Molecular constraints on resistance-tolerance trade-offs.

Plants have numerous mechanisms to cope with the negative effects of herbivory, including plant resistance, structural and chemical traits that reduce damage, and plant tolerance, the ability to compensate for tissues lost. It has been argued that resistance and tolerance represent alternate strategies and thus there should be a trade-off between resistance and tolerance. However, resistance and tolerance are controlled via the same molecular pathway, the oxidative pentose phosphate pathway and the process of endoreduplication. Endoreduplication is the replication of the genome without mitosis, which leads to an increase in cellular chromosome number. Increasing chromosome number and therefore gene copy number provides a means of increasing gene expression that has been shown to enhance compensation following herbivory. By measuring glucosinolate levels and seed production following the removal of apical dominance in genotypes of Arabidopsis thaliana we show that there is a positive association between tolerance and induced chemical defense. Similarly, the direct association between tolerance and resistance is demonstrated by genetically manipulating the endoreduplication pathway. By overexpressing ILP1, a positive regulator of endoreduplication, and thus compensation, we experimentally increased glucosinolate production and tolerance in the Col-0 genotype. We suggest that many herbaceous plants that endoreduplicate (~90%) would show a positive relationship between compensation and chemical defense, given that the molecular pathways are shared in common. We discuss these findings in light of contrasting results on measures of tolerance and resistance, given that the true relationship can be masked by ignoring genetic variation in endoreduplication and the timing of chemical measurement.

Characterization of Arabidopsis thaliana regrowth patterns suggests a trade-off between undamaged fitness and damage tolerance.

Herbivory is a fundamental type of plant-animal interaction that presents substantial selection pressure on plants to replace lost tissues and to prevent subsequent losses in fitness. Apical herbivory, which entails removal or damage to the apical meristem, causes a change in plant architecture by disrupting the balance of hormones produced in part by the apical meristem. Therefore, for an annual semelparous plant, the ability to preserve reproductive success following damage (i.e., to tolerate damage) is largely dependent on the plant's pre-damage investment into fitness and its regrowth pattern following damage. Using multiple regression analyses, we assessed the relationship of developmental and architectural traits of experimentally damaged plants relative to undamaged plants of 33 Arabidopsis thaliana genotypes that display a wide range of undamaged fitness and damage tolerance. Our analyses revealed evidence for an evolutionary bet-hedging strategy within a subset of genotypes to presumably maximize fitness under natural herbivory-genotypes with the greatest seed production when undamaged exhibited a significant reduction in seed yield when damaged, while genotypes with low undamaged seed production were the only genotypes whose seed yield increased when damaged. Patterns of endopolyploidy paralleled those of seed production, such that the increase in whole-plant ploidy by genome re-replication during growth/regrowth contributes to undamaged fitness, damage tolerance, and their trade-off. Overall, this study provides the first large-scale characterization of A. thaliana regrowth patterns and suggests that investment into fitness and endopolyploidy when undamaged may come at a cost to tolerance ability once damaged.

The role of invertases in plant compensatory responses to simulated herbivory.

BACKGROUND: 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. RESULTS: 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. CONCLUSION: 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.

Plasticity in ploidy underlies plant fitness compensation to herbivore damage.

How plants mitigate damage by animal herbivores is a fundamental ecological and evolutionary question of plant-animal interactions. Some plants can increase their fitness when damaged in a phenomenon termed 'overcompensation'. Despite overcompensation being observed in a variety of plant species, its mechanistic basis remains elusive. Recent research has shown that the Arabidopsis thaliana genotype Columbia-4 employs endoreduplication, the replication of the genome without mitosis, following damage and that it overcompensates for seed yield. The related genotype Landsberg erecta, in contrast, does not increase its endoreduplication following damage and suffers reduced seed yield. While these results suggest that a plant's ability to plastically increase its ploidy during regrowth may promote its mitigation of damage, no studies have explicitly linked the endoreduplication genetic pathway to the regrowth and fitness of damaged plants. By comparing fitness and ploidy between undamaged and damaged plants of Columbia-4, Landsberg erecta and their offspring, we provide evidence that endoreduplication is directly involved in compensatory performance. We then overexpressed an endoreduplication regulator and compared this mutant's endoreduplication and compensation with its background genotype Columbia-0, an undercompensator. Enhancing Columbia-0's ability to endoreduplicate during regrowth led to the complete mitigation of the otherwise detrimental effects of damage on its fitness. These results suggest that the ability of these plants to increase their ploidy via endoreduplication directly impacts their abilities to compensate for damage, providing a novel mechanism by which some plants can mitigate or even benefit from apical damage with potential across the wide range of plant taxa that endoreduplicate.

