Vít Latzel

Epigenetic diversity increases the productivity and stability of plant populations

Biological diversity within species can be an important driver of population and ecosystem functioning. Until now, such within-species diversity effects have been attributed to underlying variation in DNA sequence. However, within-species differences, and thus potentially functional biodiversity, can also be created by epigenetic variation. Here, we show that epigenetic diversity increases the productivity and stability of plant populations. Epigenetically diverse populations of Arabidopsis thaliana produce up to 40% more biomass than epigenetically uniform populations. The positive epigenetic diversity effects are strongest when populations are grown together with competitors and infected with pathogens, and they seem to be partly driven by complementarity among epigenotypes. Our study has two implications: first, we may need to re-evaluate previous within-species diversity studies where some effects could reflect epigenetic diversity; second, we need to incorporate epigenetics into basic ecological research, by quantifying natural epigenetic diversity and testing for its ecological consequences across many different species.

Epigenetic variation in plant responses to defence hormones

BACKGROUND AND AIMS There is currently much speculation about the role of epigenetic variation as a determinant of heritable variation in ecologically important plant traits. However, we still know very little about the phenotypic consequences of epigenetic variation, in particular with regard to more complex traits related to biotic interactions. METHODS Here, a test was carried out to determine whether variation in DNA methylation alone can cause heritable variation in plant growth responses to jasmonic acid and salicylic acid, two key hormones involved in induction of plant defences against herbivores and pathogens. In order to be able to ascribe phenotypic differences to epigenetic variation, the hormone responses were studied of epigenetic recombinant inbred lines (epiRILs) of Arabidopsis thaliana - lines that are highly variable at the level of DNA methylation but nearly identical at the level of DNA sequence. KEY RESULTS Significant heritable variation was found among epiRILs both in the means of phenotypic traits, including growth rate, and in the degree to which these responded to treatment with jasmonic acid and salicylic acid. Moreover, there was a positive epigenetic correlation between the responses of different epiRILs to the two hormones, suggesting that plant responses to herbivore and pathogen attack may have a similar molecular epigenetic basis. CONCLUSIONS This study demonstrates that epigenetic variation alone can cause heritable variation in, and thus potentially microevolution of, plant responses to defence hormones. This suggests that part of the variation of plant defences observed in natural populations may be due to underlying epigenetic, rather than entirely genetic, variation.

The Association of Dispersal and Persistence Traits of Plants with Different Stages of Succession in Central European Man-Made Habitats

Traits related to seed dispersal, clonality and bud bank affect the success or failure of plant species. Using data from 13 successional seres in various human-made habitats the spectra of traits associated with dispersal and persistence were compared to determine the traits that can be used to predict the occurrence of particular plant species at each stage in a succession and how the importance of these traits changes over time. Differences in the traits of species associated with primary and secondary successions were also studied. Species with seeds that are dispersed by water (hydrochory) decreased in abundance during the course of succession. Species with a splitting main root, monocyclic and dicyclic shoots also decreased in abundance. Species capable of forming a potential below-ground bud bank, hypogeogenous rhizome and retaining a long-term connection with clonal offspring increased in abundance. The results indicate that seed dispersal is more important in determining the species composition in the early stages of succession whereas bud banks and clonal traits are more important in the later stages and for colonizing a locality. Primary and secondary seres did not remarkably differ in the trait spectra of the species present indicating that these trends occur in both types of succession.

Costs and benefits of induced resistance in a clonal plant network

Plant defense theory suggests that inducible resistance has evolved to reduce the costs of constitutive defense expression. To assess the functional and potentially adaptive value of induced resistance it is necessary to quantify the costs and benefits associated with this plastic response. The ecological and evolutionary viability of induced defenses ultimately depends on the long-term balance between advantageous and disadvantageous consequences of defense induction. Stoloniferous plants can use their inter-ramet connections to share resources and signals and to systemically activate defense expression after local herbivory. This network-specific early-warning system may confer clonal plants with potentially high benefits. However, systemic defense induction can also be costly if local herbivory is not followed by a subsequent attack on connected ramets. We found significant costs and benefits of systemic induced resistance by comparing growth and performance of induced and control plants of the stoloniferous herb Trifolium repens in the presence and absence of herbivores.

Ecological plant epigenetics: Evidence from model and non-model species, and the way forward

Growing evidence shows that epigenetic mechanisms contribute to complex traits, with implications across many fields of biology. In plant ecology, recent studies have attempted to merge ecological experiments with epigenetic analyses to elucidate the contribution of epigenetics to plant phenotypes, stress responses, adaptation to habitat, and range distributions. While there has been some progress in revealing the role of epigenetics in ecological processes, studies with non-model species have so far been limited to describing broad patterns based on anonymous markers of DNA methylation. In contrast, studies with model species have benefited from powerful genomic resources, which contribute to a more mechanistic understanding but have limited ecological realism. Understanding the significance of epigenetics for plant ecology requires increased transfer of knowledge and methods from model species research to genomes of evolutionarily divergent species, and examination of responses to complex natural environments at a more mechanistic level. This requires transforming genomics tools specifically for studying non-model species, which is challenging given the large and often polyploid genomes of plants. Collaboration among molecular geneticists, ecologists and bioinformaticians promises to enhance our understanding of the mutual links between genome function and ecological processes.

