Impaired auxin signaling increases vein and stomatal density but reduces hydraulic efficiency and ultimately net photosynthesis

Auxins are known to regulate xylem development in plants, but their effects on water transport efficiency are poorly known. Here we used tomato plants with the diageotropica mutation (dgt), which has impaired function of a cyclophilin 1 cis-trans isomerase involved in auxin signaling, and the corresponding wild type (WT) to explore the mutation's effects on plant hydraulics and leaf gas exchange. The xylem of the dgt mutant showed a reduced hydraulically weighted vessel diameter (D-h) (24-43%) and conduit number (25-58%) in petioles and stems, resulting in lower theoretical hydraulic conductivities (K-t); on the other hand, no changes in root D-h and K-t were observed. The measured stem and leaf hydraulic conductances of the dgt mutant were lower (up to 81%), in agreement with the K-t values; however, despite dgt and WT plants showing similar root D-h and K-t, the measured root hydraulic conductance of the dgt mutant was 75% lower. The dgt mutation increased the vein and stomatal density, which could potentially increase photosynthesis. Nevertheless, even though it had the same photosynthetic capacity as WT plants, the dgt mutant showed a photosynthetic rate c. 25% lower, coupled with a stomatal conductance reduction of 52%. These results clearly demonstrate that increases in minor vein and stomatal density only result in higher leaf gas exchange when accompanied by higher hydraulic efficiency. The tomato diageotropicamutant, with impaired auxin signaling, exhibits increased leaf vein and stomatal density; however, an intrinsic compromised hydraulic efficiency counteracts this positive effect and, ultimately, reduces its net photosynthesis.