Maere Lab | Evolutionary Systems Biology
Steven Maere
CV
1999 MSc Engineering Physics, Ghent University
2001 MSc Biotechnology, Ghent University
2002-2006 Predoctoral Fellow of the Research Foundation - Flanders (FWO)
2006 PhD in Computational Biology, Ghent University
2006-2013 Postdoctoral Fellow of the Research Foundation - Flanders (FWO)
2008-2009 Visiting postdoc UC Berkeley (Eisen lab), sponsored by FWO, Fulbright
and BAEF
2009-now PI, Center for Plant Systems Biology, VIB
2013-2018 Assistant Professor, Ghent University
2018-now Associate Professor, Ghent University
Research
Group Leader
VIB / Ghent University
Evolutionary Systems Biology
Technologiepark 927
B-9052 Gent
BELGIUM
Publications
* co-first or co-last author
(47) Wendrich, J.R. *, Yang, B. *, Vandamme, N. *, Verstaen, K. *, Smet, W., Van de Velde, C., Minne, M., Wybouw, B., Mor, E., Arents, H.E., Nolf, J., Van Duyse, J., Van Isterdael, G., Maere, S., Saeys, Y. *, De Rybel, B. * (2020) Vascular transcription factors guide plant epidermal responses to limiting phosphate conditions. Science 370: eaay4970.
(46) Parry, G., Provart. N.J., Brady. S.M., Uzilday, B.; Multinational Arabidopsis Steering Committee (2020) Current status of the multinational Arabidopsis community. Plant Direct 4:e00248.
(45) Gallone, B. *, Steensels, J. *, Mertens, S., Dzialo, M.C., Gordon, J.L., Wauters, R., Theßeling, F.A., Bellinazzo, F., Saels, V., Herrera-Malaver, B., Prahl, T., White, C., Hutzler, M., Meußdoerffer, F., Malcorps, P., Souffriau, B., Daenen, L., Baele, G., Maere, S. *,Verstrepen, K.J. * (2019) Interspecific hybridisation facilitates niche adaptation in beer yeast. Nat Ecol Evol. 3:1562–1575.
(44) Bhosale, R., Maere, S., De Veylder, L. (2019) Endoreplication as a potential driver of cell wall modifications. Curr Opin Plant Biol. 51:58-65.
(43) Bhosale, R. *, Boudolf, V. *, Cuevas, F. *, Lua, R., Eekhout, T., Hua, Z., Van Isterdael, G., Lambert, G.M., Nowack, M.K., Smith, R.S., Vercauteren, I., De Rycke, R., Storme, V., Beeckman, T., Larkin, J.C., Kremer, A., Höfte, H., Galbraith, D.W., Kumpf, R.P., Maere, S. *, De Veylder, L. * (2018) A spatiotemporal DNA endoploidy map of the Arabidopsis root reveals roles for the endocycle in root development and stress adaptation. Plant Cell 30: 2330-2351.
(42) Li, F.-W., Brouwer, P., Carretero-Paulet, L., Cheng, S., de Vries, J., Delaux, P.-M., Eily, A., Koppers, N., Kuo, L.-Y., Li, Z., Simenc, M., Small, I., Wafula, E., Angarita, S., Barker, M.S., Bräutigam, A., dePamphilis, C., Gould, S., Hosmani, P.S., Huang, Y.-M., Huettel, B., Kato, Y., Liu, X., Maere, S., McDowell, R., Mueller, L.A., Nierop, K.G.J., Rensing, S.A., Robison, T., Rothfels, C.J., Sigel, E.M., Song, Y., Timilsena, P.R., Van de Peer, Y., Wang, H., Wilhelmsson, P.K.I., Wolf, P.G., Xu, X., Der, J.P., Schluepmann, H., Wong, G.K.-S., Pryer, K.M.(2018) Fern genomes elucidate land plant evolution and cyanobacterial symbioses. Nature Plants 4, 460-472.
(41) Cova, M., López-Gutiérrez, B., Artigas-Jerónimo, S., González-Díaz, A., Bandini, G., Maere, S., Carretero-Paulet, L. *, Izquierdo, L. * (2018) The Apicomplexa-specific glucosamine-6-phosphate N-acetyltransferase gene family encodes a key enzyme for glycoconjugate synthesis with potential as therapeutic target. Scientific Reports 8: 4005.
(40) Gallone, B., Mertens, S., Gordon, J.L., Maere, S., Verstrepen, K.J. *, Steensels, J. * (2018) Origins, evolution, domestication and diversity of Saccharomyces beer yeasts. Curr Opin Biotechnol. 49, 148-155.
