Meret Huber’s research while affiliated with Johannes Gutenberg University Mainz and other places

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Publications (52)


Copper-Induced Transgenerational Plasticity in Plant Defence Boosts Aphid Fitness
  • Article

January 2025

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19 Reads

Plant Cell and Environment

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Anne Schreyer

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Pauline Prüsener

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[...]

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Meret Huber

Transgenerational plasticity in plants is an increasingly recognized phenomenon, yet it is mostly unclear whether transgenerational plasticity is relevant to both the fitness of the plant and its interacting species. Using monoclonal strains of the giant duckweed ( Spirodela polyrhiza) and its native herbivore, the waterlily aphid ( Rhopalosiphum nymphaeae ), we assessed whether pre‐treating plants with copper excess, both indoors and outdoors, induces transgenerational plasticity in plant defences that alter plant and herbivore fitness. Outdoors, copper pre‐treatment tended to increase plant growth rates under recurring copper excess. Indoors, copper pre‐treatment either increased or decreased plant growth rates under recurring conditions, depending on the plant genotype. Copper pre‐treatment induced anthocyanins that protected plants against copper toxicity, and these elevated levels were transgenerationally retained. Copper pre‐treatment also transgenerationally increased the levels of 12‐oxo‐phytodienoic acid (OPDA), a jasmonate precursor. Nevertheless, aphids grew up to 50% better when the plants were pre‐treated with copper. The increased aphid growth was likely caused by transgenerationally elevated OPDA levels, as aphids grew better when jasmonates were externally applied to plants. Taken together, this study shows that transgenerational plasticity is relevant to both plant and herbivore fitness, which highlights the role of transgenerational plasticity in plant evolution and species interactions.


Herbivory can increase plant fitness via reduced interspecific competition—evidence from models and mesocosms
  • Article
  • Full-text available

January 2025

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40 Reads

Herbivores are generally considered to reduce plant fitness. However, as in natural communities they often feed on several competing plant species, herbivores can also increase plant fitness by reducing interspecific competition among plants. In this study, we developed a testable model to predict plant fitness in the presence of an interspecific competitor and a herbivore that feeds on both plant species. Our model allows prediction of the herbivore and competitor densities at which the focal species will benefit from herbivory. This can be estimated by quantifying the effects of the herbivore on the fitness of the focal plant and on its competitor, and by estimating the levels of intra- and interspecific competition in a pairwise fashion, respectively. We subsequently validated the model in indoor microcosms using three interacting species: an aquatic macrophyte (the giant duckweed Spirodela polyrhiza), its native competitors (green algae) and its native herbivore (the pond snail Lymnaea stagnalis). Additional outdoor mesocosm experiments supported our model under natural conditions. Together, this study provides a conceptual framework to understand how herbivores shape plant fitness in a community context.

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Assessing Rapid Adaptation Through Epigenetic Inheritance: A New Experimental Approach

October 2024

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15 Reads

Plant Cell and Environment

statement Epigenetic inheritance is hypothesized to lead to rapid adaptation, yet evidence is scarce, possibly because of the current experimental approaches. We propose a new approach to simultaneously assess whether species adapt through selection of epimutations or formation of stress‐induced epialleles.



