Barry A. Logan

Acclimation of foliar antioxidant systems to growth irradiance in three broad-leaved evergreen species

The protective role of leaf antioxidant systems in the mechanism of plant acclimation to growth irradiance was studied in Vinca major, Schefflera arboricola, and Mahonia repens, which were grown for several months at 20, 100, and 1200 [mu]mol photons m-2 s-1. As growth irradiance increased, several constituents of the “Mehler-peroxidase” pathway also increased: superoxide dismutase, ascorbate peroxidase, glutathione reductase, ascorbate, and glutathione. This occurred concomitantly with increases in the xanthophyll cycle pool size and in the rate of nonphotochemical energy dissipation under steady-state conditions. There was no evidence for photosystem II overreduction in plants grown at high irradiance, although the reduction state of the stromal NADP pool, estimated from measurements of NADP-malate dehydrogenase activity, was greater than 60% in V. major and S. arboricola. Ascorbate, which removes reactive O2 species generated by O2 photoreduction in the chloroplast and serves as a reductant for the conversion of the xanthophyll cycle pigments to the de-epoxidized forms A plus Z, generally exhibited the most dramatic increases in response to growth irradiance. We conclude from these results that O2 photoreduction occurs at higher rates in leaves acclimated to high irradiance, despite increases in xanthophyll cycle-dependent energy dissipation, and that increases in leaf antioxidants protect against this potential oxidative stress.

Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments

Abstract We investigated differences between summer and winter in photosynthesis, xanthophyll cycle-dependent energy dissipation, and antioxidant systems in populations of Mahonia repens (Lindley) Don growing in the eastern foothills of the Colorado Rocky Mountains in deep shade, full exposure, and under a single-layered canopy of Pinus ponderosa (partially shaded). In summer, increasing growth irradiance (from deep shade to partial shade to full exposure) was associated with increased xanthophyll cycle-dependent energy dissipation in PSII and an increased capacity to detoxify reactive reduced oxygen species, as measured by increases in the activities of ascorbate peroxidase, superoxide scavenging, glutathione reductase, and monodehydroascorbate reductase, as well as increases in leaf ascorbate and glutathione content. Leaves of exposed and partially shaded plants exhibited decreased capacities for photosynthetic O2 evolution in winter compared to summer, while in the deeply shaded plants this parameter did not differ seasonally. Seasonal differences in the levels of antioxidants generally exhibited an inverse response to photosynthesis, being higher in winter compared to summer in the exposed and partially shaded populations, but remaining unchanged in the deeply shaded population. In addition, total pool size and conversion state of the xanthophyll cycle were higher in winter than in summer in all populations. These trends suggest that both xanthophyll cycle-dependent energy dissipation in PSII and the capacity to detoxify reactive reduced oxygen species responded to the level of excess light absorption.

Biochemistry and physiology of foliar isoprene production

Leaves of some plants emit isoprene, a volatile hydrocarbon. This is formed by a novel chloroplastic isoprenoid biosynthetic pathway, the 1-deoxy-D-xylulose-5-phosphate pathway. The thermoprotection hypothesis suggests that isoprene protects thylakoids from damage at high temperatures. In this article, we discuss the most recent discoveries about the metabolic pathway underlying isoprene biosynthesis, explore the experimental evidence surrounding thermoprotection and advance some alternative hypotheses about the adaptive role that isoprene biosynthesis might play.

Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics.

