In the project, we will investigate the causes and consequences of regular and synchronized phenological transitions in tropical tree species. Investigating tropical tree phenology requires an integrative approach that takes into account the monitoring of tree phenology, molecular methods to study gene expression, and ecological approaches to study plant-animal interactions.

The study will be carried out in the montane humid forests and the seasonally dry tropical forest of Southern Ecuador, at the research stations Estacíon Científica San Francísco and Estacíon Científica Laipuna. Here, available data from previous and ongoing projects (most importantly from the research unit RESPECT) and continuous measurements of important parameters such as climate and carbon flux provide an ideal basis for realizing a study on tree phenology. During this project, we will simultaneously monitor phenological transitions, changes of gene expression, stem diameter variation, optical properties of canopies in four tree species and link this to carbon fluxes and climatic parameters. Thereby, this project will provide insights on how phenological transitions are triggered, which gene regulatory networks are involved in phenological transitions, and how these influence plant growth and carbon sequestration. Further, we will study the interdependencies of trees and their mutualistic and antagonistic partners in the light of phenological transitions. First, we will investigate pollinator assemblages, pollen-mediated gene flow, seed set, and germination rates. Second, we will investigate associated herbivore assemblages and rates of herbivory over time. Overall, this project will make important contributions to future predictions of the impact of climate change on montane rainforests.

The project is funded as an Emmy Noether research group by the DFG (HE 7345/8-1).

Climate change and global species loss are the major environmental threats to human well-being in the coming decades. However, despite more than 200 years of organized forestry and research in temperate forests, some fundamental knowledge is still missing about (i) the phenotypic plasticity of forest trees, (ii) about the interplay of trees with their microbiome, and (iii) about how these interactions may facilitate acclimation (regulatory changes) and adaptation based on genetic changes of trees and/or their holobiont partners. In this light, we have assembled a group of experts in (population) genetics, epigenetics, transcriptomics, metabolomics as well as in tree physiology and morphology working on a wide range of organisms from bacteria to trees to investigate a tree holobiont. We focus on Quercus robur L., a foundation species of European forests with a long lifespan and broad geographical distribution and an exceptionally high diversity of biotrophic interactions. A central benefit of working with Q. robur is the availability of the DF159 clone that is readily in-vitro propagated in large numbers. This resource allows us to exclude genetic variability of the tree host in order to disentangle the role of the holobiont partners in the acclimation and adaptation processes of the oak holobiont. In PHASE I of the RU, the subprojects SP1 – SP7 will mainly work on three experimental platforms with the clone DF159 to

(i) perform controlled experiments in two Ecotrons that expose the holobiont to two moderate droughts (previous year and current year for longer-term stress memory, spring and summer for shorter term stress memory) and above- and below-ground herbivory, respectively;

(ii) expose oak clonal saplings to the microclimatic variability of the canopy of mature trees; and

(iii) assess clonal oak saplings released across Germany and Europe for analyzing A&A mechanisms under a wide range of environmental conditions.

The research unit is funded by the DFG, and coordinated by Prof. Dr. Lars Opgenoorth (University Marburg).

For more details on the project and the subprojects, please have a look at our website.

Trees are emerging as powerful ‘model systems’ to investigate epimutational processes in plants. Given their exceptional longevity, trees act as natural (epi)mutation accumulation systems and permit unprecedented insights into the dynamics, mitotic stability, and functional impact of spontaneous epimutations over time-frames that have been inaccessible to previous prospective studies. Focusing on European beech (Fagus sylvatica) as a model, we will combine unique experimental tree resources, proximate-sensing technology, multi-omic assays, and novel analytical tools to quantify how somatic epimutations alongside micro-environmental factors shape epigenetic and functional diversity within the 3D-topology of a tree, and how this intra-tree variation affects seeds and seedling performance in the next generation.

The BMBF funded project is coordinated by Frank Johannes (TUM), and in collaboration with Lars Opgenoorth (Universität Marburg) and Hans Pretzsch (TUM).

