quantifying the effects of corn growth and physiological responses

Agronomy Journa l • Volume 105 , I s sue 5 • 2013 1367

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

Published in Agron. J. 105:1367–1377 (2013)doi:10.2134/agronj2013.0113Copyright © 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.

Ultraviolet-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

suggest that the United States is already experiencing UV-B dosage that may be deleterious to crop growth and develop-ment (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 chem-istry 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 com-ponents 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 asso-ciation 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.,

ABSTRACTTo 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 regu-larly. 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.

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]).

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; gs, 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, pig-ments, 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 (Helian-thus 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 devel-oping 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. There-fore, 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 physi-ological 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 agricul-tural 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 vari-ability (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 infor-mation about the causes of changes in growth, development, and physiology and how these changes vary between hybrids.

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 METHODSSoil–Plant Atmosphere Research Units

This study was conducted in sunlit Soil–Plant Atmosphere Research (SPAR) chambers located at the RR Foil Plant Sci-ence 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 accom-modate 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 spec-tral variability in absorption and is opaque to solar UV-B radia-tion (280–320 nm), but transmits 12% of UV-A radiation (wave-length 320–400 nm; Zhao et al., 2003). To avoid the effect of germicidal effects of UV-C radiation (<280 nm) (Mercier et al., 2001), the lamps were wrapped with pre-solarized (kept under UV-B light for 48 h to stabilize transmission) 0.07 mm cellulose diacetate (CA) film (JCS Industries Inc., La Mirada, CA). The CA film was changed every 3 to 4 d to account for the degrada-tion of CA properties. More details of the SPAR unit operation and control have been described by Reddy et al. (2001). During these experiments, the minimum, maximum, and mean of the daily solar radiation (285–2800 nm) outside of the SPAR units, measured with a pyranometer (Model 4-8; The Eppley Labora-tory Inc., Newport, RI), were 3, 27, and 19 MJ m–2 d–1 (2003) and 3, 23, and 17 MJ m–2 d–1 (2008), respectively.

Air ducts located on the northern side of each SPAR unit connect the heating and cooling devices to each unit. Condi-tioned air was passed through the plant canopy with sufficient velocity to cause leaf flutter (4.7 km h–1) and was returned to the air-handling unit just above the soil level. Chilled ethylene glycol was supplied to the cooling system via several parallel solenoid valves that opened or closed depending on the cooling requirement. Two electrical resistance heaters provided short pulses of heat, as needed, to fine-tune the air temperature. Chamber air temperature, [CO2], and soil watering in each SPAR unit, as well as continuous monitoring of all-important environmental and plant gas exchange variables, were con-trolled by a dedicated computer system (Reddy et al., 2001).

Temperatures in all units were maintained at 30/22°C (day/night) during the experiments. Air temperature in each SPAR unit was monitored and adjusted every 10 s throughout the day and night and maintained within set points ±0.5°C. The daytime temperature was initiated at sunrise and returned to the nighttime temperature 1 h after sunset. The mean temperature (day/night) and relative humidity (day) between SPAR units and years were not significantly different and recorded as 26±0.8°C and 46±13% (2003) and 26±0.37°C and 45±12% (2008), respectively. The [CO2] in each SPAR unit was monitored and adjusted every 10 s throughout the day, and maintained within set points ± 10 µmol mol–1 as 360 and 400 µmol mol–1 in 2003 and 2008, respectively. The mean

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CO2 did differ significantly between experiments and recorded as 368 ± 10 µmol mol–1 in 2003 and 407 ± 8 µmol mol–1 in 2008.

