Quantifying the Effects of Corn Growth and ... - Semantic Scholar
Biometry, Modeling & Statistics
Quantifying the Effects of Corn Growth and Physiological Responses to Ultraviolet-B Radiation for Modeling K. Raja Reddy,* Shardendu K. Singh, Sailaja Koti, V. G. Kakani, Duli Zhao, Wei Gao, and V. R. Reddy ABSTRACT
To understand the consequences of rising levels of ultraviolet-B (UV-B) radiation on corn (Zea mays L.), two experiments were conducted using sunlit growth chambers at a wide range of UV-B radiation levels. Corn hybrids, Terral-2100 and DKC 65-44, were grown in 2003 and 2008, respectively, at four UV-B levels (0, 5, 10, and 15 kJ m–2 d–1) at 30/22°C, from 4 d after emergence to 43 d under optimum nutrient and water conditions. Plant growth, development, and photosynthetic rates were measured regularly. An inverse relationship between many growth process and dosage of UV-B radiation was recorded. Shorter plants were due to shorter internodal lengths rather than fewer internodes and the total leaf area was less due to smaller leaves. Lower biomass under enhanced UV-B was closely related to smaller leaf area and lower photosynthesis. Critical UV-B limits, defined as 90% of optimum or control, were estimated from the UV-B response indices. The critical limits for stem extension and leaf area expansion were lower in both hybrids (1.7–3.5 kJ m–2 d–1) than the critical limit for leaf number (>15 kJ m–2 d–1) and photosynthetic processes, indicating that expansion or extension rates of organs were the more sensitive to UV-B radiation. Hybrid Terral-2100 exhibited greater sensitivity to UV-B radiation than DKC 65-44 for studied parameters. Thus, both current and projected UV-B radiation can adversely affect corn growth. The functional algorithms developed in this study could be useful to enhance the corn models to predict accurately field performance.
U
ltraviolet-B radiation (280–320 nm) is an integral part of sunlight that reaches the surface of Earth. Even though UV-B represents a small fraction of total solar radiation, exposure to UV-B at current and projected levels is known to elicit a variety of responses in all living organisms, including higher plants (Kakani et al., 2003; Runeckles and Krupa, 1994). Over the past 50 yr, the concentration of ozone in the stratosphere, which absorbs most of the UV-B radiation, has decreased about 5%, mainly due to release of anthropogenic pollutants such as chloroflurocarbons (Pyle, 1996). Current global distribution of mean erythemal (biologically effective/ potential for biological damage) daily dose of UV-B radiation between the latitudes 40°N and 40°S during summer ranges between 2 and 9 kJ m–2 (McKenzie et al., 2007), a level which is about 3 kJ m–2 higher than the 1994 observation (Seckmeyer et al., 1995). Elevated UV-B levels are expected to continue well into the 21st century (WMO, 2007). Model simulations
K.R. Reddy, Dep. of Plant and Soil Sciences, 117 Dorman Hall, Box 9555, Mississippi State Univ., Mississippi State, MS 39762; S.K. Singh, and V.R. Reddy, Crop Systems and Global Change Lab., USDA-ARS, Beltsville, MD 20705; S. Koti, RiceTec, Inc., P.O. Box 1305, Alvin, TX 77512; V.G. Kakani, Dep. of Plant and Soil Sciences, Oklahoma State Univ., Stillwater, OK 74078; Duli Zhao, USDA-ARS, Sugarcane Field Station, 12990 U.S. HWY 441, Canal Point, FL 33438; W. Gao, USDA-UV-B Monitoring Network, Natural Resource Ecology Lab., Colorado State Univ., Fort Collins, CO 80523. Received 5 Mar. 2013. *Corresponding author ([email protected]). Published in Agron. J. 105:1367–1377 (2013) doi:10.2134/agronj2013.0113 Copyright © 2013 by the American Society of Agronomy, 5585 Guilford Road, Madison, WI 53711. All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
suggest that the United States is already experiencing UV-B dosage that may be deleterious to crop growth and development (Lubin and Jensen, 1995). Recent estimates have shown that continued increase in ground-level UV-B radiation will occur over the next few decades, although there is considerable uncertainty between changes projected in atmospheric chemistry and associated changes in climate and their interactions (Taalas et al., 2000; Zerefos et al., 1997). Previous reviews and published studies clearly demonstrate the extent of damage caused by both ambient (Caldwell et al., 1989; Teramura, 1983; Teramura and Sullivan, 1994) and elevated UV-B radiation (Kakani et al., 2003; Krupa, 1998; Rozema et al., 1997; Searles et al., 2001; Teramura, 1983) on morphological, physiological, biochemical, and molecular components of crop plants including corn. Some of the primary effects of UV-B radiation on plant metabolic systems are DNA damage, dilation, and disintegration of cellular membranes, photooxidation of leaf pigments and phytohormones, and inhibition of photosynthesis (Correia et al., 1999; He et al., 1994; Mark and Tevini, 1997; Ros and Tevini, 1995) in association with down-regulation of genes responsible for processes such as photosynthesis and phytohormone metabolism and cell wall loosening (Casati and Walbot, 2003; Hectors et al.,
Abbreviations: fCO2 , the apparent quantum yield of CO2 assimilation; fPSII, the fraction of absorbed photon that are used for photochemistry for a light adapted leaf; BIO, aboveground biomass; Ci, internal CO2 concentration; DAE, days after emergence; Fv’/Fm’, efficiency of energy harvesting by oxidized (open) PSII reaction centers in light; g s, stomatal conductance; LA, leaf area; LFWt, leaf dry weight; LN, mainstem leaf number; PH, plant height; PSII, photosystem-II; Pn, rate of photosynthesis; qN, non-photochemical quenching; SPAR, Soil–Plant Atmosphere Research; STWt, stem dry weight; Tr, transpiration; UV-B, ultraviolet-B; WUE, instantaneous water use efficiency (Pn/Tr).
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2007). These primary effects result in numerous secondary and tertiary effects causing altered crop growth and development, reduced fruit numbers and retention, and finally, biomass and yield reductions (Kakani et al., 2003). Ultraviolet-B radiation has a large photobiological effect as it is readily absorbed by biomolecules such as amino acids, pigments, and nucleic acids (Caldwell and Flint, 1994; Sullivan and Teramura, 1989). Several studies were performed on UV-B effects on growth and physiological responses on many field crops such as bean (Phaseolus vulgaris L., Deckmyn et al., 1994), cotton (Gossypium hirsutum L., Kakani et al., 2004; Reddy et al., 2003, 2004), corn (Correia et al., 1998, 1999; Gao et al., 2004; Mark and Tevini, 1996), pea (Pisum sativum L., Day et al., 1996; Mepsted et al., 1996), rice (Oryza sativa L., Dai et al., 1992; Teramura et al., 1990), soybean [Glycine max (L.) Merr., Miller et al., 1994; Sinclair et al., 1990], sunflower (Helianthus annuus L., Battaglia and Brennen, 2000), cowpea [Vigna unguiculata (L.) Walp., Singh et al., 2008], and wheat (Triticum aestivum L., Yuan et al., 2000; Teramura et al., 1990). Several reviews have recently summarized the effects and consequences of UV-B radiation on major agricultural and non-agricultural plant species (Allen, 1994; Caldwell et al., 1998; Frohnmeyer and Staiger, 2003; Kakani et al., 2003; Krupa and Kickert, 1989; Teramura and Sullivan, 1994). The inferences from these studies and reviews are that plant sensitivities to UV-B radiation differ among species and hybrids within a species. Even though several studies addressed UV-B effects on corn growth, little is known about the quantitative dose response functions for developing algorithms for models on corn. It is important to better understand UV-B radiation effects on corn because of its major economic importance worldwide (FAO, 2011). Plant growth and development play a pivotal role in crop production systems. The vegetative growth and developmental processes such as production of new leaves, leaf expansion, and extension of internodes are the major determinants of crop biomass production. Any factor (biotic or abiotic) that affects these crop growth and developmental processes will have profound influence on the interception of photosynthetically active radiation (PAR) during the production season. Therefore, it is useful to understand factors that control plant growth and development and to quantify the responses so that suitable management practices can be devised to optimize production. Quantification of these responses of crop growth and physiological processes to broad ranges of abiotic factors such as UV-B radiation is also a key for developing process-based crop simulation models to be used for predicting crop and agricultural systems responses to changes in climate. Corn and all other crops cultivated between 40°N and 40°S latitudes are already experiencing UV-B dosage of 2 to 10 kJ m–2 d–1 depending on location and season (Gao et al., 2004; McKenzie et al., 2007). Corn is sensitive to both ambient and elevated UV-B radiations with noticeable intraspecific variability (Correia et al., 1998, 1999; Gao et al., 2004; Mark and Tevini, 1996). It is hypothesized that both the current levels and the projected increases in UV-B radiation can alter corn growth and development. An understanding of the effects of solar UV-B radiation on corn hybrids would provide information about the causes of changes in growth, development, and physiology and how these changes vary between hybrids. 1368
Therefore, the objectives of this study were to determine the growth, development, and physiological responses of two corn hybrids to UV-B radiation and to quantify and develop UV-B radiation-specific functional algorithms, which can be used in corn simulation models. MATERIALS AND METHODS Soil–Plant Atmosphere Research Units This study was conducted in sunlit Soil–Plant Atmosphere Research (SPAR) chambers located at the RR Foil Plant Science Research facility of Mississippi State University, (33°28¢ N, 88°47¢ W), Mississippi State, MS, in 2003 and 2008. Each SPAR chamber consists of a steel soil bin (1-m deep by 2 m long by 0.5 m wide) to accommodate the root system, and a Plexiglas chamber (2.5 m tall by 2.0 m long by 1.5 m wide) to accommodate aerial plant parts, a heating and cooling system, and an environmental monitoring and control system. The Plexiglas transmits 97% of the visible solar radiation to pass without spectral variability in absorption and is opaque to solar UV-B radiation (280–320 nm), but transmits 12% of UV-A radiation (wavelength 320–400 nm; Zhao et al., 2003). To avoid the effect of germicidal effects of UV-C radiation ( 0.05. ns, not significant.