In this project, we aim to investigate the genomic diversity dynamics of beech (Fagus sylvatica) in order to estimate the effect of natural selection in populations among life stages (seedlings, saplings, and adult trees) across a large representative sample using all beech-containing Experimental Forest Plots

The project is funded in the framework of the SPP Biodiversity Exploratories (HE7345/12-1) and carried out in collaboration with Marieke Lenga, Dr. Mona Schreiber, Dr. Christian Lampei and Prof. Dr. Lars Opgenoorth (all Philipps University Marburg).

We will investigate a chronosequence (forest sites recovering for different time spans from a former use as pasture or plantation) to assess and compare the reassembly of interaction networks and trajectories of ecosystem processes. We will quantify the effects of functional traits that are predicted to be important for network reassembly and resilience to perturbations: response traits to environmental conditions, and interaction traits as determinants of network links.

Overall, our research unit will unravel how, to what extent, and how fast a forest ecosystem can re-establish after deforestation, including the diverse species communities, complex interaction networks, and relevant processes that characterize such forest ecosystems.

The research site is located in the Chocó lowland forest of North-West Ecuador in collaboration with Fundación Jocotoco, a private Ecuadorian conservation foundation. Sites include the Canandé Reserve and Tesoro Escondido Reserve.

Together with Nina Farwig (Marburg) and Sybille Unsicker (Jena), I will be responsible for subproject 5,  studying seedling recruitment along the chronosequence. Specifically, we focus on the dynamics of tree seedling-herbivore interactions during forest recovery.

The research unit is coordinated by Nico Blüthgen (Darmstadt) & funded by the DFG (HE 7345/11-1).

More information can be found on our project website and on Twitter.

In this collaborative project, we aim to investigate the local adaptation of Nothofagus pumilio along extreme latitudinal, elevational, and precipitation gradients. In the next three years, we will gather genetic and dendrophenotypic data along the latitudinal gradient of the Andes, and investigate gene flow in two intensive study sites. For the exome capture design, we will use a transcriptome we assembled based on RNAseq data from a preliminary study with seedlings grown under different temperatures and day length conditions. Here, we seek to determine whether genes involved in the regulation of circadian clock are differentially expressed in N. pumilio seedlings grown under different temperature regimes.

The collaboration with the team from INTA Bariloche was funded by the DAAD and Trees4future and is currently funded by the DFG (HE 7345/6-1). Check out the project website.

Publications

Sekely J, Marchelli P, Arana V, Dauphin B, Mattera MG, Pastorino M, Scotti I, Soliani C, Heer K, Opgenoorth L (2024) Genomic Responses to Climate: Understanding local adaptation in the Andean tree species Nothofagus pumilio and implications for a changing world. Accepted in Plants People Planet.

Estravis-Barcala M, Heer K, Marchelli P, Ziegenhagen B, Arana MV, Bellora N. (2021) Deciphering the transcriptomic regulation of heat stress responses in Nothofagus pumilio. PLoS ONE 16(3): e0246615. https://doi.org/10.1371/journal.pone.0246615

Estravis-Barcala M, Mattera MG, Soliani S, Bellora N, Opgenoorth L, Heer K, Arana MV (2020) Molecular bases of responses to abiotic stress in trees. Journal of Experimental Botany, 71(13), 3765–3779. https://doi.org/10.1093/jxb/erz532

In this European Training Network (ETN), we studied the naturally occurring epigenetic variation in natural populations of Fragaria vesca, Thlaspi arvense, and Populus nigra.

PhD student Bárbara Díez Rodríguez established a common garden with ~ 450 poplar cuttings in the Botanical Garden in Marburg where we have phenotyped and epi-genotyped the trees in 2018 – 2020.

The ETN was funded by Marie-Skłodowska-Curie Actions and coordinated by Koen Verhoeven (NIOO, Netherlands). Detailed info on the project can be found on the project website and updates on twitter @EpiDiverse and ResearchGate.