Plant Culture

Corn hybrids Terral-2100 and DKC 65-44 seeds were sown on 13 May 2003 and 16 July 2008, respectively. Seeds were planted in fine sand medium within the four SPAR soil bins each year. Thus, there were two separate experiments each using four SPAR chambers but different corn hybrids. Emergence was observed 5 d after sowing in both years. In both years, corn seed were planted in 11 rows of five plants row–1, with each row 18.2 cm apart in each SPAR unit’s soil bin. Six rows of plants (total 30 plants from odd rows in each chamber) were harvested at 15 DAE, and two rows of plants from remaining five rows (total 10 plants) were harvested 23 DAE to avoid competition and to determine aboveground biomass at the early growth periods, and thus three rows (66.7 cm apart) of 15 plants m–2 (10 cm apart) were retained until 43 DAE. Plants were irrigated three times a day with half-strength Hoagland’s nutrient solution delivered at 0800, 1200, and 1700 h with an automated, and computer-controlled drip system to pro-vide favorable nutrient and water conditions for plant growth (Hewitt, 1952). Variable-density shade cloths (Hummert Seed Co., St. Louis, MO) placed around the edges of plants at emer-gence, were adjusted regularly to match plant heights, simulat-ing the natural shading by other plants.

Ultraviolet-B Radiation Treatments

Four UV-B radiation treatments, zero (control, no UV-B), and a total daily dose of biologically effective UV-B radiation of 5, 10, and 15 kJ m–2 d–1 were imposed from 4 DAE to the end of the experiments in both years. The approximated daily dos-age of UV-B radiation in the United States ranges from 0.02 to 8.75 kJ m–2 d–1 depending on season and cloud cover (USDA, UV-B-Monitoring and Research Program, Colorado State University, CO; http://uvb.nrel.colostate.edu/UVB). There-fore, the imposed UV-B dosages are expected to reflect near ambient (5 kJ m–2 d–1), high UV-B (10 kJ m–2 d–1) and severe (15 kJ m–2 d–1) treatments. In both years the square-wave sup-plementation systems (constant UV-B supplements) were used to provide desired UV-B radiation dosages which were delivered from 0.5 m above the plant canopy for 8 h, each day, from 0800 to 1600 h by eight fluorescent UV-B-313 lamps (Q-Panel Com-pany, Cleveland, OH) mounted horizontally on a metal frame inside each SPAR chamber, driven by 40 W dimming ballasts. The UV-B radiation delivered at the top of the plant canopy was monitored at 10 different locations in each SPAR chamber daily at 1000 h with a UVX digital radiometer (UVP Inc., San Gabriel, CA) which was calibrated against an Optronic Laboratory (Orlando FL) Model 754 Spectroradiometer that was being used initially to quantify the lamp output. The lamp output was adjusted, as needed, to maintain desired UV-B level. The weighted total biologically effective UV-B radiation at the top of the plant canopy during the experiment for both years are presented in Fig. 1, which were calculated using generalized erythermal plant response spectrum (Caldwell, 1971) as formu-lated by Green et al. (1974), normalized at 300 nm. Although the square-wave UV-B supplementation systems in controlled

environments provide disproportionate spectral conditions on cloudy days than those that occur in field conditions, they are particularly useful for quantifying the growth and developmen-tal responses of plants to UV-B and allow modeling its impact without the interacting effects of other variables (Koti et al., 2007; Musil et al., 2002; Reddy et al., 2003; Singh et al., 2010).

Growth and Developmental Measurements

In both years, nodes were counted and plant heights (PH) were measured on nine plants from three rows (three plants per row) in each chamber at 4-d intervals. Leaf lengths were also measured on all expanding mainstem leaves at 4-d interval. The leaf length measurements were converted to leaf areas (LA) by developing a relationship between the lengths and areas of different leaves measured using a LI-3100 LA meter (LICOR, Inc., Lincoln, NE) from the destructive harvests for each hybrid. The LA were estimated using the quadratic equations, y = 0.0779x2 – 0.6786x + 9.4377 (r2 = 0.90, n = 225; Ter-ral-2100), y = 0.0499x2 + 0.8315x – 10.315 (r2 = 0.92, n = 227; DKC 65-44) where, (y) is area in cm2 and (x) is the leaf length in centimeters. Plants were separated into leaves and stems at each harvest, and mainstem leaf number (LN), LA, and dry weights of leaves (LFWt), stems (STWt), and aboveground bio-mass (BIO) were determined.