(39) Nelissen, H., Sun, X.H., Rymen, B., Jikumaru, Y., Kojima, M., Takebayashi, Y., Abbeloos, R., Demuynck, K., Storme, V., Vuylsteke, M., De Block, J., Herman, D., Coppens, F., Maere, S., Kamiya, Y., Sakakibara, H., Beemster, G.T.S., Inzé, D. (2018) The reduction in maize leaf growth under mild drought affects the transition between cell division and cell expansion and cannot be restored by elevated gibberellic acid levels. Plant Biotechnol J. 16: 615-27.
(38) Tasdighian, S., Van Bel, M., Li, Z., Van de Peer, Y., Carretero-Paulet, L., Maere S. (2017) Reciprocally retained genes in the angiosperm lineage show the hallmarks of dosage balance sensitivity. Plant Cell 29: 2766-85.
(37) Gordon, J.L., Gallone, B., Maere, S., Verstrepen, K.J. (2017) Evolutionary context improves regulatory network predictions. Cell Syst. 4: 478-9.
(36) Ruelens, P., Zhang, Z., van Mourik, H., Maere, S., Kaufmann, K., Geuten, K. (2017) The origin of floral organ identity quartets. Plant Cell 29: 229-42.
(35) Clauw, P., Coppens, F., Korte, A., Herman, D., Slabbinck, B., Dhondt, S., Van Daele, T., De Milde, L., Vermeersch, M., Maleux, K., Maere, S., Gonzalez, N.* and Inzé, D.* (2016) Leaf growth response to mild drought: natural variation in Arabidopsis sheds light on trait architecture. Plant Cell 28:2417-34.
(34) Gallone, B. *, Steensels, J. *, Prahl, T., Soriaga, L., Saels, V., Herrera-Malaver, B., Merlevede, A., Roncoroni, M., Voordeckers, K., Miraglia, L., Teiling, C., Steffy, B., Taylor, M., Schwartz, A., Richardson, T., White, C., Baele, G., Maere, S. *, Verstrepen, K.J. * (2016) Domestication and divergence of Saccharomyces cerevisiae beer yeasts. Cell 166:1397-1410.
(33) Baute, J., Herman, D., Coppens, F., De Block, J., Slabbinck, B., Dell'Aqcua, M., Pè, M.E., Maere, S., Nelissen, H., Inzé, D. (2016) Combined large-scale phenotyping and transcriptomics in maize reveals a robust growth regulatory network. Plant Physiol. 170:1848-67.
(32) Li, Z. *, Defoort, J. *, Tasdighian, S., Maere, S., Van de Peer, Y., De Smet, R. (2016)
Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell 28:326-44.
(31) Chen, Q., Liu, Y., Maere, S., Lee, E., Van Isterdael, G., Xie, Z., Xuan, W., Lucas, J., Vassileva, V., Kitakura, S., Marhavy, P., Wabnik, K., Geldner, N., Benková, E., Le, J., Fukaki, H., Grotewold, E., Li, C., Friml, J., Sack, F., Beeckman, T., Vanneste, S. (2015)
A coherent transcriptional feed-forward motif model for mediating auxin-sensitive PIN3 expression during lateral root development. Nat. Commun. 18: 8821.
(30) Olvera-Carrillo, Y., Van Bel, M., Van Hautegem, T., Fendrych, M., Huysmans, M., Simaskova, M., van Durme, M., Buscaill, P., Rivas, S., Sánchez-Coll, N., Coppens, F., Maere, S., Nowack, M.K. (2015) A conserved core of PCD indicator genes discriminates developmentally and environmentally induced programmed cell death in plants. Plant Physiol. 169:2684-99.
(29) Baute, J., Herman, D., Coppens, F., De Block, J., Slabbinck, B., Dell'Acqua, M., Pè, E., Maere, S., Nelissen, H., Inzé, D. (2015) Correlation analysis of the transcriptome of growing leaves with mature leaf parameters in a maize RIL population. Genome Biol. 16:168.
(28) Vanneste, K., Baele, G., Maere, S. *, Van de Peer, Y. * (2014) Analysis of 41 plant genomes supports a wave of successful genome duplications at the Cretaceous-Tertiary boundary. Genome Res. 24:1334-47.
(27) Vanneste, K., Maere, S., Van de Peer, Y. (2014) Tangled up in two: A burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Phil Trans R Soc B 369: 20130353
(26) Gutiérrez, J., Maere, S. (2014) Modeling the evolution of molecular systems from a mechanistic perspective. Trends Plant Sci. 19:292-303.
(25) Maere, S. (2014) Interview with Steven Maere. Trends Plant Sci. 19(5):276-7.
