Hydraulic basis for the evolution of photosynthetic productivity

Abstract

Clarifying the evolution and mechanisms for photosynthetic productivity is a key to both improving crops and understanding plant evolution and habitat distributions. Current theory recognizes a role for the hydraulics of water transport as a potential determinant of photosynthetic productivity based on comparative data across disparate species. However, there has never been rigorous support for the maintenance of this relationship during an evolutionary radiation. We tested this theory for 30 species of Viburnum, diverse in leaf shape and photosynthetic anatomy, grown in a common garden. We found strong support for a fundamental requirement for leaf hydraulic capacity (Kleaf) in determining photosynthetic capacity (Amax), as these traits diversified across this lineage in tight coordination, with their proportionality modulated by the climate experienced in the species' range. Variation in Kleaf arose from differences in venation architecture that influenced xylem and especially outside-xylem flow pathways. These findings substantiate an evolutionary basis for the coordination of hydraulic and photosynthetic physiology across species, and their co-dependence on climate, establishing a fundamental role for water transport in the evolution of the photosynthetic rate.

Linking Auxin with Photosynthetic Rate via Leaf Venation

“…Asterisks denote a significant difference in means (P , 0.001). Scoffoni et al, 2015Scoffoni et al, , 2016. Recently, the influence of the distance through the mesophyll for water flow on K leaf was demonstrated experimentally using a genetic approach (Caringella et al, 2015), and here we present genetic evidence that auxin, through leaf venation, acts as a regulator of both maximum leaf hydraulic supply and maximum A, and likely whole plant productivity.…”

“…This increase in vein density is correlated with an equally substantial increase in maximum A across extant lineages that diverged during this major transition in leaf anatomy. Similar correlations between vein density, K leaf , and A can be observed within angiosperms Carins Murphy et al, 2012;Scoffoni et al, 2015Scoffoni et al, , 2016.…”

“…The length of this final nonxylem transfer has a major influence on the efficiency of the entire water transport system (Brodribb et al, 2007). Current theory posits that as hydraulic supply is essential for A, a reduction in the mean path length for water flow through the mesophyll will increase leaf hydraulic conductance (K leaf ), which will increase stomatal conductance (g s ) and consequently theoretical maximum A (Sack and Frole, 2006;Brodribb et al, 2007Scoffoni et al, 2011Scoffoni et al, , 2016.…”

“…Of these adaptations, vein density has been a major focus due to the high plasticity of this trait both within species (Carins Murphy et al, 2012;Scoffoni et al, 2015) and across vascular plant taxa (Boyce et al, 2009). Using this variation in vein density, strong correlations have been established between the terminal path length for water flow through the mesophyll and maximum K leaf (Sack and Frole, 2006;Brodribb et al, 2007Scoffoni et al, 2016). These correlations are supported by singlegene vein density mutants in Arabidopsis (Arabidopsis thaliana) and Solanum lycopersicum spanning a spectrum of vein modifications that influence K leaf (Caringella et al, 2015;Zsögön et al, 2015).…”

Stomatal Biology of CAM Plants

“…Variation in stomatal traits appears to be accommodated within a network of coordinated leaf traits in CAM species in the same way as has been observed in C 3 plants (Reich et al, 1997(Reich et al, , 1999Wright et al, 2004Wright et al, , 2005Donovan et al, 2011;Vasseur et al, 2012;Díaz et al, 2016). Recent modeling and empirical studies have highlighted the importance of the alignment of variation in stomatal, xylem, and veinal traits in angiosperms for optimal physiological function (Brodribb et al, 2013(Brodribb et al, , 2016Fiorin et al, 2016;Carins Murphy et al, 2016;Scoffoni et al, 2016). It would be particularly interesting to explore the degree of coordination between Phase I (nighttime) and Phase IV (daytime) stomatal and mesophyll conductances in CAM plants.…”