Remko Offringa
Professor of Plant developmental genetics
- Name
- Prof.dr. R. Offringa
- Telephone
- +31 71 527 5097
- r.offringa@biology.leidenuniv.nl
- ORCID iD
- 0000-0002-3293-5295
Prof. Dr. Remko Offringa is Professor of Plant Developmental Genetics and head of cluster Plant Sciences. His research focusses on the role of the plant hormone auxin in developmental responses to environmental signals and on plant developmental phase transitions.
More information about Remko Offringa
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Former PhD candidates
Prof. Dr. Remko Offringa is Professor of Plant Developmental Genetics at the IBL. During his PhD research, he established the use of the Agrobacterium vector system for gene targeting in plants. After his graduation, his research focus switched to the role of the plant hormone auxin in development of the model plant Arabidopsis thaliana. These investigations led to the key discovery that the polarity of the transport of auxin is determined by phosphorylation of the PIN FORMED (PIN) auxin transporters by the plant-specific protein kinase PINOID. This finding, for which Remko Offringa received the C.J. Kok award and a NWO CW TOP subsidy, formed the basis for one of the main of research topics in his lab, how environmental signals alter plant development by modulating the subcellular localisation of PIN proteins.
Meanwhile, his research interests have expanded to the role of the plant hormone auxin in plant developmental switches, such as the initiation of (somatic) embryogenesis and fruit development, and recently also to bulb propagation and ageing. Remko co-authors more than 50 peer reviewed publications in high impact journals such as Science, Nature, Cell, PNAS, and The Plant Cell (h index = 33).
He is also co-author on several book chapters and patent applications, and acts as editor for Molecular Plant. He is theme leader in the research committee of the National Graduate School Experimental Plant Sciences (EPS), and co-founder of the Leiden University spin-off company Add2X Biosciences BV.
Professor of Plant developmental genetics
- Science
- Instituut Biologie Leiden
- IBL Plant Sciences
- Chen S., Marcelis L.F.M., Offringa R., Kohlen W. & Heuvelink E. (2024), Far-red light-enhanced apical dominance stimulates flower and fruit abortion in sweet pepper, Plant Physiology 195(2): 924-939.
- Karami O., Khadem A., Rahimi A., Zagari N., Aigner S. & Offringa R. (2024), Transient efflux inhibition improves plant regeneration by natural auxins, The Plant Journal 118(2): 295-303.
- Chen S., Dalla Villa V. Kohlen W., Kusuma P., Offringa R., Marcelis L.F.M. & Heuvelink E. (2024), High ratio of blue:red light reduces fruit set in sweet pepper, which is associated with low starch content and hormonal changes, Environmental and Experimental Botany 225: 105850.
- Spaninks K., Lamers G.E.M., Lieshout J. van & Offringa R. (2023), Light quality regulates apical and primary radial growth of Arabidopsis thaliana and Solanum lycopersicum, Scientia Horticulturae 317: 112082.
- Spaninks K. & Offringa R. (2023), Local phytochrome signalling limits root growth in light by repressing auxin biosynthesis, Journal of Experimental Botany 74(15): 4642-4653.
- Karami O., Jong H. de, Somovilla V.J., Villanueava Acosta B., Sugiarta A.B., Ham M., Khadem A., Wennekes T. & Offringa R. (2023), Structure–activity relationship of 2,4‐D correlates auxinic activity with the induction of somatic embryogenesis in Arabidopsis thaliana, The Plant Journal 116(5): 1355-1369.
- Karami O., Philipsen C., Rahimi A., Nurillah A.R., Boutilier K. & Offringa R. (2023), Endogenous auxin maintains embryonic cell identity and promotes somatic embryo development in Arabidopsis, The Plant Journal 113(1): 7-22.
- Rahimi A., Karami O., Lestari A.D., Werk T. de, Amakorová P., Shi D., Novák O., Greb T. & Offringa R. (2022), Control of cambium initiation and activity in Arabidopsis by the transcriptional regulator AHL15, Current Biology 32(8): 1764-1775.e3.
- Rahimi A., Karami O., Balazadeh S. & Offringa R. (2022), miR156‐independent repression of the ageing pathway by longevity‐promoting AHL proteins in Arabidopsis, New Phytologist 235(6): 2424-2438.
- Thonglim A., Bortolami G., Delzon S., Larter M., Offringa R., Keurentjes J.J.B., Smets E., Balazadeh S. & Lens F. (2022), Drought response in Arabidopsis displays synergistic coordination between stems and leaves, Journal of Experimental Botany 74(3): 1004-1021.
