Table 1 Review of previous studies (references) of structural markers of oxidative stress and indications of the physiological processes triggered by O3 in symptomatic foliage samples completed by new results with sound pictures Figs. 3, 4, 5, and 6
From: Macro- and microscopic leaf injury triggered by ozone stress in beech foliage (Fagus sylvatica L.)
Visible injury | Compartment | Structural marker | Affected tissues | Figure | Physiological process | Contribution to visible injury | References*; species; ambient (a) or artificially elevated (e) O3 |
|---|---|---|---|---|---|---|---|
Photobleaching and bronzing | Leaf blade | Severity of cell injury increasing adaxially£ | Primarily the mesophyll | Photooxidative stress | Discoloration of adaxial and sun-exposed leaf areas | Alvarez 1998 Abies religiosa (a); Moura et al. 2011 Ipomoea nil (e) | |
|  | Cell | Condensation of cytoplasm and nucleus£,§ | All | Acceleration of plant senescence (ACS) | – | Günthardt-Goerg and Vollenweider 2007 various species (a) and (e); Vollenweider et al. 2003 Robinia pseudoacacia (a) | |
|  | Chloroplast | Decrease in size£,§ | Mesophyll, primarily the palisade parenchyma | ACS | Discoloration of leaf areas (bleaching) | Günthardt-Goerg and Vollenweider 2007; Kivimäenpää et al. 2005 Pinus sylvestris, Picea abies (a) and (e) | |
|  |  | Degradation of grana and thylakoids£,§ | Mesophyll | Oxidative stress; ACS | Discoloration of leaf areas (bleaching) | Günthardt-Goerg and Vollenweider 2007; Holopainen et al. 1996 Pinus sylvestris, Picea abies (e); Inada et al. 1998 Oryza sativa (a) | |
|  |  | Increased plastoglobule size and density (epidermis: within leucoplasts)£,§ | All | ACS | Discoloration of leaf areas (bleaching) | Bréhélin et al. 2007 (a); Mikkelsen and Heide-Jørgensen 1996 Fagus sylvatica (a) and (e) | |
|  | Mitochondria | Degradation of inner membrane and matrix£ | All | Oxidative stress | – | Jones 2000 PCD eucaryotes; Vollenweider et al. 2013 Pinus ponderosa (a) | |
|  | Vacuome | Increase in size£,§ | Mesophyll | ACS | – | Mikkelsen and Heide-Jørgensen 1996; Inada et al. 1998; Paoletti et al. 2010 Fraxinus ornus (a) and (e) | |
|  |  | Accumulation of condensed tannins£,§ | All, especially the palisade parenchyma | Oxidative stress; ACS | Discoloration of leaf areas (bronzing) | Bussotti et al. 1998 Fagus sylvatica (a); Oksanen et al. 2001 Populus tremuloides (e); Reig-Armiñana et al. 2004 Pistacia lentiscus (e) | |
|  |  | Oxidation of condensed tannins (tannin plugs) £,§ | Upper palisade parenchyma | Photooxidative stress | Discoloration of leaf areas (bronzing) | Calderón Guerrero et al. 2013 Quercus ilex (a); Vollenweider et al. 2003 (various species) | |
Stippling | Leaf blade | Discretely distributed groups of cytorrhyzed cells | Primarily the upper and sometimes lower palisade parenchyma | Hypersensitive response-like (HR-like) | Formation of tiny dark stipples | Gravano et al. 2004 Fraxinus excelsior (a); Günthardt-Goerg and Vollenweider 2007; Vollenweider et al. 2003 | |
|  | Mesophyll | Leakage of cellular material into the apoplast | Upper palisade | HR-like | – | Calderón Guerrero et al. 2013; McQuattie and Schier 1993 Pinus rigida (e) | |
|  | Cells | Disruption of cell content, incomplete degradation of cell organelles and condensation of aggregated cellular remnants# | Primarily the upper and sometimes the lower palisade parenchyma | Hallmark of programmed cell death during apoptosis and HR-like | – | Levine et al. 1996 Glycine max (a); Günthardt-Goerg and Vollenweider 2007 | |
|  | Nucleus | Sizable shrinkage, condensation and deformation (pyknotic nucleus)# | Primarily the upper and sometimes the lower palisade parenchyma | Hallmark of programmed cell death during apoptosis and HR-like | – | Günthardt-Goerg and Vollenweider 2007; Jones 2000; Pasqualini et al. 2003 Nicotiana tabaccum (e) | |
|  | Chloroplast | Condensation, deformation, advanced membrane injury# | Primarily the upper and sometimes the lower palisade parenchyma | ROS production and injury during HR-like | Dot-like discoloration | Kangasjärvi 2005 Arabidopsis (e); Yamasaki et al. 1997 Schefflera arboricola (a); Vollenweider et al. 2013 | |
|  | Vacuome | Tonoplast disruption# | Primarily the upper and sometimes the lower palisade parenchyma | Cell death; mechanistically linked to cell cytorrhysis | – | Jones 2000 | |
|  |  | Accumulation of vacuolar lipids | Mesophyll | Dysfunction of hydrolytic capacity shortly before cell death | – | Mikkelsen and Heide-Jørgensen 1996; Vollenweider et al. 2013 | |
Necrotic dots | Leaf blade | Large groups of alternating strands of cells, either cytorrhyzed and disrupted or degenerated | All; worse injury in lower mesophyll | HR-like and ACS following acute O3 exposure | Formation of yellowish dots | Faoro and Iriti 2009 Phaseolus vulgaris (e) | |
|  |  | Leakage of cellular remnants into the intercellular space | Mesophyll | HR-like | – |