Fig. 2. Changes in plant height of corn as affected by ultraviolet-B radiation. Each data point is a mean of nine individual plants and standard errors of the mean are shown when larger than the symbols.
Photosynthesis and Fluorescence Measurements These measurements were made on the upper most fully expanded leaves (24 DAE and 31 DAE, Terral-2100; and 23 DAE and 40 DAE, DKC 65-44) between 1000 and 1300 h from three individual plants per treatment using a LI-6400 (LI6400 photosynthesis meter, LI-COR Inc., Lincoln, NE) with an integrated fluorescence chamber head (LI-COR 6400-40 Leaf Chamber Fluorometer; LI-Cor Inc.). The temperature in leaf cuvette was set to the day time chamber air temperature (30°C) and [CO2] was controlled by the CO2 injection system to match the [CO2] treatments. The PAR provided by a 6400-02 LED light source was set to 1500 µmol m–2 s–1. Relative humidity inside the cuvette was maintained at approximately 50%. To measure fluorescence, the built-in leaf chamber fluorometer was used which uses two red LEDs (center wavelength about 630 nm) and a detector (sees radiation at 715 nm in the PSII fluorescence band). A flash light (>7000 µmol m–2 s–1) achieved by using 27 red LEDs was used to measure the maximal fluorescence (Fm’). Rapid dark adaptation to measure minimal fluorescence (Fo’) was achieved by turning off the actinic light while using the far red LED (center wavelength at 740 nm). The far red radiation drives photosystem-I (PSI) momentarily to help drain PSII of electrons. The software in the instrument provides data on the fluorescence parameters and also calculated parameters such as PSII reactions centers under light (Fv’/Fm’), PSII efficiency (fPSII), quantum yield from gas exchange, and nonphotochemical quenching (qN) (LI-6400 Instruction Manual, version 5, LI-Cor Inc., Lincoln, NE).
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Ultraviolet-B Radiation Indices and Critical Ultraviolet-B Limits Regression analysis (SAS Institute, 2008) was used as an exploratory tool to obtain the overall measure of UV-B sensitivity for understanding the growth and physiological responses of corn hybrids to UV-B. To test the significance of the relationship between measured parameters and dosage of UV-B radiation, a significance level of 0.05 (P = 0.05) was used. To obtain UV-B indices, the measured values from each parameter were normalized to obtain the slopes in response to UV-B radiation. The estimated values at 0 kJ m–2 d–1 UV-B were used as a denominator so that the derived values range between a relative scale of 0 to 1 as described by Reddy et al. (2003, 2008). Critical limits of UV-B were calculated from the developed algorithms as 90% of the optimum or control. Analysis of Data The statistical analysis was conducted separately for each hybrid using ANOVA procedure of SAS (SAS Institute, 2008). The least significant difference (LSD) tests at P = 0.05 were employed to distinguish among treatments for the growth and physiological parameters measured in the study. The standard errors of each mean were also calculated and presented in the figures as error bars. RESULTS Ultraviolet-B radiation treatments were very close to the set points and did not differ significantly between both years (Fig. 1). Plant Height Plant height increased exponentially as plants aged for both hybrids (Fig. 2) and differed significantly over time within a UV-B treatment and among UV-B treatments (Table 1). The UV-B radiation caused significant decrease in PH with maximum decrease for both the hybrids at 15 kJ m–2 d–1. By the end of experiments, plants grown under control (without UV-B radiation) were 163 cm (Terral-2100) and 158 cm (DKC 65-44) tall. In comparison to the control, UV-B treatments Agronomy Journal • Volume 105, Issue 5 • 2013
Fig. 3. Changes in (A and C) leaf number and (B and D) leaf area of corn as affected by ultraviolet-B radiation. Each data point is a mean of nine individual plants and standard errors of the mean are shown when larger than the symbols.
of 5, 10, and 15 kJ m–2 d–1, decreased plant height by 35, 47, and 66% for Terral-2100, and 17, 23, and 41% for DKC 65-44, respectively. Mainstem Nodes Unlike the PH, adding leaves on the main stem increased linearly as the plants aged irrespective of UV-B treatments for both hybrids (Fig. 3A, 3C). The mainstem leaf number exhibited a significant DAE X UV-B interaction only for Terral-2100. Although, leaf number differed significantly over time and among UV-B levels (Table 1), the final count of the leaf numbers were not statistically different. The days to produce one leaf, calculated as the inverse of the slope over time, did not differ among the three lowest UV-B treatments (0, 5, and 10 kJ m–2 d–1) for Terral-2100. It took about 2.3 d (slope 2.344) for the plants grown at 0, 5, and 10 kJ m–2 d–1 of UV-B, while the plants grown under the 15 kJ m–2 d–1 UV-B treatment took 2.6 d (slope 2.481) to produce a leaf. The average count of the mainstem leaves produced were 16 and 14 leaves for Terral-2100 and DKC 65-44, respectively. Leaf Area Development Total leaf area of the plants in both experiments followed similar trends to that of PH across all UV-B treatments (Fig. 3B, 3D), and differed significantly over time and among UV-B levels (Table 1). In general, the reductions in LA development were slightly lower than the reductions in PH across all UV-B levels tested. Final leaf size, the product of the duration of expansion and rate of leaf growth, increased as nodal position up the plant increased to node 8 in all UV-B treatments. Final leaf size remained almost the same for leaves 10 to 11 and then showed smaller leaf sizes as nodes increased above 11 irrespective of UV-B treatment and hybrid (Fig. 4). The UV-B treatments had greater effect on the early-formed leaves than on the leaves that developed at later stages of crop development (Fig. 4). At the end of experiments, the control plants had produced about 0.635 m2 (Terral-2100) and 0.722 m2 plant–1 (DKC 65-44) LA, whereas
Fig. 4. Effects of ultraviolet-B radiation on corn leaf areas 43 d after emergence. Standard errors of the mean values from nine plants are shown with bars.
UV-B treatments of 5, 10, and 15 kJ m–2 d–1 produced 16, 22, and 50% lower LA in Terral-2100, and 7, 10, and, 22% lower LA for DKC 65-44, respectively. Biomass Significant DAE X UV-B interactions were observed for biomass production in both hybrids (Table 1). The main effects of UV-B treatments were significant at all sampling dates (Fig. 5). Similar to the PH and LA, the treatment differences for biomass production were established at early growth stage
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Fig. 5. Biomass production as affected by ultraviolet-B radiation at 15, 23, and 43 days after emergence (DAE) of corn plants. Each data point is a mean of 30 (15 DAE), 10 (23 DAE), and 15 (43 DAE) individual plants and standard errors of the mean are shown above the histograms. Within a DAE, treatment means followed by the same letter are not significantly different (P > 0.05).