Phylogeny, population structure and demographic model of 228 S. polyrhiza
a The population structure of 228 S. polyrhiza genotypes. b The principal component (PC) analysis of the SNPs from 228 S. polyrhiza genotypes. The three coordinates indicate the first three PCs. c The Maximum Likelihood phylogenetic tree of 228 S. polyrhiza genotypes. The gray branch represents the outgroup - C. esculenta. Dashed branches represent internal nodes with supporting values lower than 0.75 (the max is 1). d The demographic model of S. polyrhiza populations. “Tpopulation” indicates the estimated divergence time in generations.
Genomic diversity variation among four populations might result from the switching between sexual and asexual propagation in S. polyrhiza
a Scheme of asexual and sexual propagation cycles in S. polyrhiza. (A) Vegetative stage of S. polyrhiza; (B) Budding; (C) Offspring from clonal propagation; (D) S. polyrhiza flowering; (E) Putative schematic of ovule at endosperm cellularization stage; (F) Putative schematic of seeds. b Bar plots show the differences among the four populations in terms of “π”: genome-wide nucleotide diversity; “LD”: the physical extent (in kb) of pairwise SNPs at r² of 0.2 (Europe does not yet reach r² = 0.2 at 100 kb, Supplementary Fig. 5); “πN/πS”: the efficacy of linked selection; “r”: genome-wide recombination rate; “H”: the median of per population genome-wide heterozygosity rate. c Two panels of pie charts indicate the allele frequencies of the functional allele of SOC1-like and AGL62-like genes among populations. Gray: functional allele frequency; Black: SVs allele frequency. d The distribution and migration world map of the four S. polyrhiza populations. “+” suggests the increased functional allele frequency, while  “-”  suggests the decreased functional allele frequency.
Weighted methylation level (wML) among four populations
a–c Box plots of genome-wide weighted methylation level (wML) in (a) CpG, (b) CHG, and (c) CHH context (N = 5). Uppercase letters indicate statistical differences among populations using Wilcoxon test (with bonferroni method for multiple tests corrections). d–f wML in the gene body and its flanking 2 kb regions in (d) CpG, (e) CHG, and (f) CHH context. g–i wML in TE and its flanking 2 kb regions in (g) CpG, (h) CHG, and (i) CHH context. The asterisks indicate significant differences between populations (P < 0.05; Wilcoxon test), while “n.s.” indicates no significant difference.
Branch-specific selection signature scans
a Population tree is used for the population-specific selection analyses. Input consists of an “outgroup” population (America) and two “ingroup” populations (India and SE-Asia, or Europe and SE-Asia). We present the number of genes in the ingroup populations belonging to the top 1% CLR scores reported by 3P-CLR. b Venn diagram showing the genes under selection that are common between the populations of SE-Asia, India, and Europe. c Branch-specific genome-wide scan of selection: each dot represents a chromosomal locus picked by 3P-CLR for which a CLR score is calculated; loci on the top 1% CLR are shown in red. The dashed purple lines between European and Indian panels indicate common peaks of selection detected at the same genomic regions in both populations. d Genomic diversity as depicted by π (solid black lines) and Tajima’s D (solid red lines) for two selected loci: the FLK (left) and the CYP78A9 (right). FLK shows a signature of selection (low π and negative Tajima’s D) in the European population, while CYP78A9 shows a signature of selection in both Europe and India. Dashed lines indicate genome-wide averages for π (black) and Tajima’s D (red).
Population genomics and epigenomics of Spirodela polyrhiza provide insights into the evolution of facultative asexuality

May 2024

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148 Reads

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5 Citations

Communications Biology

Many plants are facultatively asexual, balancing short-term benefits with long-term costs of asexuality. During range expansion, natural selection likely influences the genetic controls of asexuality in these organisms. However, evidence of natural selection driving asexuality is limited, and the evolutionary consequences of asexuality on the genomic and epigenomic diversity remain controversial. We analyzed population genomes and epigenomes of Spirodela polyrhiza, (L.) Schleid., a facultatively asexual plant that flowers rarely, revealing remarkably low genomic diversity and DNA methylation levels. Within species, demographic history and the frequency of asexual reproduction jointly determined intra-specific variations of genomic diversity and DNA methylation levels. Genome-wide scans revealed that genes associated with stress adaptations, flowering and embryogenesis were under positive selection. These data are consistent with the hypothesize that natural selection can shape the evolution of asexuality during habitat expansions, which alters genomic and epigenomic diversity levels.


Herbivory can increase plant fitness via reduced interspecific competition. Evidence from models and mesocosms

April 2024

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68 Reads

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2 Citations

Herbivores are generally considered to reduce plant fitness. However, as in natural communities herbivores often feed on several competing plant species, herbivores can also increase plant fitness by reducing interspecific competition among plants. In this study, we developed a testable model to predict plant fitness in the presence of an interspecific competitor and an herbivore that feeds on both plant species. Our model allows to predict at which herbivore and competitor densities the focal species will benefit from herbivory. This can be estimated by quantifying the effects of the herbivore on the fitness of the focal plant and on its competitor, and by estimating the levels of intra- and interspecific competition in a pair-wise fashion, respectively. We subsequently validated the model in indoor microcosms using three interacting species: an aquatic macrophyte (the giant duckweed Spirodela polyrhiza ), its native competitors (green algae), and its native herbivore (the pond snail Lymnaea stagnalis ). Additional outdoor mesocosm experiments supported our model under natural conditions. Together, this study provides a conceptual framework to understand how herbivores shape plant fitness in a community context.