(24) Gadeyne, A., Sánchez-Rodríguez, C., Vanneste, S., Di Rubbo, S., Zauber, H., Vanneste, K., Van Leene, J., De Winne, N., Eeckhout, D., Persiau, G., Van De Slijke, E., Cannoot, B., Vercruysse, L., Mayers, J.R., Adamowski, M., Kania, U., Ehrlich, M., Schweighofer, A., Ketelaar, T., Maere, S., Bednarek, S.Y., Friml, J., Gevaert, K., Witters, E., Russinova, E., Persson, S., De Jaeger, G., Van Damme, D. (2014) The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 156:691-704.
(23) Bhosale, R.*, Jewell, J.B.*, Hollunder, J., Koo, A.J.K., Vuylsteke, M., Michoel, T., Hilson, P., Goossens, A., Howe, G.A., Browse, J., Maere, S. (2013) Predicting gene function from uncontrolled expression variation among individual wild-type Arabidopsis plants. Plant Cell 25:2865-77.
(22) De Smet, R., Adams, K.L., Vandepoele, K., Van Montagu, M.C., Maere, S., Van de Peer, Y. (2013) Convergent gene loss following gene and genome duplications creates single-copy families in flowering plants. Proc. Natl. Acad. Sci. U. S. A. 110:2898-903.
(21) Vanneste, K., Van de Peer, Y., Maere, S. (2013) Inference of genome duplications from age distributions revisited. Mol. Biol. Evol. 30:177-90.
(20) Fawcett, J., Van de Peer, Y., Maere, S. (2013) Significance and biological consequences of polyploidization in land plant evolution. In: Plant Genome Diversity, Volume 2, Greilhuber, J., Dolezel, J., Leitch, I. and Wendel, J. (eds) Springer-Verlag (Vienna)
(19) Voordeckers, K.*, Brown, C.A.*, Vanneste, K., van der Zande, E., Voet, A., Maere, S.*, Verstrepen, K.J.* (2012) Reconstruction of ancestral metabolic enzymes reveals molecular mechanisms underlying evolutionary innovation through gene duplication. PLoS Biol. 10:e1001446.
(18) Vekemans, D., Proost, S., Vanneste, K., Coenen, H., Viaene, T., Ruelens, P., Maere, S., Van de Peer, Y., Geuten, K. (2012) Gamma paleohexaploidy in the stem-lineage of core eudicots: significance for MADS-box gene and species diversification. Mol. Biol. Evol. 29:3793-806.
(17) Vandesteene, L., Lopez-Galvis, L., Vanneste, K., Feil, R., Maere, S., Lammens, W., Rolland, F., Lunn, J.E., Avonce, N., Beeckman, T., Van Dijck, P. (2012) Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis thaliana. Plant Physiol. 160:884-96.
(16) Smoot, M., Ono, K., Ideker, T., Maere, S. (2011) PiNGO: a Cytoscape plugin to find candidate genes in biological networks. Bioinformatics 27:1030-1.
(15) Van Leene, J., Hollunder, J., Eeckhout, D., Persiau, G., Van De Slijke, E., Stals, H., Van Isterdael, G., Verkest, A., Neirynck, S., Buffel, Y., De Bodt, S., Maere, S., Laukens, K., Pharazyn, A., Ferreira, P.C., Eloy, N., Renne, C., Meyer, C., Faure, J.D., Steinbrenner, J., Beynon, J., Larkin, J.C., Van de Peer, Y., Hilson, P., Kuiper, M., De Veylder, L., Van Onckelen, H., Inzé, D., Witters, E., De Jaeger, G. (2010) Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 10:397.
(14) Van de Peer, Y., Maere, S., Meyer, A. (2010) 2R or not 2R is not the question anymore. Nat Rev Genet doi:10.1038/nrg2600-c2 (Correspondence on Nat. Rev. Genet. 10:725-32)
(13) Maere, S., Van de Peer, Y. (2010) Duplicate retention after small‐ and large‐scale duplications. In: Evolution after gene duplication, Liberles, D.A. and Dittmar, K., eds., Wiley (New York)
(12) Van de Peer, Y., Maere, S., Meyer, A. (2009) The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10:725-32.
(11) Baele, G., Bredeche, N., Haasdijk, E., Maere, S., Michiels, N., Van de Peer, Y., Schmickl, T., Schwarzer, C., Thenius, R. (2009) Open-ended on-board evolutionary robotics for robot swarms. Proceedings of the 2009 IEEE Congress On Evolutionary Computation (CEC 2009), 1123-30.
(10) * Fawcett, J., * Maere, S., Van de Peer, Y. (2009) Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. U. S. A. 106, 5737-42.