(15 DAE); however, the differences in the biomass among three levels of UV-B (5, 10, and 15kJ m–2 d–1) were more obvious in Terral-2100 and showed a decreasing trend as UV-B radiation increased. In Terral-2100, compared to the plants grown without UV-B radiation, UV-B treatments of 5, 10, and 15 kJ m–2 d–1 recorded decrease in biomass of 20, 39, and 54% (15 DAE), 0, 21, and 60% (23 DAE) and 11, 14, and 55% (43 DAE), respectively (Fig. 5). Similarly in DKC 65-44, compared to the plants grown without UV-B radiation, UV-B treatments of 5, 10, and 15 kJ m–2 d–1 recorded a decrease in biomass of 43, 30, and 34% (15 DAE), 38, 32, and 39% (23 DAE) and 7, 12, and 21% (43 DAE), respectively. At the final harvest (43 DAE); the biomass production for both the hybrids was comparable between the 5 and 10 kJ m–2 d–1 UV-B treatments (Fig. 5). Photosynthesis and Fluorescence Parameters The photosynthetic rates of the uppermost fully expanded leaves were significantly (P < 0.001) affected by UV-B radiation treatments, and differences between the two measurement dates were significant (P < 0.05) in both hybrids (Table 2). The deleterious effects of UV-B radiation on plants were more pronounced in Terral-2100 than in DKC 65-44. However, in DKC 65-44, when 5 kJ m–2 d–1 UV-B was used as the reference, photosynthetic parameters decreased at 10 and 15 kJ m–2 d–1 UV-B. Averaged across measurement dates, leaf Pn of control plants was 58% more than the plants irradiated with 15 kJ m–2 d–1 of UV-B radiation in Terral-2100. Leaf Pn 1372
of plants grown at 5 and 10 kJ m–2 d–1 of UV-B were 42 and 20% greater, respectively, than the 15 kJ m–2 d–1 and 10 and 24% lower, respectively, than the 0 kJ m–2 d–1 of UV-B treated plants (Table 2). In DKC 65-44, averaged across the measurements, the Pn of control plants was only 9% greater than 15 kJ UV-B treated plants. On average, UV-B radiation stimulated Pn of DKC 65-44 plants grown at 5 and 10 kJ m–2 d–1 UV-B treatments. The internal CO2 concentrations were not affected significantly by the time of measurement and UV-B treatments in both hybrids. The main effect of UV-B was significant for gs and transpiration in both hybrids. Averaged over DAE in Terral-2100, both gs and transpiration decreased as UV-B radiation increased from 0 kJ to 15 kJ m–2 d–1 with maximum percentage decrease (47% gs, and 43% transpiration) recorded at 15 kJ m–2 d–1 UV-B. Relatively smaller decrease in gs (13%) and transpiration (5%) were observed only at 15 kJ m–2 d–1 UV-B in DKC 65-44. The influence of UV-B on water-use efficiency (WUE) was significant in Terral-2100 but not in DKC 65-44. The WUE was found to be approximately 9% higher in Terral-2100 plants grown under 15 kJ m–2 d–1 UV-B compared to the plants grown under 0, 5, and 10 kJ m–2 d–1 UV-B at both 24 DAE and 31 DAE. Fluorescence parameters such as Fv’/Fm’, fCO2 , and qN in both hybrids were significantly affected by UV-B radiation; however the measurement dates and its interaction with UV-B treatments were mostly nonsignificant (P > 0.05) (Table 3). Similar to photosynthesis, the deleterious effect of UV-B Agronomy Journal • Volume 105, Issue 5 • 2013
Table 2. Effect of ultraviolet-B (UV-B) radiation on photosynthesis (Pn), conductance (gs), internal CO2 concentration (Ci), transpiration (Tr), and instantaneous water-use efficiency (WUE, Pn/Tr) of uppermost fully expanded leaf recorded at two different times of corn growth and development. UV-B DAE†
kJ
Terral-2100 24
m–2 0 5 10 15 0 5 10 15
31
ANOVA DAE UV-B DAE ´ UV-B DKC 65–44 24
31
ANOVA DAE UV-B DAE ´ UV-B
0 5 10 15 0 5 10 15
d–1
Pn µmol CO2
gs m–2 s–1
mol H2O
Ci m–2 s–1
48.4 47.8 41.2 36.3 49.2 39.8 32.7 25.3
0.297 0.285 0.245 0.196 0.342 0.278 0.208 0.140
* *** ns
ns‡ * ns
38.57 45.33 40.60 37.17 46.17 46.77 45.60 40.50
0.225 0.288 0.245 0.217 0.304 0.339 0.274 0.241
* *** ns
* * ns
µmol CO2 mol
Tr –1
mmol H2O
WUE m–2 s–1
µmol CO2 mmol–1 H2O
77.1 66.8 76.2 47.4 108.1 98.2 90.9 58.5
7.39 7.09 6.12 5.00 8.21 7.10 5.94 3.90
6.58 6.78 6.73 7.24 6.07 5.67 5.50 6.50
ns ns ns
ns ** ns
*** * ns
6.76 8.31 7.33 6.11 5.17 6.24 5.84 5.17
5.71 5.48 5.55 6.09 8.98 7.63 7.91 7.87
*** ** ns
*** ns ns
107.07 125.23 114.17 105.63 137.77 154.20 108.77 114.33 ns ns ns
* Significance level P £ 0.05. ** Significance level P £ 0.01. *** Significance level P £ 0.001. † DAE, days after emergence. ‡ Significance level ns represents P > 0.05. ns, not significant.
radiation on these parameters were more pronounced in Terral-2100 than in DKC 65-44. Averaged over measurement dates, these parameters decreased as UV-B radiation increased from 0 kJ to 15 kJ m–2 d–1 with maximum percentage decrease in Fv’/Fm’ (22%), fCO2 (36%), and qN (19%) recorded at 15 kJ m–2 d–1 UV-B compared to the 0 kJ m–2 d–1 UV-B treatment. Decreased in Fv’/Fm’ (3%), fCO2 (9%), and qN (3%) were as only observed at 15 kJ m–2 d–1 in DKC 65-44. Ultraviolet-B Response Indices The results of the regression analysis and the UV-B indices for various growth and physiological parameters are presented in Table 4 and Fig. 6 and 7. In general, linear decreasing trends were recorded for growth parameters such as stem extension, leaf area development and biomass accumulation in both the hybrids. The parameters including Pn, gs, Fv’/Fm’, fPSII, and qN showed similar linear trend in Terral-2100, but these trends were quadratic in DKC 65-44. In general, the critical limits of UV-B as defined by the 90% of the optimum or control, for growth parameters (stem extension, leaf area expansion, and biomass accumulation) were lower than above listed parameters. Based on the estimated critical limits, the stem extension and leaf area expansion were the most sensitive parameters with a critical limit of »1.7 kJ m–2 d–1 UV-B compared to the
other growth and physiological parameters including biomass accumulation (4 kJ m–2 d–1 UV-B) in Terral-2100. The hybrid, DKC 65-44, behaved similarly to Terral 2100; however, the critical limit for stem extension was 3.23 kJ m–2 d–1 UV-B followed by leaf area expansion and biomass accumulation with a critical limit of »7.5 kJ m–2 d–1 UV-B. For the hybrid Terral-2100, the critical limits for leaf photosynthetic rates, gs, and fPSII were similar (»4.2 kJ m–2 d–1 UV-B) and lower than critical limits for Fv’/Fm’ and qN (»8 kJ m–2 d–1 UV-B). Based on the quadratic relationships between photosynthetic parameters and UV-B in DKC 65-44, the critical limits for photosynthesis, gs and transpiration were similar (»14 kJ m–2 d-–1 UV-B) and lower than the critical limits for Fv’/Fm’, fPSII, and qN (16 to 19 kJ m–2 d–1 UV-B). DISCUSSION Through this study and for the first time, UV-B stress response indices for various growth and photosynthetic parameters for corn are provided which could be used to improve existing corn models. The two corn hybrids used in both years were significantly affected by ambient and projected UV-B radiations for most of the plant attributes measured. Furthermore, corn responses to UV-B radiation treatments for both the experiments were comparable for many traits. The whole plant and leaf
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Table 3. Effect of ultraviolet-B (UV-B) radiation (kJ m –2 d –1) on the efficiency of energy harvesting by oxidized (open) PSII reaction centers in light (Fv’/Fm’), the fraction of absorbed photon that are used for photochemistry for a light adapted leaf (fPSII, µmol electron (µmole photon) –1), the apparent quantum yield of CO2 assimilation (fCO2 , µmol CO2 (µmole photon) –1) and non-photochemical quenching (qN) of uppermost fully expanded leaf recorded at two different times of corn growth and development. DAE Terral-2100 24
31
UV-B
Fv’/Fm’
fPSII
fCO2
qN
0 5 10 15 0 5 10 15
0.4903 0.4533 0.4683 0.4367 0.5263 0.5000 0.4247 0.3530
0.2880 0.2893 0.2997 0.2737 0.3033 0.2787 0.2690 0.2290
0.0390 0.0387 0.0340 0.0293 0.0390 0.0323 0.0260 0.0203
1.986 1.836 1.882 1.787 2.122 2.004 1.742 1.547
ANOVA DAE UV-B
ns† ** ns
DAE ´ UV-B DKC 65–44 24
0 5 10 15 0 5 10 15
31
ANOVA DAE UV-B DAE ´ UV-B
ns ns ns
* ** ns
ns ** ns
0.5307 0.5603 0.5720 0.5070 0.5200 0.5607 0.5173 0.5077
0.3177 0.3213 0.3040 0.3060 0.3357 0.3430 0.3390 0.3157
0.0313 0.0367 0.0330 0.0300 0.0370 0.0377 0.0370 0.0323
2.132 2.282 2.348 2.037 2.085 2.293 2.077 2.034
ns * ns
* ns ns
*** *** ns
ns * ns
* Significance level P £ 0.05. ** Significance level P £ 0.01. *** Significance level P £ 0.001. † Significance level ns represents P > 0.05. ns, not significant.
