Picture of a man standing in front of a conifer tree, a road can be seen in the background on the left

Zan, Yanjun - Complex Trait Genetics and Plasticity for Climate-Resilient Plants

Research

A chinese man with blue jeans shirt is standing next to pine trees looking into the cameraPhoto: Lei Liang

How does natural genetic variation shape plant responses to a changing climate? Many traits central to plant performance — including stress tolerance, growth, flowering time, reproduction, and yield stability — are complex traits controlled by many genes whose effects often depend strongly on the environment.

Our research seeks to understand how genomes and environments interact to shape these traits, and how this knowledge can be used to predict plant performance, improve breeding, and support the conservation of adaptive diversity.

We study how plants respond to drought, heat, and other climate-related challenges by linking genomic variation to phenotypic plasticity across environments. By combining genomics, quantitative genetics, and computational modelling, we aim to uncover why different genotypes respond differently to the same stress, how adaptive responses evolve, and how environmentally contingent genetic effects can be predicted.

A long-term goal of the group is to turn large-scale biological data into predictive insight for plant breeding and biodiversity management. We use genomic, phenotypic, and environmental information to advance climate-resilient breeding and to help preserve the genetic diversity that underpins future adaptation in natural, agricultural, and forest systems.

Our research

Genetic and genomic basis of climate-responsive trait plasticity

A central focus of the group is to understand how genetic variation shapes phenotypic plasticity under environmental stress. We are particularly interested in complex traits whose expression changes across environments, such as flowering time, reproductive success, growth, and stress tolerance.

Using Arabidopsis thaliana as a model system, alongside crop and forest species where appropriate, we investigate how plants differ in their responses to drought, heat, and other climate-related stresses. This allows us to dissect genotype-by-environment interactions, identify the genetic architecture of plastic responses, and uncover the biological mechanisms that link genome variation to trait variation across environments.

Through this work, we aim to understand how adaptive responses are built, why genotypes differ in environmental sensitivity, and how complex traits evolve under heterogeneous and changing climates.

Genome diversity, genome structure, and adaptive variation

We develop genomic resources to better understand the diversity of plant genomes across populations, breeding materials, and evolutionary timescales. Using systems such as Arabidopsis thaliana and Nicotiana tabacum, we study genome diversity beyond single-reference genomes, with particular interest in structural variation, pan-genome diversity, and genome organization.

These approaches allow us to ask how genome structure differs across lineages, habitats, and breeding populations, and how such variation contributes to trait diversity, adaptation, and long-term resilience. By revealing previously hidden forms of genomic variation, we seek to better understand the raw material on which selection and adaptation act.

Predictive models for climate-resilient breeding and deployment

A major long-term goal of the group is to translate fundamental insights into predictive tools for agriculture, forestry, and biodiversity management. Once we understand how genomic variation shapes plant performance across environments, we can use that knowledge to improve prediction, selection, and deployment under climate uncertainty.

We develop models that integrate genomic, phenotypic, and environmental data to improve plant breeding in heterogeneous environments. This includes multi-environment genomic prediction, plasticity-informed breeding frameworks, and approaches for optimizing trial networks and phenotyping strategies.

More broadly, we are interested in how predictive models can guide both breeding and conservation: improving the efficiency of selection in crops and trees, while also helping identify and preserve adaptive genetic diversity in natural populations.

Vision

We believe that understanding plant adaptation requires linking genome variation, gene regulation, phenotypic plasticity, and performance across environments within a single framework. By combining genomic discovery, quantitative genetics, and predictive modelling, our research aims to advance both climate-resilient breeding and the conservation of adaptive diversity in a rapidly changing world.

Graphical representation split in three columns. The first one shows a herbaceous plant and how abiotic stresses and developmental mechanisms connect; the second one shows a herbaceous plant and two trees; the third shows how genotype, environment and phenotype are used together to generate models used to prepare prediction.We study how natural genetic variation interacts with changing environments to shape complex trait plasticity, and how this knowledge can be used for prediction, breeding, and deployment (illustration: Yanjun Zan).

Key publications:

  • Zan Y, Chen S, Ren M,Liu G, Liu Y, Han Y, Dong Y, Zhang Y, Si H, Liu Z (2025) The genome and GeneBank genomics of allotetraploid Nicotiana tabacum provide insights into genome evolution and complex trait regulation. Nature Genetics; 57, 4, 986-996
  • Kang M, Wu H, Liu H, Liu W, Zhu M, Han Y, Liu W, Chen C, Song Y, Tan L (2023) The pan-genome and local adaptation of Arabidopsis thaliana. Nature Communications;14,1,6259
  • Han Y, Liu L, Lei M, Liu W, Si H, Ji Y, Du Q, Zhu M, Zhang W, Dai Y (2025) Divergent Flowering Time Responses to Increasing Temperatures Are Associated With Transcriptome Plasticity and Epigenetic Modification Differences at FLC Promoter Region of Arabidopsis thaliana. Molecular Ecology; 34, 15, e17544
  • Zan Y, Carlborg Ö (2020) Dissecting the genetic regulation of yeast growth plasticity in response to environmental changes. Genes; 11,11,1279
  • Zan Y, Carlborg Ö (2019) A polygenic genetic architecture of flowering time in the worldwide Arabidopsis thaliana population. Molecular biology and evolution;36,1,141-154
  • Han Y, Du Q, Dai Y, Gu S, Lei M, Liu W, Zhang W, Zhu M, Feng L, Si H (2025) EasyOmics: A graphical interface for population-scale omics data association, integration, and visualization. Plant Communications; 6,5
David Martinelli

Frew, Adam - Mycorrhizal Ecology

Research

Adam Frew with a light-blue shirt and short trousers, is standing with one leg up in front of whitish bushes in a sunny environment. He has short hair and wears glasses.Photo: David Martinelli

The first plants to colonise land formed symbiotic partnerships with fungi, relationships that helped enable plant life to establish in terrestrial environments. Today, the majority of plant species still host fungal partners within their roots, forming complex belowground communities that influence plant nutrition, growth, and resilience.

Our research group investigates the factors that shape the community assembly of mycorrhizal fungi and the consequences this has for their plant hosts. To address these questions, we combine ecological theory, molecular approaches, and experimental plant biology.

