B
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Table 4 Correlation analysis between several plant parameters and total plant dry weight Parameter
UV
C
Leaf area Plant height Ear length NAR LAD SLA
0.362a 0.406a 0.322 0.659c 0.326 ÿ0.741c
0.426b 0.352a 0.384a 0.453b 0.402a ÿ0.366a
a
Significant at p0.1. Significant at p0.05. c Significant at p0.001. b
treated plants, which indicates that leaf thickness per se has an important relationship with radiation use ef®ciency. Relative sensitivities of the cultivars varied according to which response variable was used in the ranking but were consistently most or least affected by the UVB in terms of dry matter production, plant height and leaf area (Barnes et al., 1993). The cultivars REG.VR and Polo were the least affected by UV-B whereas, DK 498, Braga and REG.VS were the most affected. The calculated UV-B sensitivity index (SI) ranged from ÿ6.6 for the least affected cultivar (REG.VR) to ÿ54.6 for the most affected (DK 498)(Table 5). Using this combined response, cultivars with an SI greater than ÿ20 were arbitrarily classi®ed as insensitive while those with an index value of less than ÿ40 were considered as sensitive. Cultivars with sensitivity Table 5 Ranking of the maize cultivars with respect to a UV-B sensitivity index. The sensitivity index was determined by adding the percentage changes in plant dry weight, plant height and leaf area Cultivar Insensitive REG.VR Polo Intermediate Avantage Anjou 37 Teodora Sensitive Braga REG.VS DK 498
Sensitivity index ÿ6.6 ÿ16.4 ÿ27.4 ÿ30.0 ÿ35.3 ÿ46.2 ÿ51.0 ÿ54.6
indices between ÿ20 and ÿ40 were considered to be of intermediate sensitivity. 4. Discussion Ultraviolet-B radiation had a signi®cant inhibitory effect on the growth and biological yield of several of the maize cultivars used in this study. This agrees with other works (Santos et al., 1993; van Staaij, 1994; Correia, 1995) where maize was found to be sensitive to UV-B. However, considerable variation in UV-B sensitivity exists between maize cultivars. These responses showed both similarities to and differences from what has been described for other species, both cultivated (Biggs et al., 1981; Teramura and Murali, 1986; Reed et al., 1992; Barnes et al., 1993) and native taxa (Caldwell et al., 1982; Sullivan et al., 1992). Reduction in plant dry weight may be explained by alterations in morphological and physiological processes. Decreases in leaf area, leaf area duration, ear length and, namely, in net assimilation rate, contribute to lower biomass accumulation in UV-B-treated plants. Thus, lower biological yields result from both inferior source and sink capacities. Decrease in RGR and NAR suggest that the growth reduction of the plants exposed to UV-B radiation was mainly due to the reduction in the ef®ciency of dry matter production per unit of leaf area, namely, net photosynthetic rate. Several researchers have reported that the exposure to UV-B radiation caused a reduction in the net photosynthetic rate of crop plants (Teramura, 1983; Strid et al., 1990; Ziska et al., 1993; Correia, 1995). This reduction may be closely related to the inhibition of photosynthetic electron transport, the inhibition of photosynthetic enzymes, increases in stomatal and mesophyll resistance and ultrastructural changes in chloroplasts (Brandle et al., 1977; Pfundel et al., 1991; Nedunchezhian and Kulandaivelu, 1991; Jordan et al., 1992; Eichhorn et al., 1993; Musil and Wand, 1993; Grammatikopoulos et al., 1994; He et al., 1994). Maize UV plants may compensate for a lower NAR by increasing LAR, which suggests changes in the structural characteristics of the plants. A bigger LAR represents a greater investment of photosynthates in leaf area than in plant biomass and is due to an increase of LWR and SLA, which indicates larger biomass partition leaves and altered leaf morphology,