Publications

Pena-Ponton C, Diez-Rodriguez B, Perez-Bello P, Becker B, McIntyre LM, van der Putten WH, De Paoli E, Heer K, Opgenoorth L, Verhoeven KJF (2024) High-resolution methylome analysis uncovers stress-responsive genomic hotspots and drought-sensitive TE superfamilies in the clonal Lombardy poplar. Accepted Experimental Journal of Botany

Can SN, Nunn A, Galanti D, Langenberger D, Becker C, Volmer K, Heer K, Opgenoorth L, Fernandez-Pozo N, Rensing S (2021) The EpiDiverse plant Epigenome-Wide Association Studies (EWAS) pipeline. Epigenomes 5(2), 2. https://doi.org/10.3390/epigenomes5020012

This study focused on a neotropical liana species, Marcgravia longifolia, that produces flowers and fruits across all strata in the forest, and interacts with a large number of different nectarivores and frugivores. We studied these plant-animal interactions in detail, with a specific focus on the vertical stratification of these interactions and the consequences on dispersal, and ultimately, gene flow.

Dr. Sarina Thiel has collected data on visitation rates, species assemblages, and nectar and fruit quality and quantity across the vertical gradient.

This project was carried out in collaboration with Eckhard Heymann (DPZ) and Marco Tschapka (University of Ulm), and funded by the German Research Council (DFG HE7345/5-1).

Publications

Thiel S, Gottstein M, Heymann EW, Kroszewski J, Lieker N, Shahuano Tello N, Tschapka M, Junker RR, Heer K (2024) Vertically stratified interactions of nectarivores and nectar-inhabiting bacteria in a liana flowering across forest strata. Accepted in American Journal of Botany.

Thiel S, Tschapka M, Heymann EW*, Heer K* (2021) Vertical stratification of seed-dispersing vertebrate communities and their interactions with plants in tropical forests. Biological Reviews. https://doi.org/10.1111/brv.12664

Thiel S, Willems F, Farwig N, Schabo D, Schleuning M, Shahuano Tello N, Töpfer T, Tschapka M, Heymann EW, Heer K (2023). Vertically stratified frugivore community composition and interaction frequency in a liana fruiting across forest strata. Biotropica. https://doi.org/10.1111/btp.13216

Heymann EW, Thiel S, Paciência FMD, Rimachi Taricuarima MN, Zárate Gómez R, Shahuano Tello N, Heer K, Sennhenn-Reulen H, Mundry R. Non-random host tree infestation by the Neotropical liana Marcgravia longifolia. PeerJ 10:e14535

The overall goal of GenTree is to provide the European forestry sector with better knowledge, methods, and tools to improve the conservation and use of adapted and genetically diverse FGR in European forests in the context of global environmental change and evolving societal demands for a diversified range of forest products.

In Marburg, we were involved in sampling of F. sylvatica, A. alba, P. abies and P. nigra, and in the development of the phenotyping protocols. Further, we participate in a germination trial that tests the quantitative genetics of early fitness traits in Pinus sylvestris and Betula pendula. At a later stage, we will analyze exome capture data of F. sylvatica and Q. robur. In collaboration with researchers from the WSL, we also work on the integration of phenotypes derived from dendrocores in phenotype-genotype association studies. GenTree is funded under the EU H2020 program. For more information on the project, please have a look at the website and on twitter @GenTree.

Publications

Ramirez-Valiente J, Solé-Medina A, Pyhäjärvi T, Savolainen O, Heer K, Opgenoorth L, Danusevicius D, Robledo-Arnuncio JJ (2022) Adaptive responses to temperature and precipitation variation at the early-life stages of Pinus sylvestris. New Phytologist 232 (4), 1632-1647. https://doi.org/10.1111/nph.17678

Opgenoorth L, Dauphin B, Benavides R, Heer K, Alizoti P, Martínez-Sancho E, [108 authors in alphabetical order], Fady B, Myking T, Valladares F, Aravanopoulos F, Cavers S. (2021) The GenTree-Platform: linking phenotypes, tree-level environmental data, and genotypes in twelve major European forest tree species. GigaScience 10(3). giab010. https://doi.org/10.1093/gigascience/giab010

Benavides R, Carvalho B, Bastias CC, López-Quiroga D, Mas A, Cavers S [93 authors in alphabethical order, including Heer K, Kappner JP, Lambertz J, Meischner H], Fady B, Valladares F (2021) The GenTree Leaf Collection: inter- and intraspecific leaf variation in seven forest tree species in Europe. Global Ecology and Biogeography 30(3) 590-597. https://doi.org/10.1111/geb.13239

