Research
We aim to understand molecular pathways of developmental adaptability to a changing climate,
using herbaria as windows into the past.
Plants are masters of developmental flexibility, from within-generation plasticity to short-term environmental variation, to trans-generational heritable adaptation to anthropogenic climate change. Over 250 years of historical records document this flexibility, and show trends such as advanced flowering (>3 days per 1°C warming) or reduced stomatal density (by 40%, following 200 years of increasing [CO2]).
Our lab studies this developmental flexibility over multiple timescales, to dissect the mechanisms of plant adaptation to climate change. We track historical change with herbarium phenotyping, ancient DNA sequencing and population genetics, and study its effects with modern molecular biology tools.
The lab combines molecular methods and large-scale herbarium genomics to open a functionally-informed window into the molecular mechanisms of historical adaptation processes, addressing these core questions:
How have 250 years of historical climate change affected development, and what is the contribution of plasticity vs evolution?
Could microRNA silencing promote rapid developmental responses to historical climate change?
Are climate change responses at the genetic, phenotypic, and possibly molecular mechanism level shared across many species?
While the model species Arabidopsis thaliana serves to dissect mechanisms, we also expand the lessons learned to non-model (native) species. In the long term, we aim to combine field and historical samples to scale up functional historical genomic approaches, and test experimental results under natural conditions. The generated knowledge of past species adaptation will be key to understanding the developmental mechanisms of plant responses to future climate change.
Fore more details, read on below.
How has development adapted in the last 250 years?
Mining herbaria to recreate & characterize historical adaptive variation
Herbaria, collections of pressed and dried plant specimens (b), allow us to interrogate plants for their responses to historical climate change. With them, we can follow changes in phenotypes, genotypes and even at the molecular pathway level as they happen "in real time" over the last ~250 years. One likely target of climate change adaptation are stomata, plants' pores that facilitate efficient photosynthesis. Their density and size reflect environmental conditions (a) – and they are highly preserved in herbaria (c). In addition, in our model plant Arabidopsis thaliana, their developmental and functional pathway is well understood and easy to manipulate with molecular tools.
We follow stomatal change in our collection of historical European A. thaliana specimens (d), looking at genetic change with whole-genome sequencing data of the DNA extracted from >250 herbarium specimens (so-called ancient DNA), and phenotypic change through scanning electron microscopy images of >600 herbarium leaf surfaces (c).
As this catalog grows with more whole-genome aDNA sequencing and historical phenotypes, we will use it to mine physiological pathways for genetic variation and molecular mechanisms of plant climate change adaptation.
Further reading:
Century-long timelines of herbarium genomes predict plant stomatal response to climate change (Lang et al. 2022, bioRxiv preprint)
Using herbaria to study global environmental change (Lang et al. 2018, New Phytologist)
Dissecting the contribution of plasticity and evolutionary change
Ultimately, to understand how plant development adapts to change, and why a selected genetic variant is beneficial, we need to functionally characterize the evolutionarily selected historical genetic variation. We will use CRISPR gene editing to revive phenotype- and climate-associated historical genetic variants, and characterize their effects on stomata in climate- and CO2-manipulating growth experiments.
Of course, plants can also respond to environmental variation independent of genetic change, through plasticity – the range of phenotypes attainable by a single genotype across different environments. Observed historical phenotype change may result from a combination of both such plasticity, and genetic variation. To disentangle the two, we are mapping the ranges and limits of stomatal size and density plasticity across temperature and CO2 gradients. In the long term, defining the contributions of both will be key to resolve to what extent adaptation relies on existing versus new genetic variation, and how engineered variation might be used to promote future adaptation.
Could MicroRNA silencing promote developmental plasticity to climate change?
Changing only single phenotypes at a time will likely not be sufficient for adaptation to climate change – we for example already know that both flowering time and stomatal density have shifted in recent decades. One mechanism that could generate a broader response across development and phenotypes is microRNA silencing. By sequence complementarity, microRNAs modulate targeted mRNAs' expression (a powerful mechanism also used to engineer gene suppression): For instance, lack of miRNA156 causes early flowering, while its excess suppresses it. Variation in microRNA (precursor) sequences or microRNA biogenesis factors tunes this balance through modulating microRNA production, accumulation, or activity.
We investigate if microRNAs could be plasticity modulators for rapid historical adaptation from two angles, studying (historical) genetic variation with climate-sensitive effects both in microRNAs themselves, and in core components of the microRNA biogenesis machinery. Where variation of existing miRNAs and factors does not suffice for adaptation and survival, Miniature Inverted-Repeat TEs (MITEs) are another exciting avenue for future work. As an evolutionary origin of new miRNAs, MITEs fine-tune neighboring genes and move in the genome temperature-dependently.
Further reading:
Alternative usage of miRNA-biogenesis co-factors in plants at low temperatures (Re, Lang et al. 2019, Development)
Polymorphic Inverted Repeats near coding genes impact chromatin topology and phenotypic traits in Arabidopsis thaliana (Arce et al. 2022, Cell Reports)
Do species share climate change responses – and underlying molecular changes?
Climate change is, unfortunately, affecting far more species than just Arabidopsis thaliana. Thus, while this model plant is exceptionally useful to study climate change responses especially at a detailed molecular level, to understand general plant responses to the changing climate, we need to expand our scope. Prime responses have are being reported across many species, such as an acceleration of flowering with higher spring temperatures, or decreased stomatal density with increased [CO2].
What remains unclear is if these shared responses also imply shared pathways towards those responses. How many ways are there to adapt to climate change? We ask if there is a masterplan across species to accelerate flowering, with adapted molecular pathways, through shared genetic change, plasticity responses, and combinations of both.
Further reading:
