Abstract
The alternative oxidase pathway (AOP) is associated with excess energy dissipation in leaves of terrestrial plants. To address whether this association is less important in palustrine plants, we compared the role of AOP in balancing energy and carbon metabolism in palustrine and terrestrial environments by identifying metabolic relationships between primary carbon metabolites and AOP in each habitat. We measured oxygen isotope discrimination during respiration, gas exchange, and metabolite profiles in aerial leaves of ten fern and angiosperm species belonging to five families organized as pairs of palustrine and terrestrial species. We performed a partial least square model combined with variable importance for projection to reveal relationships between the electron partitioning to the AOP (τa) and metabolite levels. Terrestrial plants showed higher values of net photosynthesis (AN) and τa, together with stronger metabolic relationships between τa and sugars, important for water conservation. Palustrine plants showed relationships between τa and metabolites related to the shikimate pathway and the GABA shunt, to be important for heterophylly. Excess energy dissipation via AOX is less crucial in palustrine environments than on land. The basis of this difference resides in the contrasting photosynthetic performance observed in each environment, thus reinforcing the importance of AOP for photosynthesis.
Highlights
Current life on Earth would not be possible without the evolution of biochemical processes that maintained energy entry in plants during land colonization (Delwiche and Cooper, 2015; De Vries et al, 2016; De Vries and Archibald, 2018; Gago et al, 2019)
In order to assess the abundance of both terrestrial and palustrine plant species in locations and biomes with different environmental conditions, we studied the spatial distribution of these species considering data of mean annual temperature (MAT) and mean annual precipitation (MAP) from the years 1980 to 2010
WUE is primarily controlled by evaporation; whilst in sub-humid regions, WUE is mostly regulated by assimilation (Yang R. et al, 2016), which could be partly due to a different predominance of palustrine and terrestrial records displaying contrasting values of WUEi (Figure 1 and Figure 2C) agreeing with the idea of water losses acting as a driving force for the evolution in land plants of gas exchange regulation system (Raven, 2002; Berry et al, 2010; Assouline and Or, 2013)
Summary
Current life on Earth would not be possible without the evolution of biochemical processes that maintained energy entry in plants during land colonization (Delwiche and Cooper, 2015; De Vries et al, 2016; De Vries and Archibald, 2018; Gago et al, 2019). The earliest terrestrial plant ancestor, a charophycean alga, emerged from water approximately 500 million years ago AOX Activity in Different Habitats (Bhattacharya and Medlin, 1998; Yoon et al, 2004; Harholt et al, 2016; Morris et al, 2018; Reski, 2018), undergoing physiological, structural, and biochemical changes to cope with the transition from an aqueous to a gaseous medium (Kenrick and Crane, 1997; Pires and Dolan, 2012; Vermeij, 2016). Changes in metabolic pathways favored the synthesis of phenolic compounds, lignin, plant hormones, isoprenes, heat shock proteins or superoxide dismutase to favor photosynthetic performance and plant growth under a highly stressful terrestrial environment (Lowry et al, 1980; Kenrick and Crane, 1997; Waters, 2003; Weng and Chapple, 2010; Bowman et al, 2017). The antioxidant systems were enhanced in land plants allowing them to survive several deleterious types of environmental stresses worldwide that induce oxidative stress and damage to the photosynthetic apparatus (Asada, 2006; Thomas et al, 2008; Gill and Tuteja, 2010; Zandalinas et al, 2021)
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