Abstract
BackgroundThe 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.ResultsWe 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.ConclusionCollectively, 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0655-6) contains supplementary material, which is available to authorized users.
Highlights
The ability of a plant to overcome animal-induced damage is referred to as compensation or tolerance and ranges from undercompensation to overcompensation
Apical damage induces invertase gene expression in the overcompensating genotype Columbia-4, but not in the undercompensator Landsberg erecta Because previous quantitative trait loci (QTL) analyses revealed a potential contribution to overcompensation by at least one Arabidopsis invertase gene [23], we examined the expression patterns of all the members of this gene family in response to removal of the floral apex
Col-4, we found significant changes in invertase gene expression that were distinct from those observed in the undercompensating accession, Landsberg erecta (Ler)
Summary
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). Paige & Whitham [7] reported that when ungulate herbivores removed 95 % or more of the aboveground biomass of the monocarpic biennial scarlet gilia, Ipomopsis aggregata, the product of lifetime seed production, seed germination, and seedling survival averaged 3.0 times that of the uneaten controls This increase in relative fitness correlated strongly with changes in plant architecture—ungulate removal of scarlet gilia’s single inflorescence resulted in the production of multiple flowering stalks due to the release of apical dominance, leading to an overall increase in both above- and below-ground biomass [7, 9,10,11,12]. Studies comparing historically grazed and ungrazed populations of the plant Gentianella campestris indicate that repeatedly grazed populations can evolve overcompensation while ungrazed populations remain completely intolerant [16]
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