A key step in this work is understanding the broader determinants of the diversity and distribution of mycorrhizal fungi. This includes processes operating at global and continental scales, such as our work documenting the diversity of arbuscular mycorrhizal (AM) fungi across Australia (see www.ausamf.com), where we are currently examining how climate, soil properties, and vegetation collectively influence the occurrences of AM fungi. Currently we are looking for opportunties to apply similar approach across Sweden and broader Fennoscandia to have a better understanding of AM fungal communities, which are often less studied due to dominance of ectomycorrhizal hosts in boreal forest systems.

Stripes of cells that were partly broken and filled with blue coloured stripes and blubsArbuscular mycorrhizal fungi colonising inside a plant root, showing intraradical hyphae and finely branched arbuscules entering plant cells (photo: Manjeet).

At smaller scales, a different set of factors shapes the fungal communities that ultimately colonise the roots of individual plants. The composition of fungi present in soil often differs from those that establish within roots, reflecting varying degrees of selectivity from both plants and fungi. For example, our research has examined how plant species identity, nutrient availability, herbivory, and pathogen infection can influence AM fungal community assembly within host plant roots.

A red-coloured map of Australia with black dots appearingMap of the AusAMF database showing the spatial distribution of sampling locations across Australia, illustrating the continental coverage of arbuscular mycorrhizal fungal diversity records (created by Adam Frew).

A central goal of our work is to move beyond monolithic abstractions of mycorrhizal function by linking fungal community composition to functional consequences. We are therefore also interested in the functional diversity of the fungi themselves. Different mycorrhizal fungal lineages can vary substantially in their effects on plants, but also in traits related to fungal growth, colonisation dynamics, and reproductive investment. These differences among fungi are important because mycorrhizal symbioses influence not only individual plants, but can also shape plant community composition and broader ecosystem processes such as nutrient and carbon cycling and ecosystem productivity. Understanding how fungal traits vary across lineages, but also how plastic these traits are, is an important step toward linking fungal biodiversity with ecological function.

Blue coloured circles and stripes showing fungal sporesArbuscular mycorrhizal fungal spores and hyphae, highlighting thick-walled propagules involved in fungal dispersal and persistence (photo: Adam Frew).

Through a combination of biodiversity data, field studies, controlled experiments, and quantitative modelling, our research aims to better understand how fungal communities assemble, how they influence plants, and how these ancient symbioses continue to shape ecosystems today. While most of the group is based at Umeå Plant Science Centre, we continue to be active in Australia through the Hawkesbury Institute for the Environment at Western Sydney University.

Johannes Messinger sitting at a desk with different cables and other equipment in front of a window that is covered by a black blind.

Messinger, Johannes - How do plants make oxygen and fix carbon dioxide?

Research

Johannes Messinger sitting at a desk with different cables and other equipment in front of a window that is covered by a black blind.Photo: Mattias Pettersson

By harvesting and converting solar energy, photosynthesis supplies the chemical energy required for essentially all life on Earth. Thereby, photosynthesis is one of the most fundamental processes on our planet. Biological water oxidation to molecular oxygen (O2) and protons, performed by the enzyme Photosystem II, is the essential starting point in oxygenic photosynthesis, while the synthesis of carbohydrates (sugars) from carbon dioxide (CO2) by the enzyme Rubisco concludes it.

In my group, we aim to understand the design principles of biological redox catalysis by studying these two fundamental reactions in detail employing a range of structural and biophysical techniques. Of specific interest is how protein-water-cofactor interactions activate base metals, such as manganese (Mn), for complex conversion reactions of abundant small molecules and to derive design principles for scalable artificial catalysts for solar water splitting as well as to improve CO2 fixation by Rubisco.

We are also interested in the assembly and repair processes of photosystem II and the regulation of photosystem II via cellular processes, for example by CO2 and bicarbonate.

Despite the enormous progress towards a molecular understanding of the water-splitting and CO2 reduction reactions there is still a tremendous lack of knowledge. This can be exemplified by the fact that there are at present no stable and efficient synthetic catalysts for water oxidation made of abundant and inexpensive base metals and that there is at present no systematic approach for improving Rubisco, which is known to be a slow and inefficient enzyme.

The purpose of our research is to fill these knowledge gaps. The underlying hypothesis is that missing information regarding the function and basic design principles of protein-water-cofactor (p-w-c) interactions prevents full comprehension and mimicking of biological catalysis. Such interactions may include, for example, protein dynamics, temporary or permanent electric fields, control of water access, and H-bonding networks facilitating the efficient coupling of electron and proton transfer.

Employing an array of structural, biophysical and computational techniques we are aiming to prepare the ground for understanding the p-w-c interplay in Photosystem II (PSII) and Rubisco. For this, we utilize time-resolved membrane inlet mass spectrometry, cryo-EM, serial crystallography at free electron lasers, x-ray spectroscopy, neutron scattering and electron paramagnetic resonance. We perform these studies within a highly collaborative international network.

Key Publications

R Hussein, A Graça, J Forsman, AO Aydin, M Hall, J Gaetcke, P Chernev, P Wendler, H Dobbek, J Messinger, A Zouni, WP Schröder (2024) Cryo–electron microscopy reveals hydrogen positions and water networks in photosystem II, Science 348, 1349-1355. DOI: 10.1126/science.adn6541

C de Lichtenberg, L Rapatskiy, M Reus, E Heyno, A Schnegg, MM Nowaczyk, W Lubitz, J Messinger, N Cox (2024) Assignment of the slowly exchanging substrate water of nature’s water-splitting cofactor, P Natl Acad Sci USA 121, e2319374121 https://doi.org/10.1073/pnas.2319374121

A Bhowmick, R Hussein, I Bogaz, PS Simon, R Chatterjee, MD Doyle, MH Cheah, T Fransson, P Chernev, I-S Kim, H Makita, M Dasgupta, CJ Kaminsky, M Zhang, J Gätcke, S Haupt, II Nangca, SM Keable, AO Aydin, K Tono, S Owada, LB Gee, FD Fuller, A Batyuk, R Alonso-Mori, JM Holton, DW Paley, NW Moriaty, F Mamedov, PD Adams, AS Brewster, H Dobbek, NK Sauter, U Bergmann, A Zouni, J Messinger, J Kern, J Yano, VK Yachandra (2023) Structural evidence for intermediates during O2 formation in Photosystem II, Nature 617, 629-636. https://doi.org/10.1038/s41586-023-06038-z

