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

Abstract

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.

Born to revive: molecular and physiological mechanisms of double tolerance in a paleotropical and resurrection plant

“…4c). Although a coupled behaviour between g s and g m is typical during drought recovery and tissue rehydration (Flexas et al , 2012), a significant ‘uncoupling’ ( g m remained more constrained during rehydration than g s ) was found in R. myconi , suggesting important differential biochemical mechanisms driving both g s and g m (Galle et al , 2009; Clemente‐Moreno et al , 2019).…”

How do vascular plants perform photosynthesis in extreme environments? An integrative ecophysiological and biochemical story

“…Under water deficit and salinity, g s and g m can show the same degree of limitation (observed in plants from non‐extreme environments; Flexas et al , ,b), but g m responses can differ in terms of velocity with respect to the stress, as well as during recovery after rewatering in different herbaceous and woody species (Galle et al , , ; Clemente‐Moreno et al , ). A complex behaviour of g m would also be associated with additional environmental stimuli and other traits such as water status and hydraulics (Flexas et al , ; Carriquí et al , ).…”

“…The second issue is mostly related to the cell wall composition and diffusion through the cytosol and stroma (von Caemmerer and Evans, ; Flexas and Díaz‐Espejo, ). Recently, it has been reported that changes in the cell wall composition in response to stress (mostly pectins and hemicelluloses) are negatively correlated with g m , suggesting that the cell wall structure and ionic nature of the cell wall nanopores could influence the CO 2 pathway through the cell wall (Clemente‐Moreno et al , ).…”

“…The only two native vascular plants of Antarctica (Figure c) have been extensively studied in terms of temperature, water availability and nutrient deficiency (Sáez et al , , ,b; Clemente‐Moreno et al , , ). Interestingly, for both species, g m is the most important limitation under low temperature, drought and nutrient deficiency, as has been previously reported for species from semiarid‐arid environments (Galmés et al , ).…”

Photosynthesis and photosynthetic efficiencies along the terrestrial plant’s phylogeny: lessons for improving crop photosynthesis

“…In addition, not only the CWT but also the biochemical composition of cell walls may play roles – possibly opposite – in both CO 2 diffusion and plant water relations/desiccation tolerance. For instance, it has been recently demonstrated that either genetically (Ellsworth et al ., ) or stress‐induced (Clemente‐Moreno et al ., ) modifications in cell wall composition affect g m . Particularly pectins seem to affect negatively g m , possibly due to their anionic nature, but they are also known to be essential for modulating cell wall porosity, increase cell wall rigidity (then possibly ε) and determine the water holding capacity of cell walls (Voragen et al ., ), all of which are characters potentially related to desiccation tolerance.…”