Effects of elevated ozone on CO₂ uptake and leaf structure in sugar maple under two light environments

Abstract

The interactive effects of ozone and light on leaf structure, carbon dioxide uptake and short-term carbon allocation of sugar maple (Acer saccharum Marsh.) seedlings were examined using gas exchange measurements and 14 Cmacroautoradiographic techniques. Two-year-old sugar maple seedlings were fumigated from budbreak for 5 months with ambient or 3 × ambient ozone in open-top chambers, receiving either 35% (high light) or 15% (low light) of full sunlight. Ozone accelerated leaf senescence, and reduced net photosynthesis, 14 CO 2 uptake and stomatal conductance, with the effects being most pronounced under low light. The proportion of intercellular space increased in leaves of seedlings grown under elevated ozone and low light, possibly enhancing the susceptibility of mesophyll cells to ozone by increasing the cumulative dose per mesophyll cell. Indeed, damage to spongy mesophyll cells in the elevated ozone × low light treatment was especially frequent. 14 C macroautoradioraphy revealed heterogeneous uptake of 14 CO 2 in well defined areole regions, suggesting patchy stomatal behaviour in all treatments. However, in seedlings grown under elevated ozone and low light, the highest 14 CO 2 uptake occurred along larger veins, while interveinal regions exhibited little or no uptake. Although visible symptoms of ozone injury were not apparent in these seedlings, the cellular damage, reduced photosynthetic rates and reduced whole-leaf chlorophyll levels corroborate the visual scaling of whole-plant senescence, suggesting that the ozone × low light treatment accelerated senescence or senescence-like injury in sugar maple. Key-words:Acer saccharum Marsh; leaf morphology; ozone; photosynthesis; shade adaptation; stomatal patchiness; sugar maple. INTRODUCTIONSugar maple (Acer saccharum Marsh.) is a slow-growing, shade-tolerant species that is widely distributed in eastern North America where elevated ozone concentrations occur, and forests may currently be undergoing widespread decline. Because of its high phytotoxicity, ozone probably has the most negative impact of any air pollutant on tree vigour and growth (Reich 1987). Once in the leaf, ozone reacts with water to form oxygen free radicals, H 2 O 2 and hydroxyl ions (Heath 1980;Mehlhorn, Tabner & Wellburn 1990), oxidizes proteins and membrane phospholipids, increases membrane permeability (Mehlhorn et al. 1986) and directly inhibits photosynthesis (Heath 1994). Stromal reactions of photosynthesis are particularly sensitive to ozone, with ozone affecting the quantity and activity of rubisco (Pell, Eckardt & Enyedi 1992). Plant responses to ozone are proportional to ozone uptake, which is a function of atmospheric concentration and stomatal conductance (Laisk, Kull & Moldau 1989). Plants can reduce ozone uptake and minimize internal damage by closing stomata or reducing the size of the stomatal opening, resulting in a decline in stomatal conductance. However, this response may vary within and between species, with stage of leaf development, and be dependent upon atm...

Response to an ozone gradient of growth and enzymes implicated in tolerance to oxidative stress inAcer saccharum(Marsh.) seedlings

“…We conclude that the assimilation rates of the seedlings were not limited by light availability, resulting in a similar total carbon gain and a similar growth rate for seedlings in both light treatments. Leaf morphology, structure and thickness are known to differ with increasing irradiance levels [2,51]. However, in our study, specific leaf mass values were similar at both irradiance levels.…”

“…O 3 is formed by the photochemical reaction between anthropogenic and biogenic nitrogen oxides (NOx), and volatile organic compounds (VOCs) in polluted air masses. In contrast to other gaseous anthropogenic pollutants such as SO 2 , tropospheric O 3 concentration is increasing, probably due to the increase in the levels of NO x and VOC emissions [21]. Increase in global tropospheric O 3 concentration during the 21st century was projected by a range of global emission scenarios studied by the IPCC 2001 assessment.…”

“…Asthon et al [1] have reported that the leaves of young maple seedlings have a great capacity to adapt to different irradiance environments. Topa et al [52] reported that leaves grown in shade show a greater susceptibility to O 3 than leaves grown in higher light environments, which is mainly due to the structural differences of the sun and shade leaves [2,58].…”

Ozone-Induced Changes in Antioxidant Systems of Ginkgo Biloba in Relation to the Developmental Stage of the Leaves

“…It was supposed that remobilization of resource from senescing leaves to younger ones could allow the latter to withstand ozone stress [21], but this hypothesis needs more experiments to test. The increase of intercellular space during leaf development possibly enhanced the susceptibility to ozone by increasing the ozone dose into per cell, as suggested for leaves of sugar maple seedlings [22]. However, Bagard et al demonstrated that the expanding leaves of hybrid poplar showed higher resistance to O 3 with the same uptake of O 3 as the fully expanded leaves, and proposed that further work was needed to ascertain whether the contribution of the antioxidant capability was responsible for the higher resistance of young leaves [18].…”

Effects of elevated [CO2] and O3 on stomatal and surface wax characteristics in leaves of pubescent birch grown under field conditions

“…Ozone may interfere with control of the stomatal aperture and may have the potential to disturb the water balance of the leaf, or even the whole plant (Pearson and Mansfield 1993). Elevated O 3 levels have been shown to influence leaf differentiation during its formation (Frey et al 1996;Bäck et al 1999). Leaf differentiation changed towards xeromorphism, somewhat resembling sun leaves or leaf development under mild drought conditions (Matyssek et al 1991).…”