D Shevela, JF Kern, G Govindjee, J Messinger (2023) Solar energy conversion by photosystem II: principles and structures. Photosynth Res 158, 279-307. https://doi.org/10.1007/s11120-022-00991-y

R Hussein, M Ibrahim, A Bhowmick, PS Simon, R Chatterjee, L Lassalle, M Doyle, I Bogacz, I-S Kim, MH Cheah, S Gul, C de Lichtenberg, P Chernev, CC Pham, ID Young, S Carbajo, FD Fuller, R Alonso-Mori, A Batyuk, KD Sutherlin, AS Brewster, R Bolotovsky, D Mendez, JM Holton, NW Moriarty, PD Adams, U Bergmann, NK Sauter, H Dobbek, J Messinger, A Zouni, J Kern, VK Yachandra, J Yano (2021) Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition. Nat Commun 12, 6531. https://doi.org/10.1038/s41467-021-26781-z

Ekspong J, C Larsen, J Stenberg, WL Kwong, J Wang, J Zhang, EMJ Johansson, J Messinger, L Edman, T Wågberg (2021) Solar-Driven Water Splitting at 13.8% Solar-to-Hydrogen Efficiency by an Earth-Abundant Electrolyzer. Acs Sustain Chem Eng 9, 14070-14078. DOI: 10.1021/acssuschemeng.1c03565

C de Lichtenberg, CJ Kim, P Chernev, RJ Debus J Messinger (2021) The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels - implications for the water oxidation mechanism. Chem Sci 12, 12763-12775. https://doi.org/10.1039/D1SC02265B

D Shevela, HN Do, A Fantuzzi, AW Rutherford, J Messinger (2020) Bicarbonate-mediated CO2 formation on both sides of photosystem II, Biochemistry 59, 2442-2449. https://doi.org/10.1021/acs.biochem.0c00208

S Kosourov, V Nagy, D Shevela, M Jokel, J Messinger, Y Allahverdiyeva (2020) Water oxidation by photosystem II is the primary source of electrons for sustained H2 photoproduction in nutrient-replete green algae, P Natl Acad Sci USA 117, 29629-29636. https://doi.org/10.1073/pnas.2009210117

MH Cheah, M Zhang, D Shevela, F Mamedov, A Zouni, J Messinger (2020) Assessment of the manganese cluster's oxidation state via photoactivation of photosystem II microcrystals, P Natl Acad Sci USA 117, 141-145. https://doi.org/10.1073/pnas.1915879117

J. Kern, R. Chatterjee, I.D. Young, F.D. Fuller, L. Lassalle, M. Ibrahim, S. Gul, T. Fransson, A.S. Brewster, R. Alonso-Mori, R. Hussein, M. Zhang, L. Douthit, C. de Lichtenberg, M.H. Cheah, D. Shevela, J. Wersig, I. Seuffert, D. Sokaras, E. Pastor, C. Weninger, T. Kroll, R.G. Sierra, P. Aller, A. Butryn, A.M. Orville, M.N. Liang, A. Batyuk, J.E. Koglin, S. Carbajo, S. Boutet, N.W. Moriarty, J.M. Holton, H. Dobbek, P.D. Adams, U. Bergmann, N.K. Sauter, A. Zouni, J. Messinger, J. Yano, V.K. Yachandra, Structures of the intermediates of Kok's photosynthetic water oxidation clock, Nature, 563 (2018) 421-425. https://doi.org/10.1038/s41586-018-0681-2

W.L. Kwong, E. Gracia-Espino, C. Choo, R. Sandström, T. Wågberg, J. Messinger, Cationic vacancy defects in iron phosphide: A promising route toward efficient and stable hydrogen evolution by electrochemical water splitting, ChemSusChem, 10 (2017) 4544-4551. https://doi.org/10.1002/cssc.201701565

H. Nilsson, F. Rappaport, A. Boussac, J. Messinger, Substrate-water exchange in photosystem II is arrested before dioxygen formation, Nat Commun, 5 (2014). https://doi.org/10.1038/ncomms5305

N. Cox, J. Messinger, Reflections on substrate water and dioxygen formation, BBA-Bioenergetics, 1827 (2013) 1020-1030. https://doi.org/10.1016/j.bbabio.2013.01.013

L.V. Kulik, B. Epel, W. Lubitz, J. Messinger, Electronic structure of the Mn4OxCa cluster in the S0 and S2 states of the oxygen-evolving complex of photosystem II based on pulse 55Mn-ENDOR and EPR Spectroscopy, J Am Chem Soc, 129 (2007) 13421-13435. https://doi.org/10.1021/ja071487f

J. Messinger, M. Badger, T. Wydrzynski, Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II, P Natl Acad Sci USA, 92 (1995) 3209-3213. https://doi.org/10.1073/pnas.92.8.3209

Portrait photo of Jian-Feng Mao taken in a greenhouse with trees in the background

Mao, Jian-Feng - Plant genomics

Research

Portrait photo of Jian-Feng Mao taken in a greenhouse with trees in the backgroundPhoto: Mattias Pettersson Surfing the data ocean of plant genomes, we (data analysts) are discovering hidden intricacies (genome sequencing and assembly), investigating what it looks like (annotation and characterization), where and why they are there (evolutionary inference), and predicting what, when and how it will be (functional exploitation, genomic predication).

Our research interests lie in plant genomics and tree breeding, particularly in genome evolution and genomic mechanisms of various biological processes such as secondary metabolite biosynthesis and biotic/abiotic response, allele-specific gene expression. We are also keen on implementing computation-intensive multi-omics tools/strategies in dissecting complex systems to support efficient investigation, manipulation and breeding. We finished several high-quality genome assemblies for a wide-range of plant species, including a de novo genome assembly with contig N50>50 Mb for a conifer species (Cupressaceae) with ~10 Gb genome size, T2T gap-less genome assembly for two poplar species by sequencing an interspecific F1 hybrid, chromosome-scale genome assembly for yellowhorn, ginger, azaleas, oak, lilac and tetraploid Salvia splendens.

We developed a novel k-mer based genome software (https://github.com/zhangrengang/SubPhaser) to assist chromosome assignment in allopolyploid and hybrids, and computational tools/pipelines for centromere identification (https://github.com/ShuaiNIEgithub/Centromics), lncRNA predication (https://github.com/xuechantian) and allele-specific gene expression (https://github.com/shitianle77/Allele_auto) analyses.


