The role of invertases in plant compensatory responses to simulated herbivory

Madhura H. Siddappaji, Daniel R. Scholes, Sindhu M. Krishnankutty, Bernarda Calla, Steven J. Clough, Raymond E. Zielinski, Ken N. Paige

The ability of a plant to overcome animal-induced damage is referred to as compensation or tolerance and ranges from undercompensation (decreased fitness when damaged) to overcompensation (increased fitness when damaged). Although it is clear that genetic variation for compensation exists among plants, little is known about the specific genetic underpinnings leading to enhanced fitness. Our previous study identified the enzyme GLUCOSE-6-PHOSPHATE DEHYDROGENASE 1 (G6PD1) as a key regulator contributing to the phenomenon of overcompensation via its role in the oxidative pentose phosphate pathway (OPPP). Apart from G6PD1 we also identified an invertase gene which was up-regulated following damage and that potentially integrates with the OPPP. The invertase family of enzymes hydrolyze sucrose to glucose and fructose, whereby the glucose produced is shunted into the OPPP and presumably supports plant regrowth, development, and ultimately compensation. In the current study, we measured the relative expression of 12 invertase genes over the course of plant development in the Arabidopsis thaliana genotypes Columbia-4 and Landsberg erecta, which typically overcompensate and undercompensate, respectively, when damaged. We also compared the compensatory performances of a set of invertase knockout mutants to the Columbia-4 wild type. We report that Columbia-4 significantly up-regulated 9 of 12 invertase genes when damaged relative to when undamaged, and ultimately overcompensated for fruit production. Landsberg erecta, in contrast, down-regulated two invertase genes following damage and suffered reduced fitness. Knockout mutants of two invertase genes both exhibited significant undercompensation for fruit production, exhibiting a complete reversal of the wild type Col-4's overcompensation. Collectively, these results confirm that invertases are essential for not only normal plant growth and development, but also plants' abilities to regrow and ultimately compensate for fitness following apical damage.