Rapid evolution of Spirodela polyrhiza outdoors
Surface area (a) and dry weight (b) of 500 undamaged S. polyrhiza individuals of mixed-genotype populations exposed to herbivory across two growing seasons (2021 and 2022). Plant populations that experienced multigenerational herbivory outdoors showed a lower surface area and a higher dry weight per frond compared to the control group (Table S2). For each timepoint, dots represent mean values and bars show the standard deviation (n = 10). The gray area represents winter. Each plot reports the results from fitting a linear mixed-effects model using “treatment” (herbivory/control) as a fixed effect, and “time” and “pond” as random factors. Overview (c) of the experimental setup with the 10 ponds each hosting two cages (herbivory/control). Representative pictures of top pond view (d) and cross-sections of fronds (e) grown under control (d, e upper) and herbivory (d, e lower) conditions. Under herbivory fronds grew smaller in diameter but thicker. In panel (d) the styrofoam square measures 6 x 6 cm, and the line drawn in the middle measures 5 cm.
Spirodela polyrhiza populations evolved more resistance to snail herbivory
Consumed number of fronds (a), biomass (b), and surface area (c) of Spirodela polyrhiza populations that evolved without (green) and with (red) herbivory outdoors. Values for plots (b, c) are calculated by permutation (n = 999) with a set of reference fronds collected before the bioassay. For each group, dots represent mean values and bars show the standard deviation.
Snail herbivory altered genotype frequencies in the populations
Relative frequency of Spirodela polyrhiza genotypes Sp21 (a), Sp56 (b), Sp58 (c), and Sp65 (d) at the beginning of the experiment (n = 3) and after experimental evolution (weeks 8 and 12) under multigenerational herbivory or in control conditions (n = 10). For each group, dots represent mean values and bars refer to the standard deviation.
Evolution of induced responses contributed to increased resistance to herbivory
The plot shows the number of consumed fronds after 24h of herbivory in synthetic populations. The genotype frequencies represent observed frequencies outdoors in the control (Sp21 36%; Sp56 10.7%; Sp58 32.9%, Sp65 20.4%) or herbivory (Sp21 27.8%; Sp56 11.7%; Sp58 30.1%, Sp65 30.4%) cages. Genotypes were either grown under herbivory (induced, red) or control (non-induced, green) conditions. For each group, dots represent mean values and bars show the standard deviation.
Genotype-specific effects of herbivory-induced changes in plant microbiota and resistance
a Number of consumed fronds by snails for each S. polyrhiza genotype growing in microbial communities of control (green) and herbivory-induced (red) conditions, respectively. For each group, dots represent mean values and bars show the standard deviation (n = 10). b, c Canonical analysis of principal coordinates (CAP) analysis and PERMANOVA of bacterial communities (Unifrac distance matrix) associated with genotype Sp21 (b) and genotype Sp65 (c).
Induced responses contribute to rapid adaptation of Spirodela polyrhiza to herbivory by Lymnaea stagnalis

January 2024

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150 Reads

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4 Citations

Communications Biology

Herbivory-induced responses in plants are typical examples of phenotypic plasticity, and their evolution is thought to be driven by herbivory. However, direct evidence of the role of induced responses in plant adaptive evolution to herbivores is scarce. Here, we experimentally evolve populations of an aquatic plant (Spirodela polyrhiza, giant duckweed) and its native herbivore (Lymnaea stagnalis, freshwater snail), testing whether herbivory drives rapid adaptive evolution in plant populations using a combination of bioassays, pool-sequencing, metabolite analyses, and amplicon metagenomics. We show that snail herbivory drove rapid phenotypic changes, increased herbivory resistance, and altered genotype frequencies in the plant populations. Additional bioassays suggest that evolutionary changes of induced responses contributed to the rapid increase of plant resistance to herbivory. This study provides direct evidence that herbivory-induced responses in plants can be subjected to selection and have an adaptive role by increasing resistance to herbivores.