Abstract. The long-term effect of limiting soil nitrogen (N) availability on foliar antioxidants, thermal energy dissipation, photosynthetic and respiratory electron transport, and carbohydrates was investigated in Spinacia oleracea L. Starch, sucrose, and glucose accumulated in leaves of N-limited spinach at predawn, consistent with a downregulation of chloroplast processes by whole-plant sink limitation in response to a limited supply of N-based macromolecules throughout the plant. On a leaf-area or dry-weight basis, levels of chlorophyll, carotenoid pools, photosynthetic electron transport capacity, as well as activities for the predominantly chloroplast-localized antioxidant enzymes ascorbate peroxidase (EC 1.11.1.11) and glutathione reductase (EC 1.6.4.2) were much lower in N-limited versus N-replete plants. When expressed on a chlorophyll basis, foliar levels of all of these parameters were similar in N-replete versus N-limited plants. However, on a total-protein basis, antioxidant enzyme activities were higher in N-limited plants. Nitrogen-limited spinach showed higher levels of thermal energy dissipation and of zeaxanthin and antheraxanthin at midday, as well as slightly higher ascorbate contents relative to chlorophyll. These results indicate that strong, long-term N limitation led not only to alterations in the balance between different processes but also to an overall downregulation of light collection, photosynthetic electron transport capacity, and chloroplast-based antioxidant enzymes. This is further supported by the finding that glucose-feeding of excised leaves led to strong concomitant decreases in photosynthetic electron transport capacity and ascorbate peroxidase activity. On a leaf-area basis, neither superoxide dismutase (EC 1.15.1.1) activity nor dark repiration rates showed a treatment effect. This indicates that overall mitochondrial electron transport activity does not decrease under long-term N limitation and is consistent with localization of an important fraction of foliar superoxide dismutase in mitochondria.

Ecophysiology of the Xanthophyll Cycle

This chapter seeks to illustrate the impressive range of environmental modulation of the xanthophyll cycle in terrestrial plants in their natural habitats, where the demand for thermal energy dissipation can change within seconds or between seasons and vary from a moderate to a very large fraction of the absorbed light. Plants from habitats with concomitant xanthophyll cycle conversions and changes in energy dissipation activity are included as well as examples from habitats in which zeaxanthin and antheraxanthin (Z+A) persist and energy dissipation is modulated largely via their rapid engagement and disengagement. The well-characterized, rapidly inducible and reversible form of xanthophyll cycle-dependent energy dissipation is contrasted with the sustained maintenance of higher levels of (Z+A)-dependent thermal dissipation under various environmental stresses with an emphasis on seasonally low temperatures. Furthermore, the association of Z+A retention with the phenomenon of photoinhibition of Photosystem II (and alterations in the stoichiometry of proteins associated with PS II) is discussed as well as a possible involvement of thylakoid protein phosphorylation in sustained (Z+A)-dependent energy dissipation. An integrative understanding is sought by comparing acclimation patterns of thermal energy dissipation as well as overall foliar antioxidant capacity with those of photosynthetic and respiratory metabolism of whole plants. It is proposed that acclimation of all of these processes responds to whole plant source-sink relationships.

The role of antioxidant enzymes in photoprotection

The enzymatic component of the antioxidant system is discussed as one of the defensive mechanisms providing protection against excessive light absorption in plants. We present an analysis of attempts to improve stress tolerance by means of the creation of transgenic plants with elevated antioxidant enzyme activities and conclude that the effect of such transgenic manipulation strongly depends on the manner in which the stress is imposed. The following factors may diminish the differences in photosynthetic performance between transgenic plants and wild type under field conditions: effective functioning of the thermal dissipation mechanisms providing a primary line of defense against excessive light, long-term adjustments of the antioxidant system and other photoprotective mechanisms, the relatively low level of control over electron transport exerted by the Water–Water cycle, especially under warm conditions, and a decrease in the content of the transgenic product during leaf aging.

Positive correlation between levels of retained zeaxanthin + antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill

Abstract. Attached intact leaves of Schefflera arboricola grown at three different photon flux densities (PFDs) were subjected to 24-h exposures to a high PFD and subsequent recovery at a low PFD. While sun leaves showed virtually no sustained effects on photosystem II (PSII), shade-grown leaves exhibited pronounced photoinhibition of PSII that required several days at low PFD to recover. Upon transfer to high PFD, levels of nonphotochemical quenching in PSII as well as levels of zeaxanthin were initially low in shade leaves but continued to increase gradually during the 24-h exposure. The xanthophyll cycle pool size rose gradually during and also subsequent to the photoinhibitory treatment in shade leaves. Upon return to low PFD, a marked and extremely long-lasting retention of zeaxanthin and antheraxanthin was observed in shade but not sun leaves. During recovery, changes in the conversion state of the xanthophyll cycle therefore closely mirrored the slow increases in PSII efficiency. This novel report of a close association between zeaxanthin retention and lasting PSII depressions in these shade leaves clearly suggests a role for zeaxanthin in photoinhibition of shade leaves. In addition, there was a decrease in β-carotene levels, some decrease in chlorophyll, but no change in lutein and neoxanthin (all per leaf area) in the shade leaves during and subsequent to the photoinhibitory treatment. These data may be consistent with a degradation of a portion of core complexes but not of peripheral light-harvesting complexes. A possible conversion of β-carotene to form additional zeaxanthin is discussed.

Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature.

The unabated rise in atmospheric [CO(2)] is associated with increased air temperature. Yet, few CO(2)-enrichment studies have considered pre-industrial [CO(2)] or warming. Consequently, we quantified the interactive effects of growth [CO(2)] and temperature on photosynthesis of faster-growing Eucalyptus saligna and slower-growing E. sideroxylon. Well-watered and -fertilized tree seedlings were grown in a glasshouse at three atmospheric [CO(2)] (290, 400, and 650 µL L(-1)), and ambient (26/18 °C, day/night) and high (ambient + 4 °C) air temperature. Despite differences in growth rate, both eucalypts responded similarly to [CO(2)] and temperature treatments with few interactive effects. Light-saturated photosynthesis (A(sat)) and light- and [CO(2)]-saturated photosynthesis (A(max) ) increased by ∼ 50% and ∼ 10%, respectively, with each step-increase in growth [CO(2)], underpinned by a corresponding 6-11% up-regulation of maximal electron transport rate (J(max)). Maximal carboxylation rate (V(cmax)) was not affected by growth [CO(2)]. Thermal photosynthetic acclimation occurred such that A(sat) and A(max) were similar in ambient- and high-temperature-grown plants. At high temperature, the thermal optimum of A(sat) increased by 2-7 °C across [CO(2)] treatments. These results are the first to suggest that photosynthesis of well-watered and -fertilized eucalypt seedlings will remain strongly responsive to increasing atmospheric [CO(2)] in a future, warmer climate.

Inter- and intra-specific variation in nocturnal water transport in Eucalyptus

To identify environmental and biological drivers of nocturnal vapour exchange, we quantified intra-annual, intra- and inter-specific variation in nocturnal water transport among ecologically diverse Eucalyptus species. We measured sap flux (J(s)) and leaf physiology (leaf surface conductance (g(s)), transpiration (E) and water potential (Psi(l))) in three to five trees of eight species. Over 1 year, nocturnal J(s) (J(s,n)) contributed 5-7% of total J(s) in the eight species. The principal environmental driver of J(s,n) was the product of atmospheric vapour pressure deficit (D) and wind speed (U). Selected observations suggest that trees with higher proportions of young foliage may exhibit greater J(s,n) and nocturnal g(s) (g(s,n)). Compared with other tree taxa, nocturnal water use in Eucalyptus was relatively low and more variable within than between species, suggesting that (i) Eucalyptus as a group exerts strong nocturnal stomatal control over water loss and (ii) prediction of nocturnal flux in Eucalyptus may depend on simultaneous knowledge of intra-specific tree traits and nocturnal atmospheric conditions.

Elevated chloroplastic glutathione reductase activities decrease chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cotton

The effect of the overproduction of glutathione reductase (GR+) in cotton (Gossypium hirsutum L. cv.Coker 312) chloroplasts on the response of photosynthetic parameters to chilling in the light was examined. After 180 min at 10°C and 500 μmol photons m-2 s-1 in the chamber of an oxygen electrode, leaf discs of GR+ plants exhibited lower levels of sustained PSII photoinhibition than leaf discs of wild-type plants. No genotypic differences in thermal energy dissipation, leaf pigment composition, or the dynamics of xanthophyll cycle de-epoxidation were observed. The rate of induction and steady-state levels of photochemistry were greater for GR+ in comparison to wild-type plants. Enhanced photochemistry in GR+ plants could not be attributed to higher rates of CO2 assimilation at 10°C. Although GR overproduction afforded some increased protection against PSI photoinactivation, suggesting improved scavenging of reactive oxygen species, higher PSI activities could not completely explain the greater rates of photochemistry. Pools of glutathione and ascorbate were significantly more reduced in GR+ plants. Increased demand for reducing power to maintain these constituents in the reduced state may contribute to the higher rates of photochemistry observed in GR+ plants.