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respectively. The general trend towards increased SLA under UV-B treatment indicates that UV-B radiation decreases leaf thickness, as reported in other studies (van Staaij et al., 1993; Santos et al., 1993; Musil and Wand, 1994). This decrease may be important in plant dry weight reduction because decreased photosynthesis rates have been correlated with an increase in SLA, contributing to lower RGRs (Poorter, 1989). Plant height did not change after 3 months of UV-B treatment. This is in agreement with some reports (Cen and Bornman, 1990; van Staaij, 1994; Correia, 1995), but contradicts other studies (Tevini and Teramura, 1989; Krizek et al., 1993; Yakimchuk and Hoddinott, 1994). However, caution is needed in interpreting these results, because height differences may occur at one phenological stage but not at another. In a previous report (Correia, 1995) and in this study (data not shown) we have seen signi®cant differences in plant height at the vegetative stage but no differences were observed at the reproductive or maturation stage. The greater sensitivity at the early development stage to UV-B radiation has also been reported in some studies (Murali and Teramura, 1986; Naidu et al., 1993; Musil and Wand, 1994) and is attributed to lower concentrations of UV-B-absorbing compounds in young leaves (Teramura, 1983). Such growth reduction may potentially allow repair mechanisms such as photoreactivation and excision repair to be more effective in ameliorating UV-induced damage (Teramura and Sullivan, 1987). The decrease in the number of green leaves below the ear in UV-B plants indicates an early senescence of older foliage, also observed by other researchers (Sisson and Caldwell, 1977; Teramura and Sullivan, 1987; Naidu et al., 1993). Premature leaf senescence would alter the canopy carbon gain and nutrient relations. In fact, when the activity of lower leaves decreased, the supply of carbohydrates to the roots was limited (Palmer et al., 1973; Fairey and Daynard, 1978) and so root activity was reduced. Accordingly, absorption of nutrients, namely, nitrogen, was reduced too. As a consequence, increase in the decomposition of the nitrogen compounds of leaves and the photosynthetic rate was depressed. For these reasons leaf senescence may indirectly alter biomass production. Our study did not reveal any association between cultivar sensitivity and the geographic origin of the seed, as in the study of Barnes et al. (1993). Sensitivity
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was the same between hybrids and open-pollinated cultivars, despite REG.VR being the most tolerant cultivar. REG.VR is the most tolerant cultivar in this study because, with regard to both leaf area and plant height parameters, performance was increased by UVB treatment. On the other hand, DK 498 and REG.VS are the most sensitive cultivars because the response of the 3 parameters used in the ranking changed in the same direction. In almost all cultivars, plant height responses minimize the effects of UV-B radiation. The evidence of signi®cant variation in UV-B sensitivity among maize cultivars is due to inherent genotypic differences and suggests that future efforts at breeding for increased tolerance to UV-B radiation might be possible. As maize is the third major crop in the world more ®eld studies are needed in order to elucidate which mechanisms are involved in the observed growth reductions due to enhanced UV-B radiation and also what can be done to minimize these negative effects.
References Barnes, P.W., Maggard, S., Holman, S.R., Vergara, B.S., 1993. Intraspecific variation in sensitivity to UV-B radiation in rice. Crop Sci. 33(5), 1041±1046. Biggs, R.H., Kossuth, S.V., Teramura, A.H., 1981. Response of 19 cultivars of soybeans to ultraviolet-B irradiance. Physiol. Plant. 53, 19±26. Brandle, J.R., Campbell, W.F., Sisson, W.B., Caldwell, M.M., 1977. Net photosynthesis, electron transport capacity and ultrastructure of Pisum sativum L. exposed to ultraviolet-B radiation. Plant Physiol. 60, 165±168. Caldwell, M.M., 1981. Physiological plant ecology I ± Responses to the physical environment, plant response to solar ultraviolet radiation. In: Encyclopedia of Plant Physiology, New Series, vol. 12 A. Springer, Berlin, pp. 169±197. Caldwell, M.M., Robberecht, R., Nowak, R.S., Billings, W.D., 1982. Differential photosynthetic inhibition by ultraviolet radiation in species from the Arctic±Alpine life zone. Arc. Alp. Res. 14, 195±202. Cen, Y.P., Bornman, J.F., 1990. The response of bean plants to UVB radiation under different irradiances of background visible light. J. Exp. Botany 41, 1489±1495. Correia, C.M., 1995. ConsequeÃncias do Aumento dos NõÂveis de Radiac,aÄo Ultravioleta-B na Produtividade AgrõÂcola. Estudos em Zea mays L. cv. LG5. Master thesis, UTAD, Vila Real, 98 pp. Eichhorn, M., Dohler, G., Augsten, H., 1993. Impact of UV-B radiation on photosynthetic electron transport of Wolffia arrhiza (L.) Wimm.. Photosynthetica 29(4), 613±618.
