Ozone depletion and UVB radiation: impact on plant DNA damage in southern South America

Abstract

The primary motivation behind the considerable effort in studying stratospheric ozone depletion is the potential for biological consequences of increased solar UVB (280-315 nm) radiation. Yet, direct links between ozone depletion and biological impacts have been established only for organisms of Antarctic waters under the influence of the ozone "hole;" no direct evidence exists that ozone-related variations in UVB affect ecosystems of temperate latitudes. Indeed, calculations based on laboratory studies with plants suggest that the biological impact of ozone depletion (measured by the formation of cyclobutane pyrimidine dimers in DNA) is likely to be less marked than previously thought, because UVA quanta (315-400 nm) may also cause significant damage, and UVA is unaffected by ozone depletion. Herein, we show that the temperate ecosystems of southern South America have been subjected to increasingly high levels of ozone depletion during the last decade. We found that in the spring of 1997, despite frequent cloud cover, the passages of the ozone hole over Tierra del Fuego (55 degrees S) caused concomitant increases in solar UV and that the enhanced ground-level UV led to significant increases in DNA damage in the native plant Gunnera magellanica. The fluctuations in solar UV explained a large proportion of the variation in DNA damage (up to 68%), particularly when the solar UV was weighted for biological effectiveness according to action spectra that assume a sharp decline in quantum efficiency with increasing wavelength from the UVB into the UVA regions of the spectrum.

Figure 1

Ozone depletion and springtime UV levels over Ushuaia. (A) Increase in the number of ozone-hole days over Ushuaia during the past 2 decades. The graph shows the number of days with column ozone values ≤250 DU between Oct. 1 and Nov. 30 for each year. Data were obtained from the Overpass Data file on the internet TOMS site (http://jwocky.gsfc.nasa.gov/TOMSmain.html). No data are available for 1995, and a limited data set is available for October 1993; therefore, these two years are not included in the graph. (B–F) Effects of the passage of the Antarctic ozone hole over Tierra del Fuego on ground-level UV doses during October and November 1997. The spectral irradiances obtained by the National Science Foundation scanning spectroradiometer were converted into effective irradiances by using several weighting functions and integrated over the 9:00–13:30 h time period (■, effective UV dose; ▴, ozone column in Dobson units). The r² values shown in each panel are from a multiple linear regression model that incorporated Julian day and ozone level as independent variables; in all cases, the ozone term was statistically significant. A comparison of the Erythema-weighted UV doses calculated from spectral irradiance data in Ushuaia with those measured in the field site with a broad-band UV detector (Solar Light, Philadelphia, model PMA2102) indicated a significant linear correlation (r² = 0.77; 22 data points; November 1997; integration period 9:30–13:30 h).

Figure 2

Ozone depletion and DNA damage. (A) Map of the southern tip of South America and Tierra del Fuego showing the area under the Antarctic ozone hole on Oct. 14 and 17, 1997. (B) Premidday UV doses (weighted by using Setlow's action spectrum). (C) CPD density per nanogram of DNA in leaves of naturally occurring plants of G. magellanica measured at midday (full-UV treatment); 1 unit of DNA damage is defined as the number of CPD produced by 1 J⋅m⁻² of 254-nm radiation on 1 ng of purified DNA. Nonirradiated DNA gave no signal in the blots. Each bar is the average of five true replicates.

Figure 3

CPD density per nanogram of DNA in leaves of G. magellanica plants as a function of the premidday effective UV dose (A–E); 1 unit of DNA damage is defined as the number of CPD produced by 1 J⋅m⁻² of 254-nm radiation on 1 ng of purified DNA. Plants are from the full-UV treatment. (F) Relationship between the goodness of fit of the various “DNA damage/UV dose” correlations (A–E) and the radiation amplification factor (RAF) of the weighting function estimated for 30°N latitude, the month of July, and an ozone column of 305 DU (RAF data obtained from ref. and S. Madronich, personal communication).

Figure 4

CPD density per nanogram of DNA in leaves of G. magellanica plants from the full-UV (▴) and −UVB (■) treatments as a function of the effective premidday UV dose; 1 unit of DNA damage is defined as the number of CPD produced by 1 J⋅m⁻² of 254-nm radiation on 1 ng of purified DNA. The UV doses were estimated from measurements of the spectral transmittance of the filters and by using Setlow's action spectrum as a weighting function.