growth characteristics, particularly during the early stages of crop development, displayed the strongest reductions. Reduced plant growth was due to decreases in overall plant stature such as height, leaf area, and partly by effects on photosynthesis. Corn Growth and Development Shorter plants, reduced leaf area, and less biomass for both the hybrids in UV-B exposed plants observed in the current study are in agreement with the others studies including corn (Correia et al., 1999; Gao et al., 2004; Mark and Tevini, 1997; Reddy et al., 2003, 2004; Singh et al., 2008). The implication of a range of UV-B dosage in both hybrids allowed us to assess the response of these growth processes as a function of UV-B radiation. The results clearly demonstrated that stem extension, leaf area expansion, and biomass accumulation decreased per unit increase in UV-B radiation. The smaller plants in UV-B treated plants were attributed to shorter internodes because leaf number was not significantly affected similar to the observation in cotton (Gossypium hirsutum L.) (Reddy et al., 2003). Since plant growth and development play a pivotal role in crop production, any factor controlling the production of new leaves, the duration of area expansion of each leaf, 1374
and stem extension will have a profound effect on yield (Reddy et al., 1997). The UV-B radiation affects phytohormone metabolism, such as auxins, in plants thus affecting the plant morphology (Hectors et al., 2007; Ros and Tevini, 1995). Leaf Photosynthetic Characteristics The average photosynthetic capacity of the uppermost fully expanded leaves at higher UV-B levels declined in both hybrids; however, it was more pronounced in Terral-2100. Similar observations also were made in other studies using different hybrids of corn (Correia et al., 1999; Mark and Tevini, 1997). The internal CO2 concentration was not affected significantly by UV-B radiation whereas stomatal conductance and transpiration decreased to some extent mainly at the highest UV-B treatments in both hybrids. The reduction in photosynthesis was associated with decreased fluorescence parameters such as Fv’/Fm’, fPSII, and quantum yield of CO2 assimilation, indicating injury to the photosystems. Correia et al. (1999) reported that supplementary UV-B radiation reduced photosynthetic capacity in corn as a consequence of damage to PSII, increased stomatal resistance (lower gs), lowered ribulose-1,5-bisphosphate carboxylase/ oxygenase (RUBISCO), and phosphoenolpyruvate carboxylase (PEPcase) activities. Lower photosynthetic rate accompanied with smaller leaf area under UV-B stress will have major impact on overall biomass accumulation. Ultraviolet-B Response Indices and Critical Limits for Corn Growth Processes Inverse relationships between several growth processes and dosage of UV-B radiation were observed in both hybrids. Similar trends have also been observed in cotton (Reddy et al., 2003). To date, quantitative relationships between various growth and developmental processes of corn as a function of UV-B radiation are not available for developing models to study current and projected changes in UV-B radiation. The approach we used in developing UV-B-specific functional algorithms was similar to those proposed by Nobel (1991) and Reddy et al. (2008). Therefore, UV-B radiation-specific reduction factors or indices were developed in this study. All the indices, ranging from zero when the UV-B stress is totally limiting that particular development, growth, or photosynthesis process, to 1 when it does not limit that parameter, represent the fractional limitation due to the UV-B radiation. These processes decrease as the effect of UV-B radiation stress becomes more severe. This way, the effects of UV-B radiation on corn growth, development, and photosynthesis in a changing UV-B radiation environment can be quantified without the interference of other biotic and environmental stresses when grown in an essentially stress-free environment. But, more importantly, the effects of UV-B radiation could be incorporated into a mechanistic model that responds appropriately to environmental conditions and accurately predicts corn responses to weather variables. Such an approach has previously been used by others in the crop-simulation model of cotton, GOSSYM (Reddy et al., 2003; Liang et al., 2012a, 2012b). The critical limits defined as the 90% of optimum or control for growth processes were lower than for the photosynthetic processes for both hybrids. The stem extension was commonly observed as the most sensitive process as deduced from the Agronomy Journal • Volume 105, Issue 5 • 2013
Table 4. Regression parameters and coefficient of various growth and developmental ultraviolet-B (UV-B) stress response indices of corn as affected by UV-B radiation (y = a + bX), except photosynthesis, conductance, the fraction of absorbed photon that are used for photochemistry for a light adapted leaf (fPSII), efficiency of energy harvesting by oxidized (open) PSII reaction centers in light (Fv'/Fm') and non-photochemical quenching (qN) in the Exp. II which is y = c + aX + bX2 , where y = respective UV-B index for the plant parameter and X = UV-B dosage in kJ m –2 d –1). The estimated critical limits defined as the 90% of the optimum or control for each growth processes are also presented. Regression parameters Plant parameters Terral-2100 Leaf development Leaf area expansion Stem extension Biomass production Photosynthesis Conductance fPSII Fv’/Fm’ qN DKC 65-44 Leaf development Leaf area expansion Stem extension Biomass production Photosynthesis Conductance fPSII Fv’/Fm’ qN
P value
Coefficient of determination (r2)
–0.0060 –0.0431 –0.0376 –0.0359 –0.0304 –0.0313 –0.0254 –0.0136 –0.0125
0.289 0.014 0.016 0.049 0.010 0.028 0.006 0.011 0.002
0.51 0.97 0.97 0.99 0.97 0.94 0.99 0.96 0.99
>20.0 1.7 1.8 4.0 4.2 4.2 4.5 7.6 8.0
–0.0017 –0.0139 –0.0261 –0.0138 –0.0020 –0.0033 –0.0005 –0.0015 –0.0018
0.387 0.049 0.008 0.017 0.200 0.440 0.206 0.134 0.140
0.38 0.90 0.97 0.98 0.96 0.81 0.96 0.98 0.98
>20.0 7.8 3.5 7.5 14.8 13.6 19.2 16.6 16.5
a
b
1.0196 0.9737 0.9673 1.0448 1.0254 1.033 1.0158 1.0042 1.0004
0.9883 1.0080 0.9931 1.0038 0.0231 0.0362 0.0043 0.0189 0.0235
Fig. 6. Ultraviolet-B radiation indices for various growth, developmental and physiological processes of corn hybrid Terral-2100. Fv’/Fm’ is the efficiency of energy harvesting by oxidized (open) PSII reaction centers in light, fPSII is the fraction of absorbed photon that are used for photochemistry for a light adapted leaf and qN is the non-photochemical quenching.
c
1.005309 1.021819 1.002212 1.002145 1.002896
Critical limit UV-B
Fig. 7. Ultraviolet-B radiation indices for various growth, developmental, and physiological processes of corn hybrid DKC 65-44. Other details are as in Fig. 5.
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lowest critical limits. The critical limit for leaf area expansion was similar to stem extension (1.7 kJ UV-B m–2 d–1) in Terral-2100, but differed in DKC 65-44 (7.8 and 3.5 kJ m–2 d–1, respectively). The critical limits for biomass production were 4 kJ m–2 d–1 UV-B (Terral-2100) and 7.5 kJ m–2 d–1 UV-B (DKC 65-44). The leaf development exhibited the least sensitivity to UV-B radiation among the measured parameters in both hybrids. Leaf photosynthesis had lower critical limits than fluorescence parameters such as fPSII, Fv'/Fm', and qN indicating that corn photosynthesis is more sensitive to UV-B than fluorescence parameters. Although most of the studied traits in corn plants particularly vegetative growth and developmental processes exhibited a similar response to UV-B radiation in both hybrids, the critical limits for a given process differed between the hybrids. Terral-2100 tended to have lower critical limits than DKC 65-44 indicating higher sensitivity of corn plants to UV-B radiation in the former than in the latter hybrid. This difference for the critical limits between the hybrids may largely be attributed to the hybrid differences as the most of the experimental conditions for the two studies were similar. However, there were also differences between total solar radiation received outside the SPAR units (19 vs. 17 MJ m–2 d–1) and the growth CO2 concentration (360 vs. 400 µmol mol–1) between the hybrids. Based on the response indices and critical limits, corn hybrid Terral-2100 was more sensitive to the current and projected UV-B radiation levels than DKC 65-44. Reddy et al. (2003) have also reported somewhat similar sensitivity of different growth and physiological process to UV-B radiation in cotton. In summary, corn growth is affected by both ambient and projected UV-B radiation levels. Stem extension is the most sensitive process to UV-B radiation followed by leaf area development and photosynthesis leading to decrease in biomass production. Leaf appearance is the least sensitive developmental process in response to UV-B. It is worthwhile to note that the critical limits of different growth processes in corn for UV-B dosage may vary depending up on the sensitivity of hybrids as was observed in the current study. From the present database, it seems that developing functional algorithms for photosynthesis parameters, leaf and stem growth will account for most of the UV-B effects on corn growth and development. The identified UV-B-specific growth and physiological indices should be useful and could be incorporated into mechanistic corn simulation models, which previously account for variations in temperature as well as water and nutrient stresses. Models such as CERES-Corn and MaizSim (Jones and Kiniry, 1986; Lizaso et al., 2003; Yang et al., 2009) could be enhanced to include UV-B-specific sensitivity to predict yields under current and future enhanced UV-B radiation environments. ACKNOWLEDGMENTS This research was in part funded by the Colorado State University USDA-UVB Monitoring and Research Program, Natural Resource Ecology Laboratory, Department of Ecosystem Science & Sustainability, USDA-NIFA-2011-34263-30654, G-1405-2. We also thank Mr. David Brand for technical support. This article is a contribution from the Department of Plant and Soil Sciences, Mississippi State University, Mississippi Agricultural and Forestry Experiment Station, paper no. 12143.