(9) Maere, S., Van Dijck, P., Kuiper, M. (2008) Extracting expression modules from perturbational gene expression compendia. BMC Syst. Biol. 2:33.
(8) * Michoel, T., * Maere, S., Bonnet, E., Joshi, A., Saeys, Y., Van den Bulcke, T., Van Leemput, K., van Remortel, P., Kuiper, M., Marchal, K., Van de Peer, Y. (2007) Validating module networks learning algorithms using simulated data. BMC Bioinformatics 8, S5.
(7) Fleury, D., Himanen, K., Cnops, G., Nelissen, B., Boccardi, T.M., Maere, S., Beemster, G.T.S., Neyt, P., Anami, S., Robles, P., Micol, J.S., Inzé, D., Van Lijsebettens, M. (2007) The Arabidopsis thaliana homolog of yeast BRE1 has a function in cell cycle regulation during early leaf and root growth. Plant Cell 19, 417-32.
(6) Cline, M.S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., Gross, B., Hanspers, K., Isserlin, R., Kelley, R., Killcoyne, S., Lotia, S., Maere, S., Morris, J., Ono, K., Pavlovic, V., Pico, A.R., Vailaya, A., Wang, X., Adler, A., Conklin, B.R., Hood, L., Kuiper, M., Sander, C., Schmulevich, I., Schwikowski, B., Warner, G.J., Ideker, T., Bader, G.D. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366 - 2382.
(5) Casneuf, T., De Bodt, S., Raes, J., Maere, S., Van de Peer, Y. (2006) Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana. Genome Biol. 7, R13.
(4) Blomme, T., Vandepoele, K., De Bodt, S., Simillion, C., Maere, S., Van de Peer, Y. (2006) The gain and loss of genes during 600 million years of vertebrate evolution. Genome Biol. 7, R43.
(3) * De Bodt, S., * Maere, S., Van de Peer, Y. (2005) Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 20, 591-7.
(2) Maere, S., Heymans, K., Kuiper, M. (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in biological networks. Bioinformatics 21, 3448-9.
(1) * Maere, S., * De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., Van de Peer, Y. (2005) Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. U. S. A. 102, 5454-9.
Profiling individual field-grown plants to reverse engineer plant systems and crosstalk between stress pathways
To develop crops with enhanced yield and tolerance to field stress conditions, we need to fundamentally change our approach to studying stress response pathways in plants. Most stress studies performed under controlled laboratory conditions are of limited predictive value for phenotypes in the field. In lab conditions, stress responses are usually studied in isolation, whereas in the open environment a multitude of stresses operate in synergistic and antagonistic interaction to modulate plant phenotypes. To get a view on the complex interactions between plant stress response pathways and their effect on yield phenotypes, we aim to harness natural gene expression and phenotype variation among genetically identical field-grown plants, based on the premise that each individual plant is subject to subtle deviations of several micro-environmental factors from the field average. We are currently developing methods to use individual plant datasets for reverse engineering stress response pathways, their interaction and their impact on yield-related phenotypes, focusing on maize and rapeseed as model crops.
Modeling the evolution of transcriptional systems in silico
For the past few decades, the field of molecular evolution has largely focused on the evolution of individual gene families and overall genome structure. Analogous to the transition from reductionist to system-scale approaches in molecular biology, the logical next step in molecular evolution research is to study the evolution of genes in the context of the systems in which they function. One way to study how systems of interacting components evolve is to simulate the evolution of suitably abstracted system models in silico. Given recent developments in the field of high-performance computing, it is now possible to simulate the evolution of molecular systems at an unprecedented level of mechanistic detail. We use mathematical models to map the genotype of artificial transcriptional regulatory systems to their expression phenotype. We then use these models in population-scale evolutionary simulations to investigate how transcriptional systems evolve. One of our major research interests is to study how duplicated transcriptional systems diverge. We are particularly interested in unraveling the mechanisms by which dosage-balance constraints on duplicated transcription factors can be resolved over evolutionary time. Many regulatory genes do not duplicate easily on their own, because duplication upsets their dosage balance with other transcription factors or targets. Whole-genome duplication (WGD) on the other hand is thought to preserve dosage balance, and moreover to lead to selective retention of dosage-balance sensitive genes, since their loss after WGD would create a reverse dosage balance effect. As a consequence, post-WGD organisms are endowed with a 'regulatory spandrel’, a collection of regulatory genes that may not immediately add extra functionality but that cannot be purged easily from the genome. It is thought that under the right circumstances, these non-adaptively preserved genes may be co-opted for adaptive innovations, but this requires that the dosage-balance constraints be lifted, and it is currently not clear how this is accomplished.