- Thonglim A., Delzon S., Larter M.D., Karami O., Rahimi A., Offringa R., Keurentjes J.J.B., Balazadeh S., Smets E.F. & Lens F.P. (2021), Intervessel pit membrane thickness best explains variation in embolism resistance amongst stems of Arabidopsis thaliana accessions, Annals of Botany 128(2): 171-182.
- Glanc M., Gelderen K. van, Hoermayer L., Tan S., Naramoto S., Zhang X., Domjan D., Vcelarova L., Hauschild R., Johnson A., Koning E. de, Dop M. van, Radmacher E., Janson W., Wei X., Molnar G., Fendrych M., Rybel B. De, Ofrringa R. & Friml J. (2021), AGC kinases and MAB4/MEL proteins maintain PIN polarity by limiting lateral diffusion in plant cells, Current Biology 31(9): 1918-1930.e5.
- KaramiO., Rahimi A., Mak P., Horstman A., Boutilier K., Compier M., Zaal B. van der & Offringa R. (2021), An Arabidopsis AT-hook motif nuclear protein mediates somatic embryogenesis and coinciding genome duplication, Nature Communications 12(1): 2508.
- Miotto Y.E., da Costa C.T., Offringa R., Kleine-Vehn J. & dos Santos Maraschin F. (2021), Effects of light intensity on root development in a D-Root growth system, Frontiers in Plant Science 12: 778382.
- Zhang S., Habets M.E.J., Breuninger H., Dolan L., Offringa R. & Duijn A. van (2020), Evolutionary and functional analysis of a chara plasma membrane H+-ATPase, Frontiers in Plant Science 10: 1707.
- Karami O., Rahimi A., Khan M., Bemer M., Hazarika R.R., Makt P., Compier M., Noort V. van & Offringa R. (2020), A suppressor of axillary meristem maturation promotes longevity in flowering plants, Nature Plants 6: 368-376.
- Xiao Y. & Offringa R. (2020), PDK1 regulates auxin transport and Arabidopsis vascular development through AGC1 kinase PAX, Nature Plants 6: 544-555.
- Spaninks K., Lieshout J. van, Ieperen W. van & Offringa R. (2020), Regulation of early plant development by red and blue light: a comparative analysis between Arabidopsis thaliana and Solanum lycopersicum, Frontiers in Plant Science 11: 599982.
- Miotto Y.E., Tesser da Costa C., Oliveira B.H. de, Guzman F., Margis R., Cunha de Almeida R.M., Offringa R. & Dos Santos Maraschin F. (2019), Identification of root transcriptional responses to shoot illumination in Arabidopsis thaliana, Plant Molecular Biology 101(4-5): 487-498.
- Da Costa C.T., Offringa R. & Fett-Neto A.G. (2019), The role of auxin transporters and receptors in adventitious rooting of Arabidopsis thaliana pre-etiolated flooded seedlings, Plant Science 290: 110294.
- Da Costa C.T., Gaeta M.L., De Araujo Mariath J.E., Offringa R. & Fett-Neto A.G. (2018), Comparative adventitious root development in pre-etiolated and flooded Arabidopsis hypocotyls exposed to different auxins, Plant Physiology and Biochemistry 127: 161-168.
- Larsson E., Vivian-Smith A., Offringa R. & Sundberg E. (2017), Auxin homeostasis in Arabidopsis ovules is anther-dependent at maturation and changes dynamically upon fertilization, Frontiers in Plant Science 8: 1735.
- Boot K.J.M., Hille S.C., Libbenga K.R., Pelletier L.A., Spronsen P.C. van, Duijn A. van & Offringa R. (2016), Modelling the dynamics of polar auxin transport in inflorescence stems of Arabidopsis thaliana, Journal of Experimental Botany 67(3): 649-666.
- Li C.Y., Li J.Y., Chong K., Harter K., Lee Y., Leung J., Martinoia E., Matsuoka M., Offringa R., Qu L.J., Schroeder J. & Zhao Y.D. (2016), Toward a molecular understanding of plant hormone actions, Molecular Plant 9(1): 1-3.
- Gelderen K. van, Rongen M. van, Liu A., Otten A.V. & Offringa R. (2016), An INDEHISCENT-controlled auxin response specifies the separation layer in early Arabidopsis fruit, Molecular Plant 9: 857-869.
- Habets M.E.J. & Offringa R. (2015), Auxin Binding Protein 1: A Red Herring After All?, Molecular Plant 8(8): 1131-1134.
- Dhonukshe P., Huang F., Galvan-Ampudia C.S., Pekka Måhönen A., Kleine-Vehn J., Xu J., Quint A., Prasad K., Friml J., Scheres B. & Offringa R. (2015), Correction to Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling, Development 142: 2386-2387.