Fig. 1. Daily ultraviolet-B (UV-B) radiation dosages for three UV-B treatments measured at the top of the canopies and lamps placed at 0.5 m above the canopy. Each data point is a mean of three measurements. The UV-B dosage were mea-sured daily at 1000 h and immediately adjusted to the target levels of 5, 10 or 15 kJ m–2 d–1.


Photosynthesis and Fluorescence MeasurementsThese 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 (LI-6400 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 humid-ity 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 fluores-cence (Fm’). Rapid dark adaptation to measure minimal fluores-cence (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 param-eters such as PSII reactions centers under light (Fv’/Fm’), PSII efficiency (fPSII), quantum yield from gas exchange, and non-photochemical quenching (qN) (LI-6400 Instruction Manual, version 5, LI-Cor Inc., Lincoln, NE).

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.

RESULTSUltraviolet-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

Fig. 2. Changes in plant height of corn as affected by ultravi-olet-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.

Table 1. Analysis of variance significance levels for the effect of days after emergence (DAE) and ultraviolet-B radiation (UV-B) on plant height (PH, cm), mainstem leaf number (LN), leaf area (LA, cm–2 plant–1) and dry weights of leaf (LFWt, g plant–1) stem (STWt, g plant–1) and aboveground biomass (BIO, g plant–1).

Source of variation PH LN LA LFWt STWt BIO

Terral-2100DAE *** *** *** *** *** ***UV-B *** *** *** * ** ***DAE × UV-B *** * *** * *** ***

DKC 65-44DAE *** *** *** *** *** ***UV-B *** *** *** *** ** ***DAE × UV-B *** 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.


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 Ter-ral-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 pro-duce 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 treat-ment 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 expan-sion 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

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

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.

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.


(15 DAE); however, the differences in the biomass among three levels of UV-B (5, 10, and 15kJ m–2 d–1) were more obvi-ous 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 radia-tion 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

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 measure-ments, 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 treat-ments 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 effi-ciency (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 radia-tion; 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

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).


radiation on these parameters were more pronounced in Ter-ral-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 treat-ment. 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 param-eters. 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 fol-lowed 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 pho-tosynthetic 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).

DISCUSSIONThrough this study and for the first time, UV-B stress

response indices for various growth and photosynthetic parame-ters for corn are provided which could be used to improve exist-ing 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 experi-ments were comparable for many traits. The whole plant and leaf

Table 2. Effect of ultraviolet-B (UV-B) radiation on photosynthesis (Pn), conductance (gs), internal CO2 concentration (Ci), transpi-ration (Tr), and instantaneous water-use efficiency (WUE, Pn/Tr) of uppermost fully expanded leaf recorded at two different times of corn growth and development.

DAE†

UV-B Pn gs Ci Tr WUE

kJ m–2 d–1 µmol CO2 m–2 s–1 mol H2O m–2 s–1 µmol CO2 mol –1 mmol H2O m–2 s–1 µmol CO2 mmol–1 H2O

Terral-210024 0 48.4 0.297 77.1 7.39 6.58

5 47.8 0.285 66.8 7.09 6.7810 41.2 0.245 76.2 6.12 6.7315 36.3 0.196 47.4 5.00 7.24

31 0 49.2 0.342 108.1 8.21 6.075 39.8 0.278 98.2 7.10 5.67

10 32.7 0.208 90.9 5.94 5.5015 25.3 0.140 58.5 3.90 6.50

ANOVADAE * ns‡ ns ns ***UV-B *** * ns ** *

DAE ´ UV-B ns ns ns ns ns

DKC 65–4424 0 38.57 0.225 107.07 6.76 5.71

5 45.33 0.288 125.23 8.31 5.4810 40.60 0.245 114.17 7.33 5.5515 37.17 0.217 105.63 6.11 6.09

31 0 46.17 0.304 137.77 5.17 8.985 46.77 0.339 154.20 6.24 7.63

10 45.60 0.274 108.77 5.84 7.9115 40.50 0.241 114.33 5.17 7.87

ANOVADAE * * ns *** ***UV-B *** * ns ** nsDAE ´ UV-B ns ns 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.