Assessing rapid adaptation through epigenetic inheritance: a new experimental approach

October 2023

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10 Reads

1. Epigenetic inheritance is hypothesized to mediate rapid adaptation to stresses via two fundamentally different routes: first, through spontaneous epimutations that arise in a largely stochastic manner in the presence or absence of stress; if these spontaneous epimutations are heritable and beneficial, they may be selected upon ('stochastic route'); and second, through environment-induced epialleles that arise uniformly among individuals; if heritable, these epialleles may lead to stress adaptation even in the absence of selection ('deterministic route'). Testing and teasing apart these two routes is challenging, largely because a suitable experimental approach is lacking. 2. Here, we propose an experimental approach that allows to simultaneously assess the contribution of the stochastic and deterministic route. The essence of the approach is to manipulate the efficacy of selection through the population size and thereby to test whether selection is required for adaptation (stochastic route). To this end, genetically uniform populations are grown under different environments across multiple generations ('pre-treatment') at two different population sizes: in large populations, in which selection is effective; and in small populations, in which drift overcomes the effect of selection. If the deterministic route contributes to adaptation, variation in fitness, phenotypes or epigenetic marks will arise between the small populations of the different pre-treatments. If the stochastic route contributes to adaptation, variation will arise between the small and large population within each pre-treatment. As a proof-of-principle, we tested whether small and large monoclonal populations of the aquatic duckweed Spirodela polyrhiza may adapt to copper excess outdoors. 3. After five to seven generations of pre-treatment and a subsequent multi-generational growth under control conditions, large populations outperformed small populations under copper excess. Furthermore, small populations pre-treated with copper excess tended to have higher fitness under copper excess than small populations pre-treated under control conditions. These data suggest that both the stochastic and deterministic route may alter plant fitness under recurring stress. 4. The proposed approach will allow to experimentally evaluate whether species may adapt to stresses through either stochastic and deterministic epigenetic changes, which is fundamental to understand whether and how epigenetic inheritance may lead to rapid stress adaptation.


Fig. 1: Phylogeny, population structure and demographic model of 228 S. polyrhiza.
Fig. 2: Genomic diversity variation among four populations might result from the
Fig. 3: Weighted methylation level (wML) among four populations.
Fig. 4: Branch-specific selection signature scans.
Population genomics and epigenomics provide insights into the evolution of facultative asexuality in plants

July 2023

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264 Reads

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2 Citations

Many organisms, particularly plants, are facultatively asexual. Because asexual reproduction is beneficial for the short term but costly for the long term, during the range expansion, natural selection should act on the genetic controls of asexuality in these facultatively asexual organisms. However, the genomic evidence of natural selection driving asexuality remains scarce, and the evolutionary consequences of facultatively asexuality on the genomic and epigenomic diversity remain controversial. Here, by analyzing population genomes and epigenomes of Spirodela polyrhiza (L.) Schleid., a facultatively asexual plant that flowers rarely, we show that this plant has the lowest genomic diversity and DNA methylation levels among all studied multicellular eukaryotes. Within species, demographic history and the frequency of asexual reproduction jointly determined intra-specific variations of genomic diversity and DNA methylation levels. Genome-wide scans revealed that multiple genes involved in flowering and embryogenesis were under positive selection, consistent with the hypothesis that natural selection drove the evolution of asexuality during the recent habitat expansions in this plant. Together, these results provide new insights into the evolution of plant reproductive systems and suggest that natural selection can drive the evolutionary changes of asexuality, which in turn alters the levels of genomic and epigenomic diversity.


Citations (23)


... Since our lab has identified four genetic populations for S. polyrhiza (Xu et al., 2019;Wang et al., 2024), we next investigated to what extent differences in metabolite concentrations and growth are explained by population structures. Assignment of genotypes to different genetic populations was done previously. ...

Reference:

Genome-wide association study of metabolic traits in the giant duckweed Spirodela polyrhiza
Population genomics and epigenomics of Spirodela polyrhiza provide insights into the evolution of facultative asexuality

Communications Biology

... Secondary metabolites were additionally measured by High-performance liquid chromatography-Photo diode array (HPLC-PDA). The following adjustments were made: change of the LC-MS/MS machine and respectively the instrument settings, slight modifications in the compound listmostly of secondary metabolitesand addition of the starch digestion step described in Ref. [54]. The steps required for phytohormone analysis were omitted. ...

Induced responses contribute to rapid adaptation of Spirodela polyrhiza to herbivory by Lymnaea stagnalis

Communications Biology

... This process not only generates the zygote and the triploid nucleus (resulting in reduced endosperm, in Orchidaceae) but also triggers the developmental start of the ovule [73][74][75]. This initiation is facilitated by complex nutrient and growth signals originating from both the egg cell and sperm cells [58,65,76]. Therefore, in most facultative apomicts, the formation of the embryo sac may still require the presence of pollen on the stigma to initiate the process of embryo sac development [77]. ...