88
C.M. Correia et al. / Field Crops Research 59 (1998) 81±89
Fairey, N.A., Daynard, T.B., 1978. Assimilate distribution and utilization in maize. Can. J. Plant Sci. 58, 719±730. Frederick, J.E., Diaz, S.B., Smolskaia, J., Esposito, W., Lucas, T., Booth, C.R., 1994. Ultraviolet solar radiation in the high latitudes of South America. Photochem. Photobiol. 60, 362± 365. He, J., Huang, L.K., Whitecross, M.I., 1994. Chloroplast ultrastructure changes in Pisum sativum associated with supplementary ultraviolet (UV-B) radiation. Plant, Cell and Environment 17, 771±775. Hunt, R., 1978. Growth analysis of individual plants. In: Arnold, E. (Ed.), Plant Growth Analysis. London. Jordan, B.R., He, J., Chow, W.S., Anderson, J.M., 1992. Changes in mRNA levels and polypeptide subunits of Ribulose-1,5bisphosphate carboxylase in response to supplementary ultraviolet-B radiation. Plant, Cell and Environment 15, 91±98. Krizek, D.T., Kramer, G.F., Upadhyaya, A., Mirecki, R.M., 1993. UV-B response of cucumber seedlings grown under metal halide and high pressure sodium/deluxe lamps. Physiol. Plant. 88, 350±358. Krupa, S.V., Kickert, R.N., 1989. The greenhouse effect: The impact of ultraviolet-B (UV-B) radiation, carbon dioxide (CO2) and ozone (O3) on vegetation. Environ. Pollution 61, 263±293. Lydon, J., Teramura, A.H., Summers, E.G., 1986. Effects of ultraviolet-B radiation on the growth and productivity of field grown soybean. In: Worrest, R.C., Caldwell, M.M. (Eds.), Stratospheric Ozone Reduction, Solar Ultraviolet Radiation and Plant Life. Springer, Berlin. Madronich, S., de Gruijl, 1994. Stratospheric ozone depletion between 1979 and 1992: Implications for biologically active ultraviolet-B radiation and non-melanoma skin cancer incidence. Photochem. Photobiol. 59, 541±546. Middleton, E.M., Teramura, A.H., 1994. Understanding photosynthesis, pigment and growth responses induced by UV-A irradiances. Photochem. Photobiol. 60, 38±45. Murali, N.S., Teramura, A.H., 1986. Effects of supplemental ultraviolet-B radiation on the growth and physiology of fieldgrown soybean. Environ. Exp. Botany 26(3), 233±242. Musil, C.F., Wand, S.J.E., 1993. Responses of Sclerophyllous ericaceae to enhanced levels of ultraviolet-B radiation. Environ. Exper. Botany 33(2), 233±242. Musil, C.F., Wand, S.J.E., 1994. Differential stimulation of an aridenvironment winter ephemeral Dimorphotheca pluvialis (L.) Moench by ultraviolet-B radiation under nutrient limitation. Plant, Cell and Environment 17, 245±255. Naidu, S.L., Sullivan, J.H., Teramura, A.H., DeLucia, E.H., 1993. The effects of ultraviolet-B radiation on photosynthesis of different needle age classes in field-grown loblolly pine. Tree Physiology 12, 151±162. Nedunchezhian, N., Kulandaivelu, G., 1991. Effect of UV-B enhanced radiation on Ribulose-1,5-biphosphate carboxylase in leaves of Vigna sinensis (L.). Photosynthetica 25, 431±435. Palmer, A.F.E., Heichel, G.H., Musgrave, R.B., 1973. Patterns of translocation, respiratory loss, and redistribution of 14C in maize labeled after flowering. Crop. Sci. 13, 371±376. Pfundel, E.E., Pan, R.S., Dilley, R.A., 1991. Inhibition of violoxanthin deepoxidation by ultraviolet-B radiation in