Chromosomal plasticity: mitigating the impacts of herbivory.

Endoreduplication, the replication of the genome without mitosis, leads to endopolyploidy, an increase in cellular chromosome number. Although endoreduplication is widespread among angiosperms and other groups of eukaryotes, the degree to which this process is plastic under varying environmental conditions and its potential adaptive significance are not known. Here, using flow cytometry, we measured plasticity in chromosome number following the removal of apical dominance (simulating natural herbivory) in two ecotypes of Arabidopsis thaliana: Columbia and Landsberg erecta. We report that endopolyploidy of clipped Columbia plants was significantly different than unclipped controls following the removal of apical dominance and regrowth, and that cellular ploidy is positively associated with attributes of fitness (biomass, flower, fruit, and seed production). In contrast, clipped Landsberg erecta showed no significant differences in endopolyploidy and a decrease in seed production compared to unclipped controls; representing a significant genotype x environment interaction between ecotypes. Altering ploidy via endoreduplication adds a previously unknown way in which plants may be able to cope with environmental stress: enhancing regrowth rates and fitness following plant damage.

Plasticity in ploidy: a generalized response to stress.

Endoreduplication, the replication of the genome without mitosis, leads to an increase in the cellular ploidy of an organism over its lifetime, a condition termed 'endopolyploidy'. Endopolyploidy is thought to play significant roles in physiology and development through cellular, metabolic, and genetic effects. While the occurrence of endopolyploidy has been observed widely across taxa, studies have only recently begun to characterize and manipulate endopolyploidy with a focus on its ecological and evolutionary importance. No compilation of these examples implicating endoreduplication as a generalized response to stress has thus far been made, despite the growing evidence supporting this notion. We review here the recent literature of stress-induced endopolyploidy and suggest that plants employ endoreduplication as an adaptive, plastic response to mitigate the effects of stress.

Can endopolyploidy explain body size variation within and between castes in ants?

Endoreduplication is the process by which the nuclear genome is repeatedly replicated without mitotic cell division, resulting in nuclei that contain numerous additional genome copies. Endoreduplication occurs widely throughout Eucarya and is particularly common in angiosperms and insects. Although endoreduplication is an important process in the terminal differentiation of some specialized cell types, and often increases cell size and metabolism, the direct effects of increasing nuclear ploidy on cell function are not well resolved. Here, we examine if endoreduplication may play a role in body size and/or caste differentiation in ants. Nuclear ploidy was measured by flow cytometry of whole individuals (providing the basis for overall body size patterns) and individual body segments for multiple polymorphic ant species. We used cell cycle values, interpreted as the mean number of endocycles performed by each cell in the sample, as our measure of overall endoreduplication. Among females of four polymorphic ant species, endoreduplication was positively related with size within the worker caste, but was not related to caste generally in two species where we also examined queens. Additionally, abdomens had the greatest endoreduplication of all body parts regardless of caste or size. We also found that males, having derived from haploid unfertilized eggs, had the highest rates of endoreduplication and may compensate for their haploid origin by performing an additional endocycle relative to females. These results suggest that endoreduplication may play a role in body size variation in eusocial insects and the development of some segment-specific tissues.

Overcompensation in response to herbivory in Arabidopsis thaliana: the role of glucose-6-phosphate dehydrogenase and the oxidative pentose-phosphate pathway.

That some plants benefit from being eaten is counterintuitive, yet there is now considerable evidence demonstrating enhanced fitness following herbivory (i.e., plants can overcompensate). Although there is evidence that genetic variation for compensation exists, little is known about the genetic mechanisms leading to enhanced growth and reproduction following herbivory. We took advantage of the compensatory variation in recombinant inbred lines of Arabidopsis thaliana, combined with microarray and QTL analyses to assess the molecular basis of overcompensation. We found three QTL explaining 11.4, 10.1, and 26.7% of the variation in fitness compensation, respectively, and 109 differentially expressed genes between clipped and unclipped plants of the overcompensating ecotype Columbia. From the QTL/microarray screen we uncovered one gene that plays a significant role in overcompensation: glucose-6-phosphate-1-dehydrogenase (G6PDH1). Knockout studies of Transfer-DNA (T-DNA) insertion lines and complementation studies of G6PDH1 verify its role in compensation. G6PDH1 is a key enzyme in the oxidative pentose-phosphate pathway that plays a central role in plant metabolism. We propose that plants capable of overcompensating reprogram their transcriptional activity by up-regulating defensive genes and genes involved in energy metabolism and by increasing DNA content (via endoreduplication) with the increase in DNA content feeding back on pathways involved in defense and metabolism through increased gene expression.