- Soriano M., Jacquard C., Angenent G.C., Krochko J., Offringa R. & Boutilier K. (2014), Plasticity in Cell Division Patterns and Auxin Transport Dependency during in Vitro Embryogenesis in Brassica napus, The Plant Cell 26(6): 2568 - 2581.
- Habets M.E.J. & Offringa R. (2014), PIN-driven polar auxin transport in pland developmental plasticity: a key target for environmental and endogenous signals, New Phytologist 203(2): 362 - 377.
- Marhavy P., Duclercq J., Weller B., Eraru E., Bielach A., Offringa R. & Friml J. (2014), Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis, Current Biology 24(9): 1031 - 1037.
- Boer P. de, Bronkhof J., Dukik K., Kerkman R., Touw H., Berg M. van den & Offringa R. (2013), Efficient gene targeting in Penicillium chrysogenum using novel Agrobacterium-mediated transformation approaches, Fungal Genetics and Biology 61: 9-14.
- Tiwari A., Vivian-Smith A., Ljung K., Offringa R. & Heuvelink E. (2013), Physiological and morphological changes during early and later stages of fruit growth in Capsicum annuum, Physiologia Plantarum 147(3): 396-406.
- Offringa R. & Huang F. (2013), Phosphorylation-dependent Trafficking of Plasma Membrane Proteins in Animal and Plant Cells, Journal of Integrative Plant Biology 55(9): 789-808.
- Offringa R. & Kleine-Vehn J. (2013), Cell Polarity and Development, Journal of Integrative Plant Biology 55(9): 786-788.
- Boot C.J.M., Libbenga K.R., Hille S.C., Offringa R. & Duijn B. van (2012), Polar auxin transport: an early invention, Journal of Experimental Botany 63(11): 4213-4218.
- Tiwari A., Offringa R. & Heuvelink E.P. (2012), Auxin-induced fruit set in Capsicum annuum L. requires downstream gibberellin biosynthesis, Journal of Plant Growth Regulation 31(4): 570-578.
- Rademacher E.H. & Offringa R. (2012), Evolutionary adaptations of plant AGC kinases: from light signaling to cell polarity regulation, Frontiers in Plant Science 3: 250.
- Huang F., Kemel Zago M., Abas L., Marion A. van, Galvan-Ampudia C.S. & Offringa R. (2010), Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport, The Plant Cell 22: 1129-1142.
- Dhonukshe P., Huang F., Galvan-Ampudia C.S., Pekka Måhönen A., Kleine-Vehn J., Xu J., Quint A., Prasad K., Friml J., Scheres B. & Offringa R. (2010), Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling, Development 137: 3245-3255.
- Boer P. de, Bastiaans J., Touw H., Kerkman R., Bronkhof J., Berg M. van den & Offringa R. (2010), Highly efficient gene targeting in Penicillium chrysogenum using the bi-partite approach in ∆lig4 or ∆ku70 mutants, Fungal Genetics and Biology 47: 839-846.
- Kleine-Vehn J., Huang F., Naramoto J., Zhang J., Offringa R., Michniewicz M. & Friml J. (2009), PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis, The Plant Cell 21(12): 3839-3849.
- Dos Santos Maraschin F., Memelink J. & Offringa R. (2009), Auxin-induced, SCFTIR1-mediated poly-ubiquitination marks AUX/IAA proteins for degradation, The Plant Journal 59(1): 100-109.
- Robert H.S., Quint A., Brand D., Vivian-Smith A. & Offringa R. (2009), BTB and TAZ domain scaffold proteins perform a crucial function in Arabidopsis development, The Plant Journal 58(1): 109-121.
- Robert H.S. & Offringa R. (2008), Regulation of auxin transport polarity by AGC kinases, Current Opinion in Plant Biology 11(5): 495-502.
- Supena E.D.J., Winarto B., Riksen T., Dubas E., Lammeren A.A. van, Offringa R., Boutilier K. & Custers J.B. (2008), Regeneration of zygotic-like microspore-derived embryos suggests an important role for the suspensor in early embryo patterning, Journal of Experimental Botany 59(4): 803-814.
- Galvan-Ampudia C.S. & Offringa R. (2007), Plant evolution: AGC kinases tell the auxin tale, Trends in Plant Science 12(12): 541-547.
- Michniewicz M., Zago M.K., Abas L., Weijers D., Schweighofer E., Meskiene I., Heisler M.G., Ohno C., Zhang J., Huang F., Schwab R., Weigel D., Meyerowitz E.M., Luschnig C., Offringa R. & Friml J. (2007), Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux, Cell 130(6): 1044-1056.