Complex scientific illustration consisting of five individual graphs illustrating the experimental design, a time-ordered gene co-expression network for UV-B and UV-C, UV-B and UV-C, a short summary of the UV-B and UV-C response in pine and a illustration of the network comparison method

UV-B and UV-C responses in pine

Key publications

  • Nie, S., S.-W. Zhao, T.-L. Shi, W. Zhao, R.-G. Zhang, X.-C. Tian, J.-F. Guo, X.-M. Yan, Y.-T. Bao, Z.-C. Li, L. Kong, H.-Y. Ma, Z.-Y. Chen, H. Liu, Y. A. El-Kassaby, I. Porth, F.-S. Yang and J.-F. Mao (2023). "Gapless genome assembly of azalea and multi-omics investigation into divergence between two species with distinct flower color." Horticulture Research 10(1): uhac241.
  • Jia, K. H., Z. X. Wang, L. Wang, G. Y. Li, W. Zhang, X. L. Wang, F. J. Xu, S. Q. Jiao, S. S. Zhou, H. Liu, Y. Ma, G. Bi, W. Zhao, Y. A. El-Kassaby, I. Porth, G. Li, R. G. Zhang and J. F. Mao (2022). "SubPhaser: a robust allopolyploid subgenome phasing method based on subgenome-specific k-mers." New Phytol 235(2): 801-809.
  • Xu, J., H. Luo, S. S. Zhou, S. Q. Jiao, K. H. Jia, S. Nie, H. Liu, W. Zhao, X. R. Wang, Y. A. El-Kassaby, I. Porth and J. F. Mao (2022). "UV-B and UV-C radiation trigger both common and distinctive signal perceptions and transmissions in Pinus tabuliformis Carr." Tree Physiol 42(8): 1587-1600.
  • Jia, K. H., W. Zhao, P. A. Maier, X. G. Hu, Y. Jin, S. S. Zhou, S. Q. Jiao, Y. A. El-Kassaby, T. Wang, X. R. Wang and J. F. Mao (2020). "Landscape genomics predicts climate change-related genetic offset for the widespread Platycladus orientalis (Cupressaceae)." Evol Appl 13(4): 665-676.
  • Yang, F. S., S. Nie, H. Liu, T. L. Shi, X. C. Tian, S. S. Zhou, Y. T. Bao, K. H. Jia, J. F. Guo, W. Zhao, N. An, R. G. Zhang, Q. Z. Yun, X. Z. Wang, C. Mannapperuma, I. Porth, Y. A. El-Kassaby, N. R. Street, X. R. Wang, Y. Van de Peer and J. F. Mao (2020). "Chromosome-level genome assembly of a parent species of widely cultivated azaleas." Nat Commun 11(1): 5269.
Portrait photo of Laura Bacete standing in front of a waterfall

Bacete, Laura - Plant cell wall dynamics

Research

Portrait photo of Laura Bacete standing in front of a waterfall Did you know that every second, plants produce 3,000 tons of cellulose, a key component of their cell walls? These walls play a crucial role in plant growth, adaptation to environmental conditions, and ultimately, in sustaining life on our planet. Furthermore, cell walls are essential for food production, clothing (cotton), wood, and even bioenergy. And they are renewable, climate-friendly, and naturally produced, making them crucial in the fight against climate change. In my research group, we want to know more about this fascinating plant structure, especially about the dynamic processes that allow it to adapt to changing conditions.

The cell wall is a complex network of carbohydrates and proteins that plays a crucial role in plant growth and adaptation to environmental conditions. The maintenance of cell wall integrity is essential for regulating the functional integrity of cell walls during development and stress. Plant cell wall integrity monitoring systems constantly survey the status of cell walls and initiate a series of responses when they are altered. Interestingly, plant cell wall integrity seems to be related to adaptation to challenging environments, since some cell wall mutants are more resistant to certain stresses.A 3-D illustration demonstrating the importance of cellulose for circular economy: trees of different size are displayed on the left side of a circle, fields and gras loan in the middle above a root network and circle of woody parts in the bottom part of the circle; on the right upper part a house, emissions and cloads are illustrated and centrally a white circle. “The importance of cellulose for circular economy”. Image created with Midjourney text-to-image AI.

Understanding the mechanisms behind cell wall integrity monitoring and response is a key area of research in our lab. Time and dynamics are the keywords that define our research group’s approach to cell walls. We are interested in understanding how cell wall integrity is regulated over time and how it responds to changes in the environment. By studying these dynamic processes, we aim to uncover the mechanisms that govern plant growth and development and pave the way for innovative solutions that benefit agriculture and the environment. Specifically, we explore the following research interests:

  • Understanding the relationship between cell wall composition and mechanical characteristics: We investigate how the composition of cell walls changes during plant development and interaction with the environment and how these changes affect their mechanical characteristics.
  • Defining the meaning of cell wall integrity: We explore the homeostasis of plant cell walls in the context of plant growth, adaptation, and response to environmental stresses.
  • Understanding how environmental stresses impact cell wall homeostasis: We study how environmental stresses, such as drought and pathogen attacks, affect cell wall homeostasis.
  • Investigating how the plant integrates cell wall information into developmental processes: We explore how the plant integrates information about cell wall composition and mechanical properties into its developmental processes, such as cell cycle progression.Schematic 3D illustration of the primatry plant cell wall with cellulose fibres illustrated as thick green tubes, pectins as yellow thinner lines twinin on top and within of the cellulose network, hemicellulose displayed as light blue shorter lines is intertwining between the cellulose fibres and below are proteins displayed as rounded structures connecting the cell wall with the plasmamembraneSchematic illustration of the primary plant cell wall and its key components. The cell wall is composed of cellulose, hemicellulose, and proteins, including the ectodomains of cell wall integrity (CWI) sensors, which play a crucial role in monitoring cell wall’s functional integrity.

