A Specialized Histone H1 Variant Is Required for Adaptive Responses to Complex Abiotic Stress and Related DNA Methylation in Arabidopsis.
Linker (H1) histones play critical roles in chromatin compaction in higher eukaryotes. They are also the most variable of the histones, with numerous nonallelic variants cooccurring in the same cell. Plants contain a distinct subclass of minor H1 variants that are induced by drought and abscisic acid and have been implicated in mediating adaptive responses to stress. However, how these variants facilitate adaptation remains poorly understood. Here, we show that the single Arabidopsis (Arabidopsis thaliana) stress-inducible variant H1.3 occurs in plants in two separate and most likely autonomous pools: a constitutive guard cell-specific pool and a facultative environmentally controlled pool localized in other tissues. Physiological and transcriptomic analyses of h1.3 null mutants demonstrate that H1.3 is required for both proper stomatal functioning under normal growth conditions and adaptive developmental responses to combined light and water deficiency. Using fluorescence recovery after photobleaching analysis, we show that H1.3 has superfast chromatin dynamics, and in contrast to the main Arabidopsis H1 variants H1.1 and H1.2, it has no stable bound fraction. The results of global occupancy studies demonstrate that, while H1.3 has the same overall binding properties as the main H1 variants, including predominant heterochromatin localization, it differs from them in its preferences for chromatin regions with epigenetic signatures of active and repressed transcription. We also show that H1.3 is required for a substantial part of DNA methylation associated with environmental stress, suggesting that the likely mechanism underlying H1.3 function may be the facilitation of chromatin accessibility by direct competition with the main H1 variants.
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Kinga
K
Rutowicz
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Marcin
M
Puzio
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Joanna
J
Halibart-Puzio
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Maciej
M
Lirski
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Maciej
M
Kotliński
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Magdalena A
MA
Kroteń
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Lukasz
L
Knizewski
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Bartosz
B
Lange
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Anna
A
Muszewska
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Katarzyna
K
Śniegowska-Świerk
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Janusz
J
Kościelniak
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Roksana
R
Iwanicka-Nowicka
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Krisztián
http://orcid.org/0000-0002-7111-6452
K
Buza
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Franciszek
http://orcid.org/0000-0002-1095-8998
F
Janowiak
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Katarzyna
http://orcid.org/0000-0002-8115-1649
K
Żmuda
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Indrek
I
Jõesaar
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Katarzyna
K
Laskowska-Kaszub
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Anna
http://orcid.org/0000-0002-5331-7840
A
Fogtman
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Hannes
H
Kollist
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Piotr
P
Zielenkiewicz
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Jerzy
J
Tiuryn
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Paweł
P
Siedlecki
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Szymon
S
Swiezewski
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Krzysztof
K
Ginalski
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Marta
M
Koblowska
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Rafał
R
Archacki
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Bartek
B
Wilczynski
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.).
Marcin
http://orcid.org/0000-0003-1071-1159
M
Rapacz
Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02-106 Warsaw, Poland (K.R., J.H.-P., M.L., M.Kot., A.M., R.I.-N., A.F., P.Z., P.S., S.S., M.Kob., A.J.);Laboratory of Systems Biology, University of Warsaw, 02-106 Warsaw, Poland (M.P., M.Kot., B.L., R.I.-N., K.L.-K., P.S., M.Kob., R.A., A.J.);Institute of Plant Physiology, University of Rzeszów, 36-100 Kolbuszowa, Poland (J.H.-P.);College of Inter-Faculty Individual Studies in Mathematics and Natural Sciences, University of Warsaw, 02-089 Warsaw, Poland (M.A.K.);Laboratory of Bioinformatics and Systems Biology, Center of New Technologies (L.K., A.M., K.G.), and Institute of Informatics (K.B., J.T., B.W.), University of Warsaw, 02-097 Warsaw, Poland;Department of Plant Physiology, University of Agriculture in Cracow, 30-239 Cracow, Poland (K.Ś.-Ś., J.K., K.Ż., M.R.);Institute of Plant Physiology, Polish Academy of Sciences, 30-239 Cracow, Poland (F.J.); andInstitute of Technology, University of Tartu, 50411 Tartu, Tartumaa, Estonia (I.J., H.K.) andyj@ibb.waw.pl.
Andrzej
http://orcid.org/0000-0002-4684-4503
A
Jerzmanowski
D000040:Abscisic Acid / Q000378:metabolism*; D000222:Adaptation, Physiological; D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development / Q000502:physiology / Q000528:radiation effects; D002843:Chromatin / Q000235:genetics / Q000378:metabolism; D019175:DNA Methylation; D055864:Droughts; D044127:Epigenesis, Genetic; D018506:Gene Expression Regulation, Plant; D017930:Genes, Reporter; D006570:Heterochromatin / Q000235:genetics / Q000378:metabolism; D006657:Histones / Q000235:genetics* / Q000378:metabolism; D008027:Light; D010937:Plant Growth Regulators / Q000378:metabolism*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D013312:Stress, Physiological
D002843:Chromatin; D006570:Heterochromatin; D006657:Histones; D010937:Plant Growth Regulators; D010940:Plant Proteins; D000040:Abscisic Acid