The apoplastic antioxidant system and altered cell wall dynamics influence mesophyll conductance and the rate of photosynthesis

• Published in: The Plant journal : for cell and molecular biology 2019-09, Vol.99 (6), p.1031-1046
• Main Authors: Clemente‐Moreno, María José, Gago, Jorge, Díaz‐Vivancos, Pedro, Bernal, Agustina, Miedes, Eva, Bresta, Panagiota, Liakopoulos, Georgios, Fernie, Alisdair R., Hernández, José Antonio, Flexas, Jaume
• Format: Article
• Language: English
• Subjects: Antioxidants; Antioxidants - metabolism; Apoplast; Breeding; Carbon dioxide; Carbon Dioxide - metabolism; Carboxylation; Catalase - metabolism; cell wall; Cell Wall - chemistry; Cell Wall - metabolism; Cell walls; Chlorophyll - metabolism; Chloroplasts; Composition; Conductance; Diffusion rate; Drought; Droughts; Galactose; Glucosamine; Hydrogen Peroxide - metabolism; Mesophyll; Mesophyll Cells - metabolism; mesophyll conductance; Metabolic response; Metabolism; Metabolites; Multienzyme Complexes - metabolism; NADH, NADPH Oxidoreductases - metabolism; Nicotiana - enzymology; Nicotiana - metabolism; Nicotiana sylvestris; Pectin; Peroxidase - metabolism; Photosynthesis; Photosynthesis - physiology; Plant Leaves - anatomy & histology; Plant Leaves - metabolism; Plant Stomata - metabolism; Plant Stomata - physiology; reactive oxygen species; Resistance; Salinity; Stress; stress responses; Superoxide Dismutase - metabolism; Tobacco
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.14437

Summary Mesophyll conductance (gm), the diffusion of CO2 from substomatal cavities to the carboxylation sites in the chloroplasts, is a highly complex trait driving photosynthesis (net CO2 assimilation, AN). However, little is known concerning the mechanisms by which it is dynamically regulated. The apoplast is considered as a ‘key information bridge’ between the environment and cells. Interestingly, most of the environmental constraints affecting gm also cause apoplastic responses, cell wall (CW) alterations and metabolic rearrangements. Since CW thickness is a key determinant of gm, we hypothesize that other changes in this cellular compartiment should also influence gm. We study the relationship between the antioxidant apoplastic system and CW metabolism and the gm responses in tobacco plants (Nicotiana sylvestris L.) under two abiotic stresses (drought and salinity), combining in vivo gas‐exchange measurements with analyses of antioxidant activities, CW composition and primary metabolism. Stress treatments imposed substantial reductions in AN (58–54%) and gm (59%), accompanied by a strong antioxidant enzymatic response at the apoplastic and symplastic levels. Interestingly, apoplastic but not symplastic peroxidases were positively related to gm. Leaf anatomy remained mostly stable; however, the stress treatments significantly affected the CW composition, specifically pectins, which showed significant relationships with AN and gm. The treatments additionally promoted a differential primary metabolic response, and specific CW‐related metabolites including galactose, glucosamine and hydroxycinnamate showed exclusive relationships with gm independent of the stress. These results suggest that gm responses can be attributed to specific changes in the apoplastic antioxidant system and CW metabolism, opening up more possibilities for improving photosynthesis using breeding/biotechnological strategies. Significance Statement Mesophyll conductance is a complex trait which imposes considerable limitations on photosynthesis. However, beyond the current knowledge from gas‐exchange measurements and anatomical characterization, the mechanisms driving its dynamic response to the environment are still poorly understood. Here, we relate changes in apoplastic antioxidant metabolism, cell wall composition and primary metabolism with responses of mesophyll conductance to different abiotic stresses. This information improves our understanding about mesophyll conductance res