Our lab employs a range of cutting-edge technologies to achieve our research goals. These include:

  • Brillouin and confocal microscopies: We use these imaging techniques to visualize changes in cell wall composition and mechanical properties.
Two photos displaying the set up of a Brillouin microscope next to each other on top and a schematic work flow describing illustrated below from laser excitation to data processing and analaysisBrillouin microscopy, a non-invasive imaging technique used to visualize changes in the mechanical properties of plant cell walls. It works by using laser light to probe the sample, which scatters light at different frequencies due to acoustic vibrations. By analyzing the frequency shift in the scattered light, the mechanical properties of the sample, such as stiffness and elasticity, can be determined.
  • Biochemical analysis: We use various biochemical analysis techniques, including GC/LC-MS and FTIR, to investigate the chemical composition of cell walls.
  • Molecular biology: We use various molecular biology techniques such as cloning, qRT-PCR, and RNAseq to investigate gene expression patterns related to cell wall integrity.
  • Cell wall fractionation and glycome profiling: We use these techniques to analyze the polysaccharides and proteins present in plant cell walls.
  • Study of signaling cascades: We explore the various signaling pathways involved in cell wall integrity monitoring and responses, especially hormone pathways (jasmonic, salicylic and abscisic acid) and pattern-triggered immunity-related responses (Ca2+ input, MAPK phosphorylation, ectopic lignin deposition, etc.).
Four Arabidopsis roots are displayed next to each other: the cell wall is coloured in blue and the inner part in magenta; the cell wall of the left root looks like a continouse line, while the one of two middle roots displays several holes and deformations; the cell wall of the right root looks thinner than the first one but not as strongly affected like the middle onesActivation of signalling cascades in Arabidopsis thaliana roots under different cell wall stresses. Confocal microscopy picture. From left to right: mock, isoxaben (cellulose biosynthesis inhibitor), osmotic stress and isoxaben+osmotic stress. Picture by Julia Schulz, Thorsten Hamann’s lab, NTNU (Norway).
  • Analysis of traits of agronomical interest: These include resistance to biotic (pathogens) and abiotic (drought, temperature, etc.) stresses, saccharification, biomass production, etc.
  • Computational modelling: We use different models (logical, finite-elements, etc.) to integrate our different data into models that enable us to analyse and predict cell wall behaviour.

Our lab is committed to using multidisciplinary approaches and novel methodologies to solve complex problems in plant research. Our research has far-reaching implications, including improving crop yields, creating new bio-based materials, and developing sustainable energy sources. You can also read more about our research on our Scandinavian Green Cell Wall Dynamics group page. Illustration of the Laura Bacete's multidisciplinary research approach displaying the different components involved Generating knowledge through data integration. Our multidisciplinary approach combines different data sources, which must be integrated to obtain a complete understanding of cell wall integrity. We employ computational models for effective data integration.

Selected publications:

Bacete, L., Schulz, J., Engelsdorf, T., Bartosova, Z., Tichá, T., Vaahtera, L., Yan, G., Gerhold, J., Øvstebø, C., Gigli-Bisceglia, N., Margueritat, J., Kollist, H., Dehoux, T., McAdam, S.A.M., Hamann., T. (2022) THESEUS1 modulates mechanical characteristics of cell walls and abscisic acid production in Arabidopsis thaliana. PNAS, 119 (1) e2119258119. DOI: 10.1073/pnas.2119258119.

  • One of the first applications of Brillouin Microspectroscopy in plants. We used this novel technique to study changes in biophysical characteristics of A. thaliana cell walls in response to cell wall damage and hyperosmotic pressure conditions.
  • To complement the Brillouin data, we studied downstream signaling processes mediated by phytohormones quantified using LC-MS/MS.
  • By integrating these results, we have developed a model explaining how a plant cell could generate specific responses to either cell expansion and shrinkage, based on interactions between the plant cell wall and plasma membrane.

Molina, A., Miedes, E., Bacete, L., Rodríguez, T., Mélida, H., Denancé, N., Sánchez-Vallet, A., Rivieré, M.P., López, G., Freydier, A., Bartel, X., Pattathil, S., Hahn, M. and Goffner, D. (2021) Arabidopsis cell wall composition determines disease resistance specificity and fitness. PNAS 118(5). DOI: 10.1073/pnas.2010243118

  • Interdisciplinary work using mathematical modelling and biochemical analysis to link Arabidopsis thaliana mutants with alterations in cell wall composition to improvement in resistance to biotic / abiotic stress.

Bacete, L., Miedes, E., Mélida, H., López, G., Denancé, N., Marco, Y. and Molina, A. (2020) ARABIDOPSIS RESPONSE REGULATOR 6 (ARR6) affects cell wall composition and mediates resistance to Plectosphaerella cucumerina and Ralstonia solanacearum. MPMI 33(5). DOI: 10.1094/MPMI-12-19-0341-R.

  • ARR6 was believed to act exclusively as a mediator of the plant’s hormonal responses. However, in this work we demonstrated ARR6 is also involved in the control of cell-wall composition and disease resistance, which stated the role of the plant cell wall in the modulation of specific immune responses.
  • Selected as Editor’s Pick for September 2020 issue of MPMI Journal.
  • Top cited paper in MPMI Journal during 2020.

Mélida, H., Bacete, L., Ruprecht, C., Rebaque, D., Del Hierro, I., López, G., Bunner, F., Pfrengle, F. and Molina, A. (2020). Arabinoxylan-oligosaccharides act as Damage Associated Molecular Patterns in plants regulating disease resistance. Front. Plant. Sci. 11, 1210. DOI: 10.3389/fpls.2020.01210.

  • Continuation of the research done during my PhD.
  • Using cell wall fractions extracted from the arr6 mutant, we were able to identify an arabinoxylan pentasaccharide with strong immunomodulatory activity.
  • In this work, we propose 33-α-l-arabinofuranosyl-xylotetraose (XA3XX) as a hemicellulose-derived DAMP triggering strong immune responses in Arabidopsis thaliana and enhancing crop disease resistance.

Bacete, L., Mélida, H., Miedes, E. and Molina, A. (2018) Plant cell wall-mediated immunity: cell wall changes trigger disease resistance responses. Plant J., 93, 614. DOI: 10.1111/tpj.13807

  • State-of-science review about the prominent role of plant cell wall in defense to pathogens.
  • Ranked in the top 20 most downloaded articles in The Plant Journal during 2018.
Portrait photo of Stephan Wenkel

Wenkel, Stephan - Small proteins controlling development and adaptation

Research

Portrait photo of Stephan Wenkel We are interested in understanding how plants use small proteins to dynamically adjust growth and development in response to environmental changes.

There is growing evidence that proteomes are more complex than previously anticipated. For instance, until recently, genes coding for proteins with fewer than 100 amino acids were often labeled as artefacts. As a result, many such small open reading frames were excluded in genome annotations. Moreover, in addition to these single, individual, open reading frames, small proteins can also arise through processes such as alternative splicing or alternative use of transcription start sites. Thus, one gene can code for more than one protein. These and other processes result in a much larger number of protein species in a given cell compared to the number of protein-coding genes in the genome.