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Quantifying the Effects of Corn Growth and Physiological Responses to Ultraviolet-B Radiation for Modeling K. Raja Reddy,* Shardendu K. Singh, Sailaja Koti, V. G. Kakani, Duli Zhao, Wei Gao, and V. R. Reddy ABSTRACT
To understand the consequences of rising levels of ultraviolet-B (UV-B) radiation on corn (Zea mays L.), two experiments were conducted using sunlit growth chambers at a wide range of UV-B radiation levels. Corn hybrids, Terral-2100 and DKC 65-44, were grown in 2003 and 2008, respectively, at four UV-B levels (0, 5, 10, and 15 kJ m–2 d–1) at 30/22°C, from 4 d after emergence to 43 d under optimum nutrient and water conditions. Plant growth, development, and photosynthetic rates were measured regularly. An inverse relationship between many growth process and dosage of UV-B radiation was recorded. Shorter plants were due to shorter internodal lengths rather than fewer internodes and the total leaf area was less due to smaller leaves. Lower biomass under enhanced UV-B was closely related to smaller leaf area and lower photosynthesis. Critical UV-B limits, defined as 90% of optimum or control, were estimated from the UV-B response indices. The critical limits for stem extension and leaf area expansion were lower in both hybrids (1.7–3.5 kJ m–2 d–1) than the critical limit for leaf number (>15 kJ m–2 d–1) and photosynthetic processes, indicating that expansion or extension rates of organs were the more sensitive to UV-B radiation. Hybrid Terral-2100 exhibited greater sensitivity to UV-B radiation than DKC 65-44 for studied parameters. Thus, both current and projected UV-B radiation can adversely affect corn growth. The functional algorithms developed in this study could be useful to enhance the corn models to predict accurately field performance.
U
ltraviolet-B radiation (280–320 nm) is an integral part of sunlight that reaches the surface of Earth. Even though UV-B represents a small fraction of total solar radiation, exposure to UV-B at current and projected levels is known to elicit a variety of responses in all living organisms, including higher plants (Kakani et al., 2003; Runeckles and Krupa, 1994). Over the past 50 yr, the concentration of ozone in the stratosphere, which absorbs most of the UV-B radiation, has decreased about 5%, mainly due to release of anthropogenic pollutants such as chloroflurocarbons (Pyle, 1996). Current global distribution of mean erythemal (biologically effective/ potential for biological damage) daily dose of UV-B radiation between the latitudes 40°N and 40°S during summer ranges between 2 and 9 kJ m–2 (McKenzie et al., 2007), a level which is about 3 kJ m–2 higher than the 1994 observation (Seckmeyer et al., 1995). Elevated UV-B levels are expected to continue well into the 21st century (WMO, 2007). Model simulations
K.R. Reddy, Dep. of Plant and Soil Sciences, 117 Dorman Hall, Box 9555, Mississippi State Univ., Mississippi State, MS 39762; S.K. Singh, and V.R. Reddy, Crop Systems and Global Change Lab., USDA-ARS, Beltsville, MD 20705; S. Koti, RiceTec, Inc., P.O. Box 1305, Alvin, TX 77512; V.G. Kakani, Dep. of Plant and Soil Sciences, Oklahoma State Univ., Stillwater, OK 74078; Duli Zhao, USDA-ARS, Sugarcane Field Station, 12990 U.S. HWY 441, Canal Point, FL 33438; W. Gao, USDA-UV-B Monitoring Network, Natural Resource Ecology Lab., Colorado State Univ., Fort Collins, CO 80523. Received 5 Mar. 2013. *Corresponding author ([email protected]). Published in Agron. J. 105:1367–1377 (2013) doi:10.2134/agronj2013.0113 Copyright © 2013 by the American Society of Agronomy, 5585 Guilford Road, Madison, WI 53711. All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.
suggest that the United States is already experiencing UV-B dosage that may be deleterious to crop growth and development (Lubin and Jensen, 1995). Recent estimates have shown that continued increase in ground-level UV-B radiation will occur over the next few decades, although there is considerable uncertainty between changes projected in atmospheric chemistry and associated changes in climate and their interactions (Taalas et al., 2000; Zerefos et al., 1997). Previous reviews and published studies clearly demonstrate the extent of damage caused by both ambient (Caldwell et al., 1989; Teramura, 1983; Teramura and Sullivan, 1994) and elevated UV-B radiation (Kakani et al., 2003; Krupa, 1998; Rozema et al., 1997; Searles et al., 2001; Teramura, 1983) on morphological, physiological, biochemical, and molecular components of crop plants including corn. Some of the primary effects of UV-B radiation on plant metabolic systems are DNA damage, dilation, and disintegration of cellular membranes, photooxidation of leaf pigments and phytohormones, and inhibition of photosynthesis (Correia et al., 1999; He et al., 1994; Mark and Tevini, 1997; Ros and Tevini, 1995) in association with down-regulation of genes responsible for processes such as photosynthesis and phytohormone metabolism and cell wall loosening (Casati and Walbot, 2003; Hectors et al.,
Abbreviations: fCO2 , the apparent quantum yield of CO2 assimilation; fPSII, the fraction of absorbed photon that are used for photochemistry for a light adapted leaf; BIO, aboveground biomass; Ci, internal CO2 concentration; DAE, days after emergence; Fv’/Fm’, efficiency of energy harvesting by oxidized (open) PSII reaction centers in light; g s, stomatal conductance; LA, leaf area; LFWt, leaf dry weight; LN, mainstem leaf number; PH, plant height; PSII, photosystem-II; Pn, rate of photosynthesis; qN, non-photochemical quenching; SPAR, Soil–Plant Atmosphere Research; STWt, stem dry weight; Tr, transpiration; UV-B, ultraviolet-B; WUE, instantaneous water use efficiency (Pn/Tr).
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2007). These primary effects result in numerous secondary and tertiary effects causing altered crop growth and development, reduced fruit numbers and retention, and finally, biomass and yield reductions (Kakani et al., 2003). Ultraviolet-B radiation has a large photobiological effect as it is readily absorbed by biomolecules such as amino acids, pigments, and nucleic acids (Caldwell and Flint, 1994; Sullivan and Teramura, 1989). Several studies were performed on UV-B effects on growth and physiological responses on many field crops such as bean (Phaseolus vulgaris L., Deckmyn et al., 1994), cotton (Gossypium hirsutum L., Kakani et al., 2004; Reddy et al., 2003, 2004), corn (Correia et al., 1998, 1999; Gao et al., 2004; Mark and Tevini, 1996), pea (Pisum sativum L., Day et al., 1996; Mepsted et al., 1996), rice (Oryza sativa L., Dai et al., 1992; Teramura et al., 1990), soybean [Glycine max (L.) Merr., Miller et al., 1994; Sinclair et al., 1990], sunflower (Helianthus annuus L., Battaglia and Brennen, 2000), cowpea [Vigna unguiculata (L.) Walp., Singh et al., 2008], and wheat (Triticum aestivum L., Yuan et al., 2000; Teramura et al., 1990). Several reviews have recently summarized the effects and consequences of UV-B radiation on major agricultural and non-agricultural plant species (Allen, 1994; Caldwell et al., 1998; Frohnmeyer and Staiger, 2003; Kakani et al., 2003; Krupa and Kickert, 1989; Teramura and Sullivan, 1994). The inferences from these studies and reviews are that plant sensitivities to UV-B radiation differ among species and hybrids within a species. Even though several studies addressed UV-B effects on corn growth, little is known about the quantitative dose response functions for developing algorithms for models on corn. It is important to better understand UV-B radiation effects on corn because of its major economic importance worldwide (FAO, 2011). Plant growth and development play a pivotal role in crop production systems. The vegetative growth and developmental processes such as production of new leaves, leaf expansion, and extension of internodes are the major determinants of crop biomass production. Any factor (biotic or abiotic) that affects these crop growth and developmental processes will have profound influence on the interception of photosynthetically active radiation (PAR) during the production season. Therefore, it is useful to understand factors that control plant growth and development and to quantify the responses so that suitable management practices can be devised to optimize production. Quantification of these responses of crop growth and physiological processes to broad ranges of abiotic factors such as UV-B radiation is also a key for developing process-based crop simulation models to be used for predicting crop and agricultural systems responses to changes in climate. Corn and all other crops cultivated between 40°N and 40°S latitudes are already experiencing UV-B dosage of 2 to 10 kJ m–2 d–1 depending on location and season (Gao et al., 2004; McKenzie et al., 2007). Corn is sensitive to both ambient and elevated UV-B radiations with noticeable intraspecific variability (Correia et al., 1998, 1999; Gao et al., 2004; Mark and Tevini, 1996). It is hypothesized that both the current levels and the projected increases in UV-B radiation can alter corn growth and development. An understanding of the effects of solar UV-B radiation on corn hybrids would provide information about the causes of changes in growth, development, and physiology and how these changes vary between hybrids. 1368
Therefore, the objectives of this study were to determine the growth, development, and physiological responses of two corn hybrids to UV-B radiation and to quantify and develop UV-B radiation-specific functional algorithms, which can be used in corn simulation models. MATERIALS AND METHODS Soil–Plant Atmosphere Research Units This study was conducted in sunlit Soil–Plant Atmosphere Research (SPAR) chambers located at the RR Foil Plant Science Research facility of Mississippi State University, (33°28¢ N, 88°47¢ W), Mississippi State, MS, in 2003 and 2008. Each SPAR chamber consists of a steel soil bin (1-m deep by 2 m long by 0.5 m wide) to accommodate the root system, and a Plexiglas chamber (2.5 m tall by 2.0 m long by 1.5 m wide) to accommodate aerial plant parts, a heating and cooling system, and an environmental monitoring and control system. The Plexiglas transmits 97% of the visible solar radiation to pass without spectral variability in absorption and is opaque to solar UV-B radiation (280–320 nm), but transmits 12% of UV-A radiation (wavelength 320–400 nm; Zhao et al., 2003). To avoid the effect of germicidal effects of UV-C radiation ( 0.05. ns, not significant.