Transgenerational plasticity in clonal plants

Transgenerational plasticity has recently been recognized as a mechanism allowing phenotypic adjustments to local conditions to be passed onto sexually produced offspring. Although thus far it has been studied mainly in non-clonal plants, the present paper proposes that transgenerational plasticity is also applicable to asexually generated progeny, and that it can have multiple consequences for clonal plants. Indeed, in clonal plants, local phenotypic adjustment transferred to the next generation—whether produced sexually or asexually—can provide a mechanism that assists the population better exploit spatial heterogeneity. Moreover, this concept provides a framework allowing investigation of how long environmental heterogeneity will affect growth of asexually as well as sexually generated progeny.

Plant traits and regeneration of urban plant communities after disturbance: Does the bud bank play any role?

ABSTRACT Questions: What is the relative role of the bud bank, seed and various species traits in the regeneration of urban plant communities after severe disturbances? Do invasive and exotic species, highly abundant in disturbed communities, regenerate better than native species after disturbance? Methods: Hand tilling was applied to three urban plant communities with and without additional herbicide treatment to exclude regeneration from the bud bank. Plant traits were determined from the literature and databases. Species responses to the treatments were evaluated with RDA analyses in CANOCO. Linear models were applied to identify traits that could predict the responses of species to disturbance. Results: The bud bank played a key role in regeneration in the plots without herbicide. In the plots with herbicide treatment, the seed bank was important in re-establishing vegetation after disturbance. Exclusion of the bud bank by using herbicide allowed the establishment of small annuals, whereas biennials and perennials were successful in plots where the bud bank was not inhibited by herbicide. Exotic species with a long residence time in the local flora were successful in plots where regeneration from the bud bank was excluded, whereas species with short residence times or that were invasive were suppressed by both types of disturbance. Conclusion: In response to various types of disturbance, species with different regeneration strategies (either seeds or bud bank) were promoted. Exotic species were suppressed primarily by disturbance, which suggests that factors other than just regenerative capability contributed to the high abundance of exotics in urban communities. Nomenclature: Dostál (1989).

Annuals sprouting adventitiously from the hypocotyl: their compensatory growth and implications for weed management

Habitats, disturbed severely at least once a year, are often dominated by annual plants, which avoid disturbance by means of a short life span and massive production of seeds. Contrary to perennials, they lack pools of reserve meristems on and storage carbon in below-ground organs necessary for vegetative regeneration after disturbance. However, some annuals are able to initiate a bud bank on the hypocotyl after loss of their shoot.In three experiments, we investigated how the timing of disturbance or population origin affects adventitious bud formation on the hypocotyl for regeneration and compensatory growth in some annual weeds.The best regenerative abilities were observed in Kickxia spuria and K. elatine, with 87% and 80% of individuals regenerating, respectively, followed by Microrrhinum minus with almost 70%. Less than 30% of individuals regenerated in Euphorbia peplus and Anagallis arvensis. The time of injury did not affect the regeneration capacity of species for which the timing was examined, nor their consequent compensatory growth.The best compensation for biomass and fruit production was observed in M. minus, albeit two populations differed in this respect. The injured plants were shorter and produced more shoots than intact plants. Mechanical control of weeds capable of forming adventitious buds on hypocotyl by harrowing, brushing, or cutting may not be sufficient in organically farmed lands.

The role of transgenerational effects in adaptation of clonal offspring of white clover (Trifolium repens) to drought and herbivory

Environmentally induced transgenerational effects can increase success of offspring and thereby be adaptive if offspring experience conditions similar to the parental environment. The ecological and evolutionary significance of these effects in plants have been considered overwhelmingly in the context of sexual generations. We investigated whether drought stress and jasmonic acid, a key hormone involved in induction of plant defenses against herbivores, applied in the parental generation, trigger transgenerational effects in clonal offspring of Trifolium repens and whether these effects are adaptive. We found that drought stress experienced by parents significantly affected phenotypes of offspring ramets. Offspring ramets were bigger if they were produced in the parental water regime (control/drought). Repeated application of jasmonic acid to parents increased the subsequent growth of offspring ramets produced by stolons after they were disconnected from the parental clone. However, these offspring ramets experienced similar herbivory by the generalist Spodoptera littoralis caterpillar as did control offspring ramets, indicating that this jasmonic acid application in the parental generation did not result in a transgenerational effect comprising increased herbivory resistance. We conclude that, overall, environmental interaction in the parental generation can trigger transgenerational effects in clonal plants and some of these effects can be adaptive. Moreover, transgenerational effects in clonal plants that significantly influence their growth and behavior can ultimately affect the evolutionary trajectories of clonal populations.

Pitfalls in ecological research – transgenerational effects

The phenotype of an individual can be affected by the environment of its predecessors, a phenomenon commonly referred to as transgenerational effects. These effects, if not properly acknowledged and/or controlled, can impede proper interpretation of ecological studies. Using examples from more than 40 recently published studies, I discuss the most frequently used methodological approaches to deal with unwanted transgenerational effects in ecological research. In this literature, growing one generation in a common environment before the experiment or fitting seed and/or seedling size as a covariate were the most prevalent tools used to account for or even out transgenerational effects. Although these methods can efficiently control for transgenerational effects of limited generational persistence, usually just one generation of offspring, they cannot sufficiently control for effects across multiple generations. I propose that, whenever possible in ecological experiments, two generations of plants be grown in a common environment prior to the main experiment and that extreme caution should be exercised in interpreting results if the degree of transgenerational effects is not known. I also suggest that in addition to controlling for transgenerational effects in ecological research, we should actively investigate transgenerational effects as a source of plant variation.