Ramirez-Valiente J, Solé-Medina A, Pyhäjärvi T, Savolainen O, Cervantes S, Kesalahti R, Kujala S, Kumpula T, Heer K, Opgenoorth L, Siebertz J, Danusevicius D, Notivol E, Benavides R, Robledo-Arnuncio JJ (2021) Adaptive responses to climate variation at the early stages in Pinus sylvestris. New Phytologist 229(5), 3009-3025.  https://doi.org/10.1111/nph.17029

Solé-Medina A, Heer K, Opgenoorth L, Kaldewey P, Danusevicius D, Notivol E, Robledo-Arnuncio JJ, Ramírez-Valiente JA (2020). Genetic variation in early fitness traits across European populations of silver birch (Betula pendula). AOB Plants Journal 12(3), plaa019. https://doi.org/10.1093/aobpla/plaa019

Martínez-Sancho E, Slámová L, Morganti S, Grefen C, Carvalho B, Dauphin B, Rellstab C, Gugerli F, Opgenoorth L, Heer K, Knutzen F, von Arx G, Valladares F, Cavers C, Bruno Fady [54 authors in alphabethical order including Kappner JP, Lambertz J, Meischner H, Richter S] Fonti P (2020) The GenTree Dendroecological Collection: tree-ring and wood density data from seven tree species across Europe. Sci Data, 7(1), 1-7. doi:10.1038/s41597-019-0340-y

In this project, I was employed as a Postdoctoral researcher and we investigated the response of tree species to changing climatic conditions with a special focus on local adaptation. We currently analyze data to identify adequate candidate genes that vary along environmental gradients and test whether younger cohorts differ genetically from the cohort of their parental trees at these candidate loci with the goal of determining whether recent climatic changes already provoked shifts in allele frequency at adaptive genes. Further, we studied the genetic basis of dendrophenotypes that provide information on the response of individual trees towards environmental conditions (e.g. the reaction of silver fir towards SO₂ pollution in the 70s and 80s, see publications). Further, we focus on gene flow and reproductive success in the investigated populations. We closely collaborate with Martin Lascoux and Martin Källman (University of Uppsala), Bruno Fady (INRA Avignon), and Giovanni Vendramin and Andrea Piotti (Italian National Research Council). The project was funded by ERA-NET BiodivERsA and the BMBF.

Publications

Major E, Höhn M, Avanzi C, Fady B, Heer K, Opgenoorth L, Piotti A, Popescu  F, Postolache D, Vendramin GG, Csilléry K (2021) Spatial genetic structure at local and global scales across the species range in silver fir (Abies alba Mill.). Molecular Ecology. https://doi.org/10.1111/mec.16107

Avanzi C, Heer K, Büntgen U, Labriola M, Leonardi S, Opgenoorth L, Piermattei A, Urbinati C, Vendramin GG, Piotti A (2020). Individual reproductive success in Norway spruce natural populations depends on growth rate, age and sensitivity to temperature. Heredity, 124(4), 685-698. https://doi.org/10.1038/s41437-020-0305-0

Avanzi C, Piermattei A, Piotti A, Buntgen U, Heer K, Opgenoorth L, Spanu I, Urbinati C, Vendramin GG, Leonardi S (2019) Disentangling the effects of spatial proximity and genetic similarity on in situ growth performances of Picea abies. Science of the Total Environment, 650(1), 493-504. https://doi.org/10.1016/j.scitotenv.2018.08.348

Heer K*, Behringer D*, Piermattei A, Bässler C, Brandl R, Fady B, Jehl, H, Liepelt S, Lorch S, Piotti A, Vendramin GG, Weller M, Ziegenhagen B, Büntgen U, Opgenoorth L (2018) Linking dendroecology and association genetics in natural populations: Stress responses archived in tree rings associate with SNP genotypes in Abies alba (Mill.) Molecular Ecology, 27(6), 1428-1438. https://doi.org/10.1111/mec.14538

Heer K*, Ullrich KK*, Liepelt S, Rensing SA, Zhou J, Ziegenhagen B, Opgenoorth L (2016) Detection of SNPs based on transcriptome sequencing in Norway spruce (Picea abies (L.) Karst). Conservation Genetics Resources, 8(2), 105-107. https://doi.org/10.1007/s12686-016-0520-4