Fig. 2. Changes in plant height of corn as affected by ultraviolet-B radiation. Each data point is a mean of nine individual plants and standard errors of the mean are shown when larger than the symbols.
Photosynthesis and Fluorescence Measurements These measurements were made on the upper most fully expanded leaves (24 DAE and 31 DAE, Terral-2100; and 23 DAE and 40 DAE, DKC 65-44) between 1000 and 1300 h from three individual plants per treatment using a LI-6400 (LI6400 photosynthesis meter, LI-COR Inc., Lincoln, NE) with an integrated fluorescence chamber head (LI-COR 6400-40 Leaf Chamber Fluorometer; LI-Cor Inc.). The temperature in leaf cuvette was set to the day time chamber air temperature (30°C) and [CO2] was controlled by the CO2 injection system to match the [CO2] treatments. The PAR provided by a 6400-02 LED light source was set to 1500 µmol m–2 s–1. Relative humidity inside the cuvette was maintained at approximately 50%. To measure fluorescence, the built-in leaf chamber fluorometer was used which uses two red LEDs (center wavelength about 630 nm) and a detector (sees radiation at 715 nm in the PSII fluorescence band). A flash light (>7000 µmol m–2 s–1) achieved by using 27 red LEDs was used to measure the maximal fluorescence (Fm’). Rapid dark adaptation to measure minimal fluorescence (Fo’) was achieved by turning off the actinic light while using the far red LED (center wavelength at 740 nm). The far red radiation drives photosystem-I (PSI) momentarily to help drain PSII of electrons. The software in the instrument provides data on the fluorescence parameters and also calculated parameters such as PSII reactions centers under light (Fv’/Fm’), PSII efficiency (fPSII), quantum yield from gas exchange, and nonphotochemical quenching (qN) (LI-6400 Instruction Manual, version 5, LI-Cor Inc., Lincoln, NE).
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Ultraviolet-B Radiation Indices and Critical Ultraviolet-B Limits Regression analysis (SAS Institute, 2008) was used as an exploratory tool to obtain the overall measure of UV-B sensitivity for understanding the growth and physiological responses of corn hybrids to UV-B. To test the significance of the relationship between measured parameters and dosage of UV-B radiation, a significance level of 0.05 (P = 0.05) was used. To obtain UV-B indices, the measured values from each parameter were normalized to obtain the slopes in response to UV-B radiation. The estimated values at 0 kJ m–2 d–1 UV-B were used as a denominator so that the derived values range between a relative scale of 0 to 1 as described by Reddy et al. (2003, 2008). Critical limits of UV-B were calculated from the developed algorithms as 90% of the optimum or control. Analysis of Data The statistical analysis was conducted separately for each hybrid using ANOVA procedure of SAS (SAS Institute, 2008). The least significant difference (LSD) tests at P = 0.05 were employed to distinguish among treatments for the growth and physiological parameters measured in the study. The standard errors of each mean were also calculated and presented in the figures as error bars. RESULTS Ultraviolet-B radiation treatments were very close to the set points and did not differ significantly between both years (Fig. 1). Plant Height Plant height increased exponentially as plants aged for both hybrids (Fig. 2) and differed significantly over time within a UV-B treatment and among UV-B treatments (Table 1). The UV-B radiation caused significant decrease in PH with maximum decrease for both the hybrids at 15 kJ m–2 d–1. By the end of experiments, plants grown under control (without UV-B radiation) were 163 cm (Terral-2100) and 158 cm (DKC 65-44) tall. In comparison to the control, UV-B treatments Agronomy Journal • Volume 105, Issue 5 • 2013
Fig. 3. Changes in (A and C) leaf number and (B and D) leaf area of corn as affected by ultraviolet-B radiation. Each data point is a mean of nine individual plants and standard errors of the mean are shown when larger than the symbols.
of 5, 10, and 15 kJ m–2 d–1, decreased plant height by 35, 47, and 66% for Terral-2100, and 17, 23, and 41% for DKC 65-44, respectively. Mainstem Nodes Unlike the PH, adding leaves on the main stem increased linearly as the plants aged irrespective of UV-B treatments for both hybrids (Fig. 3A, 3C). The mainstem leaf number exhibited a significant DAE X UV-B interaction only for Terral-2100. Although, leaf number differed significantly over time and among UV-B levels (Table 1), the final count of the leaf numbers were not statistically different. The days to produce one leaf, calculated as the inverse of the slope over time, did not differ among the three lowest UV-B treatments (0, 5, and 10 kJ m–2 d–1) for Terral-2100. It took about 2.3 d (slope 2.344) for the plants grown at 0, 5, and 10 kJ m–2 d–1 of UV-B, while the plants grown under the 15 kJ m–2 d–1 UV-B treatment took 2.6 d (slope 2.481) to produce a leaf. The average count of the mainstem leaves produced were 16 and 14 leaves for Terral-2100 and DKC 65-44, respectively. Leaf Area Development Total leaf area of the plants in both experiments followed similar trends to that of PH across all UV-B treatments (Fig. 3B, 3D), and differed significantly over time and among UV-B levels (Table 1). In general, the reductions in LA development were slightly lower than the reductions in PH across all UV-B levels tested. Final leaf size, the product of the duration of expansion and rate of leaf growth, increased as nodal position up the plant increased to node 8 in all UV-B treatments. Final leaf size remained almost the same for leaves 10 to 11 and then showed smaller leaf sizes as nodes increased above 11 irrespective of UV-B treatment and hybrid (Fig. 4). The UV-B treatments had greater effect on the early-formed leaves than on the leaves that developed at later stages of crop development (Fig. 4). At the end of experiments, the control plants had produced about 0.635 m2 (Terral-2100) and 0.722 m2 plant–1 (DKC 65-44) LA, whereas
Fig. 4. Effects of ultraviolet-B radiation on corn leaf areas 43 d after emergence. Standard errors of the mean values from nine plants are shown with bars.
UV-B treatments of 5, 10, and 15 kJ m–2 d–1 produced 16, 22, and 50% lower LA in Terral-2100, and 7, 10, and, 22% lower LA for DKC 65-44, respectively. Biomass Significant DAE X UV-B interactions were observed for biomass production in both hybrids (Table 1). The main effects of UV-B treatments were significant at all sampling dates (Fig. 5). Similar to the PH and LA, the treatment differences for biomass production were established at early growth stage
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Fig. 5. Biomass production as affected by ultraviolet-B radiation at 15, 23, and 43 days after emergence (DAE) of corn plants. Each data point is a mean of 30 (15 DAE), 10 (23 DAE), and 15 (43 DAE) individual plants and standard errors of the mean are shown above the histograms. Within a DAE, treatment means followed by the same letter are not significantly different (P > 0.05).