Population genomics and epigenomics provide insights into the evolution of facultative asexuality in plants

... Natural rubber (NR) is a kind of natural polymer compound with cis-1,4-polyisoprene as the main component [1,2]. More than 2500 plants in the world can produce natural rubber, but only a few of these species can produce high-molecular-weight rubber [3,4]. ...

Natural rubber reduces herbivory and alters the microbiome below ground

... Additionally, a more natural way of inoculation is to grow sterile genotypes together with outdoor growing S. polyrhiza for several generations. Consistently, we also found genotype-dependent microbiota effects on plant resistance in a current study using such a natural inoculation approach in a long-term experimental evolution experiment [19]. ...

Induced responses contribute to rapid plant adaptation to herbivory

... The tiger swallowtail caterpillar Papilio glaucus can metabolize the toxic STL parthenolide produced by its host plants into a less reactive form or excrete intact parthenolide without absorption (Frankfater et al., 2005). In the larvae of the common cockchafer Melolontha melolontha, the taraxinic acid β-d-glucopyranosyl ester (TA-G) derived from dandelions is hydrolyzed by a gut digestive β-glucosidase (Huber et al., 2021). However, little is currently known about the tolerance or detoxification of the STL plant defense compounds in other herbivorous insects, particularly from genome-wide and molecular mechanism perspectives. ...

A beta-glucosidase of an insect herbivore determines both toxicity and deterrence of a dandelion defense metabolite

eLife

... Here we used diploids and neopolyploids of the model plant, the giant duckweed (Spirodela polyrhiza; Lemnaceae). These floating aquatic angiosperms mostly reproduce clonally and have a rapid generation time of 4-5 days (Acosta et al., 2021), making them a proven system for experimental population-level studies (Armitage & Jones, 2019;Hart et al., 2019;Hess et al., 2022;Hitsman & Simons, 2020;Huber et al., 2021;Subramanian & Turcotte, 2020). Here, as in these other studies, we quantify fitness as multigenerational asexual population growth rate. ...

Transgenerational non-genetic inheritance has fitness costs and benefits under recurring stress in the clonal duckweed Spirodela polyrhiza

... In contrast, insulin [6 µg/ml], used as a positive control, significantly stimulated glucose uptake in L6 cells, with a robust response of 129.7%. 30,31 . Alkaloids function as antihyperglycemic agents by inhibiting alpha-glucosidase, reducing glucose transport across the intestinal epithelium, and enhancing insulin secretion from pancreatic β cells. ...

Differential localization of flavonoid glucosides in an aquatic plant implicates different functions under abiotic stress

Plant Cell and Environment

... . Trade-offs help to explain how variation in herbivore pressure and resource availability may maintain multiple optimal defences across space and/ or time. However, recent work demonstrates that other factors such as temperature (Hahn et al. 2019;Bont et al. 2020;Rotter, Christie, and Holeski 2022) and drought (Carley et al. 2021) influence selection on plant defences and that defence traits such as trichomes (Galdon-Armero et al. 2018) and secondary metabolites (Hossain et al. 2013;Abuelsoud, Hirschmann, and Papenbrock 2016;Salehin et al. 2019) can mediate responses to abiotic stress. Thus, understanding the evolution of plant defence polymorphism may require explicit incorporation of abiotic contexts into more typical resource-economic approaches (Lin et al. 2023). ...

Heritable variation in root secondary metabolites is associated with recent climate

... A recent meta-analysis showed that, compared to small-seeded species, large-seeded species had less-negative PSFs or even positive ones (Xi et al., 2021). Moreover, on the Tibetan Plateau, 31% of the forb species have long-distance wind-dispersal mechanisms, allowing them to escape from negative conspecific PSFs, whereas only 10% of the graminoid species are wind-dispersed (Bont et al., 2020;Xu et al., 2017). Furthermore, as forbs usually contain more nutrients (e.g., nitrogen) (Thomas et al., 2019), a small forb seedling, produced by a small seed, may be more vulnerable to soil pathogens than a small graminoid seedling, leading to a negative PSF response. ...

Adapted dandelions trade dispersal for germination upon root herbivore attack