Figure showing a circle with a blue and green coloured outer circel and lines connecting different parts of the outer circle with each otherFigure 1: Circos plot of individual microProtein candidates. Links indicate conservation between species based on OrthoFinder. Red, in all 11 species; dark blue, exclusively in all five metazoans; light blue, only in metazoans; dark green, exclusively in all six plants; light green, only in plants. Has: Homo sapiens; Mmu: Mus musculus; Dre: Danio rerio; Dme: Drosophila melanogaster; Cel: Caenorhabditis elegans; Ath: Arabidopsis thaliana; Sly: Solanum lycopersicum; Stu: Solanum tuberosum; Sbi: Sorghum bicolor; Osa: Oryza sativa; Zma: Zea mays. From: Straub and Wenkel, Genome Biol. Evol. 9(3):777–789, 2017.

In our research, we use both protein-centric approaches (starting with the identification and characterization of specific small proteins, often microProteins) and process-oriented approaches, where we try to understand how plants dynamically change their developmental decisions in response to environmental changes. To identify small proteins, such as microProteins in any sequenced genome, we developed miPFinder that can classify small proteins as microProteins (Fig. 1, Straub and Wenkel, 2017). Biological processes we study involve the promotion of growth in response to shading or the induction of flowering in response to day length and temperature. One of the things we have been able to show is that small B-box microProteins can strongly influence flowering (Fig.2 and Graeff et al., 2016).

Five Arabidopsis plants in front of a black background, only the first one has inflorescencesFigure 2: Transgenic plants with elevated microProtein levels are late flowering under inductive long day conditions. Image of representative late flowering mutants co and ft and transgenic plants overexpressing two microProteins (35S::miP1a and 35S::miP1b) compared to a Col-0 wild type plant of the same age. From: Graeff et al., PLOS Genetics | DOI:10.1371/journal.pgen.1005959; 2016.

The next steps

Owing to their small size and the predictability of protein interactions, microProteins are suitable for the regulation of biotechnological processes. With the help of new genome engineering tools, we are currently exploring the possibilities of generating microProteins de novo to control developmental pathways at will.

Harry Wu in a forest

Wu, Harry - Quantitative Genetics and Tree Breeding

Research

Harry Wu in a forest

Our group conducts research on forest genetics and tree breeding through understanding and dissecting genetic base of genetic variation for quantitative traits, including tree growth and form traits, wood quality traits, phenology traits, and biotic and abiotic resistance traits.

The starting point is to investigate the genetic base of the phenotypic variation we observed between individual trees in forest stands. The first question we ask is how much of this variation between individual trees is due to genetic differences, and how much due to environmental factors. Then we need to find out the number of genes that are responsible for the genetic variation, and how these genes interact to influence the performance of trees in different environments. This basic knowledge can then be used in the design of breeding programmes for increased growth rate and quality of wood products in forest plantations.

To design efficient breeding programmes and to increase genetic gain, we also need to identify the best native tree populations for selection and breeding for a specific forest region. This involves research on genotype by environment interaction and on response curves of existing populations and genotypes, so that we can delineate optimal breeding trees (population) that match the environment (breeding zone). After assembling a breeding population for further improvement, we need to design the best breeding strategy. We not only have to select the individuals that we want to use as a parent, to produce the best progeny, we also need to identify the ideal combinations of parents (mating design). Furthermore, we need to deal with inbreeding depression.

Another important question we need to address is how to deal with improvement of multiple traits that are adversely related, such as wood quantity vs. wood quality. First we need to find out the genetic causes of such correlation, using quantitative and molecular tools. Then we develop a gene model (locus and parametric model) and use simulations to identify the best selection and mating methods for dealing with such adversely correlated multiple traits. We also study the suitability of different mating and selection methods when it comes to avoiding or removing inbreeding depression in advanced breeding programmes.

On the left photo, three persons are taking samples in a Scots pine forest. On the right site Harry Wu and two other persons are standing next to an Eucalyptus tree in China.Left: Sampling for phenology observation and DNA in Scots pine; right: Inspecting Eucalyptus plus tree in China.

With the advance of gene sequencing technology, we start to study associations between individual genes or gene complexes with phenotype variation in trees. We study candidate genes or genome-wide approach to increase knowledge about the association between variations in DNA and observable phenotype variation. In addition, we are developing a quantitative genetics tool that integrates DNA sequence-based variation with phenotypic data, in order to improve the efficiency of genetic improvement in trees. This involves the development of advanced methods for breeding value prediction, such as genomic Best Linear Unbiased Prediction (G-BLUP) and Genome-wide Breeding Value (GBV).

Key publications

  • Niu, S., Li, J., Bo, W., Yang, W., …, Wei, H., & Wu, H. X. (2022).The Chinese pine genome and methylome unveil key features of conifer evolution. Cell 185, 1–14. doi.org/10.1016/j.cell.2021.12.006
  • Chen, ZQ., Zan, Y., … Wu, H. X. (2021). Leveraging breeding programs and genomic data in Norway spruce (Picea abies L. Karst) for GWAS analysis. Genome Biology 22, 179. doi.org/10.1186/s13059-021-02392-1
  • Calleja-Rodriguez, A., Chen, Z., Suontama, M., Pan, J., & Wu, H. X. (2021). Genomic predictions with nonadditive effects improved estimates of additive effects and predictions of total genetic values in Pinus sylvestris. Frontiers in Plant Science, 12: 666820. doi.org/10.3389/fpls.2021.666820
  • Wu, H. X., Kerr, R., Chen, Z., & Ivkovic, M. (2021). Balancing breeding for growth and fecundity in radiata pine (Pinus radiata D. Don) Breeding Programme. Evolutionary Applications, 14: 834–846. doi: 10.1111/eva.13164
  • Wu, H. X, Hallingbäck, H.R., Sánchez, L. (2016). Performance of seven tree breeding strategies under conditions of inbreeding depression. Gene, Genome and Genetics. 6:529-540. doi: 10.1534/g3.115.025767.
  • Li, X.G., H. X. Wu, and S.G. Southerton. (2010). Seasonal reorganization of the xylem transcriptome at different tree ages reveals novel insights into wood formation in Pinus radiata D.Don. New Phytologist. 187:764–776.
Stéphane Verger in the UPSC Growth Facility

Verger, Stéphane – Mechanics and Dynamics of Cell-Cell Adhesion in Plants

Research

Stéphane Verger in the UPSC Growth FacilityPhoto: Johan Gunséus

Cell-cell adhesion is one of the most fundamental features of multicellular organisms. We are studying the mechanisms involved in cell-cell adhesion in both Arabidopsis and Poplar using novel and interdisciplinary approaches, including biophysical tools, confocal microscopy and computational modeling.