(15 DAE); however, the differences in the biomass among three levels of UV-B (5, 10, and 15kJ m–2 d–1) were more obvious in Terral-2100 and showed a decreasing trend as UV-B radiation increased. In Terral-2100, compared to the plants grown without UV-B radiation, UV-B treatments of 5, 10, and 15 kJ m–2 d–1 recorded decrease in biomass of 20, 39, and 54% (15 DAE), 0, 21, and 60% (23 DAE) and 11, 14, and 55% (43 DAE), respectively (Fig. 5). Similarly in DKC 65-44, compared to the plants grown without UV-B radiation, UV-B treatments of 5, 10, and 15 kJ m–2 d–1 recorded a decrease in biomass of 43, 30, and 34% (15 DAE), 38, 32, and 39% (23 DAE) and 7, 12, and 21% (43 DAE), respectively. At the final harvest (43 DAE); the biomass production for both the hybrids was comparable between the 5 and 10 kJ m–2 d–1 UV-B treatments (Fig. 5). Photosynthesis and Fluorescence Parameters The photosynthetic rates of the uppermost fully expanded leaves were significantly (P < 0.001) affected by UV-B radiation treatments, and differences between the two measurement dates were significant (P < 0.05) in both hybrids (Table 2). The deleterious effects of UV-B radiation on plants were more pronounced in Terral-2100 than in DKC 65-44. However, in DKC 65-44, when 5 kJ m–2 d–1 UV-B was used as the reference, photosynthetic parameters decreased at 10 and 15 kJ m–2 d–1 UV-B. Averaged across measurement dates, leaf Pn of control plants was 58% more than the plants irradiated with 15 kJ m–2 d–1 of UV-B radiation in Terral-2100. Leaf Pn 1372
of plants grown at 5 and 10 kJ m–2 d–1 of UV-B were 42 and 20% greater, respectively, than the 15 kJ m–2 d–1 and 10 and 24% lower, respectively, than the 0 kJ m–2 d–1 of UV-B treated plants (Table 2). In DKC 65-44, averaged across the measurements, the Pn of control plants was only 9% greater than 15 kJ UV-B treated plants. On average, UV-B radiation stimulated Pn of DKC 65-44 plants grown at 5 and 10 kJ m–2 d–1 UV-B treatments. The internal CO2 concentrations were not affected significantly by the time of measurement and UV-B treatments in both hybrids. The main effect of UV-B was significant for gs and transpiration in both hybrids. Averaged over DAE in Terral-2100, both gs and transpiration decreased as UV-B radiation increased from 0 kJ to 15 kJ m–2 d–1 with maximum percentage decrease (47% gs, and 43% transpiration) recorded at 15 kJ m–2 d–1 UV-B. Relatively smaller decrease in gs (13%) and transpiration (5%) were observed only at 15 kJ m–2 d–1 UV-B in DKC 65-44. The influence of UV-B on water-use efficiency (WUE) was significant in Terral-2100 but not in DKC 65-44. The WUE was found to be approximately 9% higher in Terral-2100 plants grown under 15 kJ m–2 d–1 UV-B compared to the plants grown under 0, 5, and 10 kJ m–2 d–1 UV-B at both 24 DAE and 31 DAE. Fluorescence parameters such as Fv’/Fm’, fCO2 , and qN in both hybrids were significantly affected by UV-B radiation; however the measurement dates and its interaction with UV-B treatments were mostly nonsignificant (P > 0.05) (Table 3). Similar to photosynthesis, the deleterious effect of UV-B Agronomy Journal • Volume 105, Issue 5 • 2013
Table 2. Effect of ultraviolet-B (UV-B) radiation on photosynthesis (Pn), conductance (gs), internal CO2 concentration (Ci), transpiration (Tr), and instantaneous water-use efficiency (WUE, Pn/Tr) of uppermost fully expanded leaf recorded at two different times of corn growth and development. UV-B DAE†
kJ
Terral-2100 24
m–2 0 5 10 15 0 5 10 15
31
ANOVA DAE UV-B DAE ´ UV-B DKC 65–44 24
31
ANOVA DAE UV-B DAE ´ UV-B
0 5 10 15 0 5 10 15
d–1
Pn µmol CO2
gs m–2 s–1
mol H2O
Ci m–2 s–1
48.4 47.8 41.2 36.3 49.2 39.8 32.7 25.3
0.297 0.285 0.245 0.196 0.342 0.278 0.208 0.140
* *** ns
ns‡ * ns
38.57 45.33 40.60 37.17 46.17 46.77 45.60 40.50
0.225 0.288 0.245 0.217 0.304 0.339 0.274 0.241
* *** ns
* * ns
µmol CO2 mol
Tr –1
mmol H2O
WUE m–2 s–1
µmol CO2 mmol–1 H2O
77.1 66.8 76.2 47.4 108.1 98.2 90.9 58.5
7.39 7.09 6.12 5.00 8.21 7.10 5.94 3.90
6.58 6.78 6.73 7.24 6.07 5.67 5.50 6.50
ns ns ns
ns ** ns
*** * ns
6.76 8.31 7.33 6.11 5.17 6.24 5.84 5.17
5.71 5.48 5.55 6.09 8.98 7.63 7.91 7.87
*** ** ns
*** ns ns
107.07 125.23 114.17 105.63 137.77 154.20 108.77 114.33 ns ns ns
* Significance level P £ 0.05. ** Significance level P £ 0.01. *** Significance level P £ 0.001. † DAE, days after emergence. ‡ Significance level ns represents P > 0.05. ns, not significant.
radiation on these parameters were more pronounced in Terral-2100 than in DKC 65-44. Averaged over measurement dates, these parameters decreased as UV-B radiation increased from 0 kJ to 15 kJ m–2 d–1 with maximum percentage decrease in Fv’/Fm’ (22%), fCO2 (36%), and qN (19%) recorded at 15 kJ m–2 d–1 UV-B compared to the 0 kJ m–2 d–1 UV-B treatment. Decreased in Fv’/Fm’ (3%), fCO2 (9%), and qN (3%) were as only observed at 15 kJ m–2 d–1 in DKC 65-44. Ultraviolet-B Response Indices The results of the regression analysis and the UV-B indices for various growth and physiological parameters are presented in Table 4 and Fig. 6 and 7. In general, linear decreasing trends were recorded for growth parameters such as stem extension, leaf area development and biomass accumulation in both the hybrids. The parameters including Pn, gs, Fv’/Fm’, fPSII, and qN showed similar linear trend in Terral-2100, but these trends were quadratic in DKC 65-44. In general, the critical limits of UV-B as defined by the 90% of the optimum or control, for growth parameters (stem extension, leaf area expansion, and biomass accumulation) were lower than above listed parameters. Based on the estimated critical limits, the stem extension and leaf area expansion were the most sensitive parameters with a critical limit of »1.7 kJ m–2 d–1 UV-B compared to the
other growth and physiological parameters including biomass accumulation (4 kJ m–2 d–1 UV-B) in Terral-2100. The hybrid, DKC 65-44, behaved similarly to Terral 2100; however, the critical limit for stem extension was 3.23 kJ m–2 d–1 UV-B followed by leaf area expansion and biomass accumulation with a critical limit of »7.5 kJ m–2 d–1 UV-B. For the hybrid Terral-2100, the critical limits for leaf photosynthetic rates, gs, and fPSII were similar (»4.2 kJ m–2 d–1 UV-B) and lower than critical limits for Fv’/Fm’ and qN (»8 kJ m–2 d–1 UV-B). Based on the quadratic relationships between photosynthetic parameters and UV-B in DKC 65-44, the critical limits for photosynthesis, gs and transpiration were similar (»14 kJ m–2 d-–1 UV-B) and lower than the critical limits for Fv’/Fm’, fPSII, and qN (16 to 19 kJ m–2 d–1 UV-B). DISCUSSION Through this study and for the first time, UV-B stress response indices for various growth and photosynthetic parameters for corn are provided which could be used to improve existing corn models. The two corn hybrids used in both years were significantly affected by ambient and projected UV-B radiations for most of the plant attributes measured. Furthermore, corn responses to UV-B radiation treatments for both the experiments were comparable for many traits. The whole plant and leaf
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Table 3. Effect of ultraviolet-B (UV-B) radiation (kJ m –2 d –1) on the efficiency of energy harvesting by oxidized (open) PSII reaction centers in light (Fv’/Fm’), the fraction of absorbed photon that are used for photochemistry for a light adapted leaf (fPSII, µmol electron (µmole photon) –1), the apparent quantum yield of CO2 assimilation (fCO2 , µmol CO2 (µmole photon) –1) and non-photochemical quenching (qN) of uppermost fully expanded leaf recorded at two different times of corn growth and development. DAE Terral-2100 24
31
UV-B
Fv’/Fm’
fPSII
fCO2
qN
0 5 10 15 0 5 10 15
0.4903 0.4533 0.4683 0.4367 0.5263 0.5000 0.4247 0.3530
0.2880 0.2893 0.2997 0.2737 0.3033 0.2787 0.2690 0.2290
0.0390 0.0387 0.0340 0.0293 0.0390 0.0323 0.0260 0.0203
1.986 1.836 1.882 1.787 2.122 2.004 1.742 1.547
ANOVA DAE UV-B
ns† ** ns
DAE ´ UV-B DKC 65–44 24
0 5 10 15 0 5 10 15
31
ANOVA DAE UV-B DAE ´ UV-B
ns ns ns
* ** ns
ns ** ns
0.5307 0.5603 0.5720 0.5070 0.5200 0.5607 0.5173 0.5077
0.3177 0.3213 0.3040 0.3060 0.3357 0.3430 0.3390 0.3157
0.0313 0.0367 0.0330 0.0300 0.0370 0.0377 0.0370 0.0323
2.132 2.282 2.348 2.037 2.085 2.293 2.077 2.034
ns * ns
* ns ns
*** *** ns
ns * ns
* Significance level P £ 0.05. ** Significance level P £ 0.01. *** Significance level P £ 0.001. † Significance level ns represents P > 0.05. ns, not significant.