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 radia-tion. 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 pro-duction of new leaves, the duration of area expansion of each leaf,

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 obser-vations also were made in other studies using different hybrids of corn (Correia et al., 1999; Mark and Tevini, 1997). The inter-nal 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 vari-ous 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 reduc-tion factors or indices were developed in this study. All the indices, ranging from zero when the UV-B stress is totally lim-iting 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 pro-cesses 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 interfer-ence 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 environ-mental 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

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 upper-most fully expanded leaf recorded at two different times of corn growth and development.

DAE UV-B Fv’/Fm’ fPSII fCO2 qN

Terral-210024 0 0.4903 0.2880 0.0390 1.986

5 0.4533 0.2893 0.0387 1.83610 0.4683 0.2997 0.0340 1.88215 0.4367 0.2737 0.0293 1.787

31 0 0.5263 0.3033 0.0390 2.1225 0.5000 0.2787 0.0323 2.004

10 0.4247 0.2690 0.0260 1.74215 0.3530 0.2290 0.0203 1.547

ANOVADAE ns† ns * nsUV-B ** ns ** **

DAE ´ UV-B ns ns ns ns

DKC 65–4424 0 0.5307 0.3177 0.0313 2.132

5 0.5603 0.3213 0.0367 2.28210 0.5720 0.3040 0.0330 2.34815 0.5070 0.3060 0.0300 2.037

31 0 0.5200 0.3357 0.0370 2.0855 0.5607 0.3430 0.0377 2.293

10 0.5173 0.3390 0.0370 2.07715 0.5077 0.3157 0.0323 2.034

ANOVADAE ns * *** nsUV-B * ns *** *DAE ´ UV-B 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.


Fig. 7. Ultraviolet-B radiation indices for various growth, de-velopmental, and physiological processes of corn hybrid DKC 65-44. Other details are as in Fig. 5.

Fig. 6. Ultraviolet-B radiation indices for various growth, de-velopmental and physiological processes of corn hybrid Ter-ral-2100. Fv’/Fm’ is the efficiency of energy harvesting by oxi-dized (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.

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.

Plant parameters

Regression parameters

P valueCoefficient of

determination (r2)Critical limit

UV-B a b c

Terral-2100Leaf development 1.0196 –0.0060 0.289 0.51 >20.0Leaf area expansion 0.9737 –0.0431 0.014 0.97 1.7Stem extension 0.9673 –0.0376 0.016 0.97 1.8Biomass production 1.0448 –0.0359 0.049 0.99 4.0Photosynthesis 1.0254 –0.0304 0.010 0.97 4.2Conductance 1.033 –0.0313 0.028 0.94 4.2

fPSII 1.0158 –0.0254 0.006 0.99 4.5Fv’/Fm’ 1.0042 –0.0136 0.011 0.96 7.6qN 1.0004 –0.0125 0.002 0.99 8.0

DKC 65-44Leaf development 0.9883 –0.0017 0.387 0.38 >20.0Leaf area expansion 1.0080 –0.0139 0.049 0.90 7.8Stem extension 0.9931 –0.0261 0.008 0.97 3.5Biomass production 1.0038 –0.0138 0.017 0.98 7.5Photosynthesis 0.0231 –0.0020 1.005309 0.200 0.96 14.8Conductance 0.0362 –0.0033 1.021819 0.440 0.81 13.6

fPSII 0.0043 –0.0005 1.002212 0.206 0.96 19.2Fv’/Fm’ 0.0189 –0.0015 1.002145 0.134 0.98 16.6qN 0.0235 –0.0018 1.002896 0.140 0.98 16.5


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 Ter-ral-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 sen-sitivity 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 devel-opmental 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 lat-ter 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 some-what 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 devel-opment and photosynthesis leading to decrease in biomass pro-duction. 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 photosynthe-sis parameters, leaf and stem growth will account for most of the UV-B effects on corn growth and development. The identi-fied 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, Mis-sissippi Agricultural and Forestry Experiment Station, paper no. 12143.

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quantifying the effects of corn growth and physiological responses

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