All living organisms experience physical stress, and notably tensions, as tissues grow. Adhesion between cells provides resistance to such forces and maintains the integrity of the organism. In turn, adhesion can be modulated, e.g. to promote cell migration in animals or organ shedding in plants. The relation between tension and adhesion is a fundamental question in the development of multicellular organisms, yet it remains largely under-studied in plants.

Cell-cell adhesion in plants largely relies on a layered structure composed of a pectin-rich middle lamella located between the walls of adjacent cells (Fig. 1). Conversely, cell separation events such as organ abscission, usually require an active degradation of the middle lamella by cell wall remodeling enzymes such as pectin methylesterases and polygalacturonases. Interestingly, such enzymes are also required for loosening the cell wall and allowing growth. In addition, turgor pressure puts the cell walls under tension; differential growth or patterns of tension can generate mechanical conflicts between adjacent cells, thus threatening cell adhesion (Fig. 1). How cell adhesion is maintained is thus not trivial when considering the coupling between forces and wall chemistry in a growing tissue.

The figure illustrates tension and adhesion in plant tissues.Fig 1: Tension and adhesion in plants. Plant cells adhere through their cell wall, while tissue scale tension tends to pull the cells apart.

Several mutants display cell adhesion defects. Among them, quasimodo1 and quasimodo2 (Fig. 2) are mutated in enzymes involved in the synthesis of the homogalacturonans (HG), the main component of the pectins and constituent of the middle lamella. However, the regulation of cell adhesion is more complex: We have previously identified suppressors of these mutants and revealed that the decrease in HG content is not the sole cause of the loss of cell adhesion in these mutants and that a feedback signal from the wall contributes to this phenotype. Beyond pectins, mutants affected in actin filament nucleation, mechanosensing and epidermal identity show cell adhesion defects, which strongly suggest that cell adhesion is under a complex, biochemical and biomechanical, control in plants.

Microscope images comparing cell adhesion defects in quasimodo mutants with wildtype plants. Fig 2: Cell adhesion defects in quasimodo2-1 cotyledon pavement cell (bottom Left) and quasimodo 1-1 dark-grown hypocotyl (bottom right), as compared to wildtype (top panels). Images are z-projection (maximal intensity) of 3D confocal stack from propidium iodide stained samples.

So far the topic has remained very challenging to study in plants, notably because the physical parameters related to cell adhesion are difficult to quantify (e.g. tensile stress at the cell-cell connections and adhesion strength). However, tools usually designed for material sciences are increasingly adapted to biophysics and living samples. For example Atomic Force Microscopy (AFM, Fig. 3) and micro-mechanical tools to deform and measure cells and tissues mechanical properties in a quantitative way, as well as mechanical models to predict tension patterns in tissues, can now be used to study cell-cell adhesion in plants.

Atomic Force Microscopy images from 4-day old wild type (A-C) and qua1-1 (D-F) cotyledons. Fig 3: Atomic Force Microscopy (AFM) images from 4-day old wild type (A-C) and qua1-1 (D-F) cotyledons. (A and D) 3D rendering of the epidermis topography. Lighter regions are more elevated than darker ones. (B and E) Topography map. (C and F) Stiffness map of the outer walls, ranging from 5.5 MPa (black) to 7 MPa (white). While for the wild type, the cell-cell connections form a clearly defined “valley” and are stiffer, in qua1-1 these regions are flatter and softer. The red arrow in panel M points to holes in the flat and soft region, suggesting that this zone may be a sheet of outer wall detached from the underlying cell. Scale bars, 10 μm.

Taking advantage of these recent developments, our aim is to unravel the mechanics and dynamics of cell adhesion in plants at unprecedented resolution. More precisely our goal is:

  • To identify the mechanisms through which plants dynamically control cell-cell adhesion, focusing on the role of mechanosensing, cytoskeleton dynamics and the cell wall secretion.
  • To study the dynamic control of cell adhesion taking place during wood fiber cell elongation, and its importance for the chemical and mechanical properties of Poplar wood.

For this purpose we combine the use of genetic, chemical and mechanical perturbations together with quantitative live imaging, micromechanical and cell wall analyses, and computational modeling.

While part of our work is carried out on the model species Arabidospis thaliana, providing basic knowledge on the questions of cell-cell adhesion in plants, in the long term our research may lead to the generation of improved trees for traits such as wood mechanical strength and biomass conversion.


Key Publications

  • Demes E & Verger S (2023). High-throughput characterization of cortical microtubule arrays response to anisotropic tensile stress. BMC Biology, 21 (1), 1-13. https://doi.org/10.1186/s12915-023-01654-7
  • Atakhani A, Bogdziewiez L, Verger S (2022) Characterising the mechanics of cell–cell adhesion in plants. Quantitative Plant Biology. 3, 2022, e2. https://doi.org/10.1017/qpb.2021.16
  • Malivert A, Erguvan Ö, Chevallier A, Dehem A, Friaud R, Liu M, Martin M, Peyraud T, Hamant O, Verger S (2021) FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot. PLoS Biology. 19, 11, e3001454. https://doi.org/10.1371/journal.pbio.3001454
  • Erguvan Ö, Louveaux M, Hamant O, Verger S (2019). ImageJ SurfCut: a user-friendly pipeline for high-throughput extraction of cell contours from 3D image stacks. BMC Biol. 17(1):38. https://doi.org/10.1186/s12915-019-0657-1
  • Verger, S., Long, Y., Boudaoud, A., Hamant, O. (2018). A tension-adhesion feedback loop in plant epidermis. eLife. 7, e34460. https://elifesciences.org/articles/34460
  • Verger, S., Chabout, S., Gineau, E., Mouille, G. (2016). Cell adhesion in plants is under the control of putative O-fucosyltransferases. Development. 143, 2536-2540. http://dev.biologists.org/content/143/14/2536.long
Åsa Strand sitting at her desk in her office at the Umeå Plant Science Centre

Strand, Åsa - Regulation and control of cellular energy metabolism

Research

Åsa Strand sitting on her desk in her office at Umeå Plant Science CentrePhoto: Mattias Pettersson

The overall goal of the research in my group is to understand the regulation and control of cellular energy metabolism. A tight choreography of the nuclear and organellar genomes within the eukaryotic cell is essential for the establishment of cellular energy metabolism during development and for acclimation to changing demands on cellular metabolism when growth conditions are changing. Our projects endeavour to identify the intracellular signalling mechanisms that coordinate the dynamic interaction between the different genomes during major cellular metabolic transitions.