growth characteristics, particularly during the early stages of crop development, displayed the strongest reductions. Reduced plant growth was due to decreases in overall plant stature such as height, leaf area, and partly by effects on photosynthesis. Corn Growth and Development Shorter plants, reduced leaf area, and less biomass for both the hybrids in UV-B exposed plants observed in the current study are in agreement with the others studies including corn (Correia et al., 1999; Gao et al., 2004; Mark and Tevini, 1997; Reddy et al., 2003, 2004; Singh et al., 2008). The implication of a range of UV-B dosage in both hybrids allowed us to assess the response of these growth processes as a function of UV-B radiation. The results clearly demonstrated that stem extension, leaf area expansion, and biomass accumulation decreased per unit increase in UV-B radiation. The smaller plants in UV-B treated plants were attributed to shorter internodes because leaf number was not significantly affected similar to the observation in cotton (Gossypium hirsutum L.) (Reddy et al., 2003). Since plant growth and development play a pivotal role in crop production, any factor controlling the production of new leaves, the duration of area expansion of each leaf, 1374
and stem extension will have a profound effect on yield (Reddy et al., 1997). The UV-B radiation affects phytohormone metabolism, such as auxins, in plants thus affecting the plant morphology (Hectors et al., 2007; Ros and Tevini, 1995). Leaf Photosynthetic Characteristics The average photosynthetic capacity of the uppermost fully expanded leaves at higher UV-B levels declined in both hybrids; however, it was more pronounced in Terral-2100. Similar observations also were made in other studies using different hybrids of corn (Correia et al., 1999; Mark and Tevini, 1997). The internal CO2 concentration was not affected significantly by UV-B radiation whereas stomatal conductance and transpiration decreased to some extent mainly at the highest UV-B treatments in both hybrids. The reduction in photosynthesis was associated with decreased fluorescence parameters such as Fv’/Fm’, fPSII, and quantum yield of CO2 assimilation, indicating injury to the photosystems. Correia et al. (1999) reported that supplementary UV-B radiation reduced photosynthetic capacity in corn as a consequence of damage to PSII, increased stomatal resistance (lower gs), lowered ribulose-1,5-bisphosphate carboxylase/ oxygenase (RUBISCO), and phosphoenolpyruvate carboxylase (PEPcase) activities. Lower photosynthetic rate accompanied with smaller leaf area under UV-B stress will have major impact on overall biomass accumulation. Ultraviolet-B Response Indices and Critical Limits for Corn Growth Processes Inverse relationships between several growth processes and dosage of UV-B radiation were observed in both hybrids. Similar trends have also been observed in cotton (Reddy et al., 2003). To date, quantitative relationships between various growth and developmental processes of corn as a function of UV-B radiation are not available for developing models to study current and projected changes in UV-B radiation. The approach we used in developing UV-B-specific functional algorithms was similar to those proposed by Nobel (1991) and Reddy et al. (2008). Therefore, UV-B radiation-specific reduction factors or indices were developed in this study. All the indices, ranging from zero when the UV-B stress is totally limiting that particular development, growth, or photosynthesis process, to 1 when it does not limit that parameter, represent the fractional limitation due to the UV-B radiation. These processes decrease as the effect of UV-B radiation stress becomes more severe. This way, the effects of UV-B radiation on corn growth, development, and photosynthesis in a changing UV-B radiation environment can be quantified without the interference of other biotic and environmental stresses when grown in an essentially stress-free environment. But, more importantly, the effects of UV-B radiation could be incorporated into a mechanistic model that responds appropriately to environmental conditions and accurately predicts corn responses to weather variables. Such an approach has previously been used by others in the crop-simulation model of cotton, GOSSYM (Reddy et al., 2003; Liang et al., 2012a, 2012b). The critical limits defined as the 90% of optimum or control for growth processes were lower than for the photosynthetic processes for both hybrids. The stem extension was commonly observed as the most sensitive process as deduced from the Agronomy Journal • Volume 105, Issue 5 • 2013
Table 4. Regression parameters and coefficient of various growth and developmental ultraviolet-B (UV-B) stress response indices of corn as affected by UV-B radiation (y = a + bX), except photosynthesis, conductance, the fraction of absorbed photon that are used for photochemistry for a light adapted leaf (fPSII), efficiency of energy harvesting by oxidized (open) PSII reaction centers in light (Fv'/Fm') and non-photochemical quenching (qN) in the Exp. II which is y = c + aX + bX2 , where y = respective UV-B index for the plant parameter and X = UV-B dosage in kJ m –2 d –1). The estimated critical limits defined as the 90% of the optimum or control for each growth processes are also presented. Regression parameters Plant parameters Terral-2100 Leaf development Leaf area expansion Stem extension Biomass production Photosynthesis Conductance fPSII Fv’/Fm’ qN DKC 65-44 Leaf development Leaf area expansion Stem extension Biomass production Photosynthesis Conductance fPSII Fv’/Fm’ qN
P value
Coefficient of determination (r2)
–0.0060 –0.0431 –0.0376 –0.0359 –0.0304 –0.0313 –0.0254 –0.0136 –0.0125
0.289 0.014 0.016 0.049 0.010 0.028 0.006 0.011 0.002
0.51 0.97 0.97 0.99 0.97 0.94 0.99 0.96 0.99
>20.0 1.7 1.8 4.0 4.2 4.2 4.5 7.6 8.0
–0.0017 –0.0139 –0.0261 –0.0138 –0.0020 –0.0033 –0.0005 –0.0015 –0.0018
0.387 0.049 0.008 0.017 0.200 0.440 0.206 0.134 0.140
0.38 0.90 0.97 0.98 0.96 0.81 0.96 0.98 0.98
>20.0 7.8 3.5 7.5 14.8 13.6 19.2 16.6 16.5
a
b
1.0196 0.9737 0.9673 1.0448 1.0254 1.033 1.0158 1.0042 1.0004
0.9883 1.0080 0.9931 1.0038 0.0231 0.0362 0.0043 0.0189 0.0235
Fig. 6. Ultraviolet-B radiation indices for various growth, developmental and physiological processes of corn hybrid Terral-2100. Fv’/Fm’ is the efficiency of energy harvesting by oxidized (open) PSII reaction centers in light, fPSII is the fraction of absorbed photon that are used for photochemistry for a light adapted leaf and qN is the non-photochemical quenching.
c
1.005309 1.021819 1.002212 1.002145 1.002896
Critical limit UV-B
Fig. 7. Ultraviolet-B radiation indices for various growth, developmental, and physiological processes of corn hybrid DKC 65-44. Other details are as in Fig. 5.
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lowest critical limits. The critical limit for leaf area expansion was similar to stem extension (1.7 kJ UV-B m–2 d–1) in Terral-2100, but differed in DKC 65-44 (7.8 and 3.5 kJ m–2 d–1, respectively). The critical limits for biomass production were 4 kJ m–2 d–1 UV-B (Terral-2100) and 7.5 kJ m–2 d–1 UV-B (DKC 65-44). The leaf development exhibited the least sensitivity to UV-B radiation among the measured parameters in both hybrids. Leaf photosynthesis had lower critical limits than fluorescence parameters such as fPSII, Fv'/Fm', and qN indicating that corn photosynthesis is more sensitive to UV-B than fluorescence parameters. Although most of the studied traits in corn plants particularly vegetative growth and developmental processes exhibited a similar response to UV-B radiation in both hybrids, the critical limits for a given process differed between the hybrids. Terral-2100 tended to have lower critical limits than DKC 65-44 indicating higher sensitivity of corn plants to UV-B radiation in the former than in the latter hybrid. This difference for the critical limits between the hybrids may largely be attributed to the hybrid differences as the most of the experimental conditions for the two studies were similar. However, there were also differences between total solar radiation received outside the SPAR units (19 vs. 17 MJ m–2 d–1) and the growth CO2 concentration (360 vs. 400 µmol mol–1) between the hybrids. Based on the response indices and critical limits, corn hybrid Terral-2100 was more sensitive to the current and projected UV-B radiation levels than DKC 65-44. Reddy et al. (2003) have also reported somewhat similar sensitivity of different growth and physiological process to UV-B radiation in cotton. In summary, corn growth is affected by both ambient and projected UV-B radiation levels. Stem extension is the most sensitive process to UV-B radiation followed by leaf area development and photosynthesis leading to decrease in biomass production. Leaf appearance is the least sensitive developmental process in response to UV-B. It is worthwhile to note that the critical limits of different growth processes in corn for UV-B dosage may vary depending up on the sensitivity of hybrids as was observed in the current study. From the present database, it seems that developing functional algorithms for photosynthesis parameters, leaf and stem growth will account for most of the UV-B effects on corn growth and development. The identified UV-B-specific growth and physiological indices should be useful and could be incorporated into mechanistic corn simulation models, which previously account for variations in temperature as well as water and nutrient stresses. Models such as CERES-Corn and MaizSim (Jones and Kiniry, 1986; Lizaso et al., 2003; Yang et al., 2009) could be enhanced to include UV-B-specific sensitivity to predict yields under current and future enhanced UV-B radiation environments. ACKNOWLEDGMENTS This research was in part funded by the Colorado State University USDA-UVB Monitoring and Research Program, Natural Resource Ecology Laboratory, Department of Ecosystem Science & Sustainability, USDA-NIFA-2011-34263-30654, G-1405-2. We also thank Mr. David Brand for technical support. This article is a contribution from the Department of Plant and Soil Sciences, Mississippi State University, Mississippi Agricultural and Forestry Experiment Station, paper no. 12143.
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