isolated chloroplasts and intact leaves. Plant Physiol. 98, 1372±1380. Poorter, H., 1989. Interspecific variation in RGR, In: Lambers, H., Cambridge, M.L., Konings, H., Pons, T.L. (Eds.), On Ecological Causes and Physiological Consequences ± Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB Academic Publishing, The Hague, Netherlands. Reed, H.E., Teramura, A.H., Kenworthy, W.J., 1992. Ancestral U.S. soybean cultivars characterized for tolerance to ultraviolet-B radiation. Crop Sci. 32, 1214±1219. Rowland, F.S., 1990. Stratospheric ozone depletion by chlorofluorocarbons. Ambio 19, 281±292. Rozema, J., Lenssen, G.M., van Staaij, J.W.M., 1990. The combined effect of increased atmospheric CO2 and UV-B radiation on some agricultural and salt marsh species. In: Goudriaan, J., van Keulen, H., van Laar, H.H. (Eds.), The Greenhouse Effect and Primary Productivity in European Agroecosystems. Pudoc, Wageningen, pp. 68±71. Runeckles, V.C., Krupa, S.V., 1994. The impact of UV-B radiation and ozone on terrestrial vegetation. Environ. Pollution 83, 191± 213. Santos, I., Almeida, J.M., Salema, R., 1993. Plants of Zea mays L. developed under enhanced UV-B radiation. I. Some ultrastructural and biochemical aspects. J. Plant Physiol. 141, 450± 456. Seckmeyer, G., Mayer, B., Erb, R., Bernhard, G., 1994. UV-B in Germany higher in 1993 than in 1992. Geophys. Res. Lett. 21, 577±580. Sisson, W.B., Caldwell, M.M., 1977. Atmospheric ozone depletion: Reduction of photosynthesis and growth of a sensitive higher plant exposed to enhanced UV-B radiation. J. Exp. Bot. 28, 691±705. Strid, A., Chow, W.S., Anderson, J.M., 1990. Effects of supplementary ultraviolet-B radiation on photosynthesis in Pisum sativum. Biochimica et Biophysica Acta 1020, 260±268. Sullivan, J.H., Teramura, A.H., Ziska, L.H., 1992. Variation in UVB sensitivity in plants from a 3000 m elevational gradient in Hawaii. Amer. J. Botany 79, 737±743. Teramura, A.H., 1983. Effects of ultraviolet-B radiation on the growth and yield of crop plants. Physiol. Plant. 58, 415±427. Teramura, A.H., Murali, N.S., 1986. Intraspecific differences in growth and yield of soybean exposed to ultraviolet-B radiation under greenhouse and field conditions. Environ. Exp. Bottany 26, 89±95. Teramura, A.H., Sullivan, J.H., 1987. Soybean growth responses to enhanced levels of ultraviolet-B radiation under greenhouse conditions. Amer. J. Botany 74(7), 975±979. Tevini, M., Teramura, A.H., 1989. UV-B effects on terrestrial plants. Photochem. Photobiol. 50(4), 479±487. Tosserams, M., Rozema, J., 1995. Effects of ultraviolet-B radiation (UV-B) on growth and physiology of the dune grassland species Calamagrostis epigeios. Environ. Pollution 89, 209±214. van Staaij, J.W.M., Lenssen, G.M., Stroetenga, M., Rozema, J., 1993. The combined effect of elevated CO2 levels and UV-B radiation on growth characteristics of Elymus athericus. Vegetatio, 104/105, 433±439.
C.M. Correia et al. / Field Crops Research 59 (1998) 81±89 van Staaij, J.W.M., 1994. Enhanced solar ultraviolet-B radiation: Consequences for plant growth. Doctoral thesis, Vrije Universiteit Amsterdam, 130 pp. Yakimchuk, R., Hoddinott, J., 1994. The influence of ultraviolet-B light and carbon dioxide enrichment on the growth and physiology of seedlings of three conifer species. Can. J. For. Res. 24, 1±8.
89
Ziska, L.H., Teramura, A.H., Sullivan, J.H., McCoy, A., 1993. Influence of ultraviolet-B (UV-B) radiation on photosynthetic and growth characteristics in field-grown Cassava (Manihot esculentum Crantz). Plant, Cell and Environment 16, 73±79. Grammatikopoulos et al., 1994.