Mitochondria and chloroplasts are the powerhouses of the cell and exposure to stress inhibits metabolic activities leading to severe constraints on cellular energy homeostasis. Failure to restore either respiration or photosynthesis severely affects vigour, and possibly survival, of the organism. Communication between the organelles and the nucleus, so called retrograde signalling networks, are essential for the recovery of energy metabolism following stress but also for the establishment of cellular energy metabolism. Mutants where this communication is impaired have dysfunctional organelles and severely impaired cellular energy metabolism. For plants this can have fatal consequences, and in humans dysfunctional mitochondria-to-nucleus signalling has been linked to the aging process and to several severe diseases.

To address the regulatory mechanisms that control the dynamic interaction between the different genomes we take an integrative approach using a combination of genetics, molecular biology, biochemistry, cell biology and biological modelling. We also combine several model systems including Arabidopsis plants and an Arabidopsis cell line, as well as conifers such as spruce and pine. Our work is divided into two large lines of research composed of several sub-projects.

Chloroplast development and establishment of photosynthetic activity

In this project the focus is on the signalling network controlling the development of functional chloroplasts and the establishment of photosynthetic activity. This developmental process drives a cellular metabolic shift in the cell from requiring external energy sources for growth and development to becoming a supplier of energy to support growth of new developing tissues. This transition in cellular metabolic activity requires a complex regulatory network involving several cellular compartments, extensive chromatin reorganisation and massive transcriptional changes. Several sub-projects address the different aspects of this process.

Illustration depicting signalling components that are involved in chloroplast development and establishment of photosynthetic activityFigure 1. Overview of the signalling components controlling the development of functional chloroplasts and the establishment of photosynthesis in Arabidopsis (Hernández-Verdeja et al., Physiol Plant. 2020).

Integration of energy and retrograde signalling pathways during plant stress responses

Within this project we investigate the integration of energy and retrograde signalling pathways during plant stress responses. We have identified CDKE1 as a central component receiving stress induced retrograde signals for both chloroplasts and mitochondria. Furthermore, CDKE1 regulates the redistribution of energy and metabolism towards either growth or stress response. Given the position of CDKE1 in the Mediator complex, this kinase could act as a sensitive relay between organellar retrograde signals and their cognate promoter-bound, stress-induced TFs and RNA polymerase II (RNAP II), regulating the expression of appropriate genes in response to stress conditions. Several sub-projects address the interaction partners of CDKE1 and the targets for its kinase activity.

Illustration depicting the interplay between energy and retrograde signalling pathways during stress responses in plantsFigure 2. Integration of retrograde signalling and energy related pathways by CDKE1 and the Mediator complex (Crawford et al., J Exp Bot. 2017).
Anita Sellstedt in the KBC cafeteria

Sellstedt, Anita - Energy Production by Microorganisms

Research

Anita Sellstedt in the KBC cafeteriaPhoto: Fredrik Larsson

The aim of our research is to study energy production in microorganisms. The research covers several projects, of which the three main projects will briefly be presented below.

Hydrogen metabolism of Frankia

Nitrogen fixation occurs in Frankia both in free-living as well as in symbioses and may contribute as much as a quarter of the total yearly biologically fixed nitrogen globally in terrestrial ecosystem.

The most important recent achievement in the Frankia research field is the sequencing of three Frankia genomes. We were able to show that there are large differences in the genome sizes. Frankia EANpec1 was found to have the largest genome with 9.0 Mb, while Frankia ACN14a had an intermediate size of 7.5 Mb and Frankia HFPCcI3 was the smallest at 5.4 Mb. These numbers were correlated with geographical origin, host plant distribution and repeated sequences, such as IS. Our findings open up a new era in Frankia research, yielding possibilities to explore the molecular biology of Frankia.

An inevitable source of energy-inefficiency in the nitrogen-fixation process is the evolution of hydrogen; as much as 25% of the in vitro electron-flow through nitrogenase goes to hydrogen evolution. Some nitrogen-fixing systems have dealt with this problem of energy loss through evolving an extra enzyme, called uptake hydrogenase, which is very common in Frankia.

Round vesicles of the bacterium Frankia are shown on the left side and elongated cells of Chalara parvispora on the right side. Left: Light micrograph of the bacterium Frankia showing vesicles; right: Light micrograph of our isolate of Chalara parvispora

Cyanobacteria in association with boreal mosses

We were able to discover that cyanobacteria live in association with feather mosses in the boreal area. We also discovered that they are able of fixing nitrogen and thereby contributing to the N status of that ecosystem.

Heterotrophic production of lipids by algae

Algae are commonly autotrophic carbon dioxide fixing prokaryotes. They are also able of storing different compounds under a variety of conditions. This year a Thesis from my laboratory revealed that some microalgae are able to use glycerol as a carbon source under growing in heterotrophic conditions. Interestingly, a microalgae isolated in the lab and originating from Umeå area has this trait and also accumulated significant amounts of lipids under this condition.


Key Publications

  • Leul M, Normand P, Sellstedt A (2009). The phylogeny of uptake hydrogenases. Int Microbiol. 12(1): 23-28.
  • Normand et al., (2007). Genome structure reflects host biogeography in three plant symbionts Frankia sp. strains. Genome Research, 17, 7-15.
  • Mohapatra A, Leul M, Mattsson U, Sellstedt A (2004). A hydrogen-evolving enzyme is present in Frankia R43. FEMS Microbiol.Lett.236: 235-240
  • DeLuca TH, O Zackrisson, M-C Nilsson, A Sellstedt (2002). Quantifying nitrogen fixation in feather moss carpets. Nature. 419: 917-920.
  • Nzayisenga JC, Eriksson K, Sellstedt A. 2018. Mixotrophic and heterotrophic production of lipids and carbohydrates by a locally isolated microalga using wastewater as growth medium. Bioresource Technology 257: 260-265.

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