- Friml J., Benfey P., Benkova E., Bennett M., Berleth T., Geldner N., Grebe M., Heisler M., Hejatko J., Jurgens G., Laux T., Lindsey K., Lukowitz W., Luschnig C., Offringa R., Scheres B., Swarup R., Torres-Ruiz R., Weijers D. & Zazimalova E. (2006), Apical-basal polarity: why plant cells don't stand on their heads, Trends in Plant Science 11(1): 12-14.
- Weijers D., Sauer A., Meurette O., Friml J., Ljung K., Sandberg S., Hooykaas P.J.J. & Offringa R. (2005), Maintenance of embryonic auxin gradients for apical-basal patterning by PIN-FORMED-dependent auxin transport in Arabidopsis, The Plant Cell 17(9): 2517-2526.
- Paciorek M., Xiong Y., Weijers D., Offringa R. & Friml J. (2004), Role of protein phosphorylation in polar auxin transport in arabidopsis, Acta Physiologiae Plantarum 26(3): 51-51.
- Friml J., Yang X., Michniewicz M., Weijers D., Quint A., Tietz O., Benjamins R., Ouwerkerk P.B.F., Ljung K., Sandberg G., Hooykaas P.J.J., Palme K. & Offringa R. (2004), A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux, Science 306(5697): 862-865.
- Benjamins R., Galván Ampudia C.S., Hooykaas P.J.J. & Offringa R. (2003), PINOID-mediated signalling involves calcium-binding proteins, Plant Physiology 132(3): 1623-1630.
- Weijers D., Hamburg J.-P. van, Rijn E. van, Hooykaas P.J.J. & Offringa R. (2003), Diphteria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development, Plant Physiology 133(4): 1882-1892.
- Friml J., Vieten A., Sauer M., Weijers D., Schwartz H., Hamann T., Offringa R. & Jürgens G. (2003), Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis, Nature 426: 147-153.
- Boutilier K., Offringa R., Sharma V.K., Kieft H., Ouellet T., Zhang L., Hattori J., Liu C.M., Lammeren A.A. van, Miki B.L., Custers J.B. & Lookeren Campagne M. van (2002), Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth, The Plant Cell 14: 1737-1749.
- Benjamins R., Quint A., Weijers D., Hooykaas P.J.J. & Offringa R. (2001), The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport, Development 128(20): 4057-4067.
- Weijers D., Geldner N., Offringa R. & Jurgens G. (2001), Seed development - Early paternal gene activity in Arabidopsis, Nature 414(6865): 709-710.
- Weijers D., Franke-Van Dijk M., Vencken R.J., Quint A., Hooykaas P.J.J. & Offringa R. (2001), An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene, Development 128(21): 4289-4299.
- Risseeuw E., Offringa R., Franke-Van Dijk M.E.I. & Hooykaas P.J.J. (1995), Targeted recombination in plants using Agrobacterium coincides with additional rearrangements at the target locus, The Plant Journal 7(1): 109-119.
- Groot M.J.A. de, Offringa R., Groet J., Does M.P., Hooykaas P.J.J. & Elzen P.J.M. van den (1994), Non-recombinant background in gene targeting: illegitimate recombination between a hpt gene and a defective 5' deleted nptII gene can restore a Km^r phenotype in tobacco, Plant Molecular Biology 25(4): 721-733.
- Offringa R., Franke-Van Dijk M.E., Groot M.J. de, Elzen P.J. van den & Hooykaas P.J.J. (1993), Nonreciprocal homologous recombination between Agrobacterium transferred DNA and a plant chromosomal locus, Proceedings of the National Academy of Sciences 90(15): 7346-7350.
- Offringa R., Elzen P.J.M. van den & Hooykaas P.J.J. (1992), Gene targeting in plants using the Agrobacterium vector system, Transgenic Research 1: 114-123.
- Groot M.J.A., Offringa R., Does M.P., Hooykaas P.J.J. & Elzen P.J.M. van den (1992), Mechanisms of intermolecular homologous recombination in plants as studied with single- and double-stranded DNA molecules, Nucleic Acids Research 20(11): 2785-2794.
- Does M.P., Dekker B.M.M., Groot M.J.A. de & Offringa R. (1991), A quick method to estimate the T-DNA copy number in transgenic plants at an early stage after transformation, using inverse PCR, Plant Molecular Biology 17(1): 151-153.
- Offringa R., Groot M.J. de, Haagsman H.J., Does M.P., Elzen P.J. van den & Hooykaas P.J.J. (1990), Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium-mediated transformation, The EMBO Journal 9(10): 3077-3084.
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