Evidence That Tolerance of Eutrema Salsugineum to Low Phosphate Conditions is Hard-wired by Constitutive Metabolic and Root-associated Adaptations

The extremophyte Eutrema salsugineum (Yukon ecotype) has adapted to an environment low in available phosphate through metabolic and root-associated traits that enables it to efficiently retrieve, use, and recycle phosphorus. Efficient phosphate (Pi) use by plants would increase crop productivity under Pi-limiting conditions and reduce our reliance on Pi applied as fertilizer. An ecotype of Eutrema salsugineum originating from the Yukon, Canada, shows no evidence of decreased relative growth rate or biomass under low Pi conditions and, as such, offers a promising model for identifying mechanisms to improve Pi use by crops. We evaluated traits associated with efficient Pi use by Eutrema (Yukon ecotype) seedlings and 4-week-old plants, including acquisition, remobilization, and the operation of metabolic bypasses. Relative to Arabidopsis, Eutrema was slower to remobilize phosphorus (P) from senescing leaves, primary and lateral roots showed a lower capacity for rhizosphere acidification, and root acid phosphatase activity was more broadly distributed and not Pi responsive. Both species produced long root hairs on low Pi media, whereas Arabidopsis root hairs were well endowed with phosphatase activity. This capacity was largely absent in Eutrema. In contrast to Arabidopsis, maximal in vitro rates of pyrophosphate-dependent phosphofructokinase and phosphoenolpyruvate carboxylase activities were not responsive to low Pi conditions suggesting that Eutrema has a constitutive and likely preferential capacity to use glycolytic bypass enzymes. Rhizosphere acidification, exudation of acid phosphatases, and rapid remobilization of leaf P are unlikely strategies used by Eutrema for coping with low Pi. Rather, equipping an entire root system for Pi acquisition and utilizing a metabolic strategy suited to deficient Pi conditions offer better explanations for how Eutrema has adapted to thrive on alkaline, highly saline soil that is naturally low in available Pi.