A non‐canonical function of Arabidopsis ERECTA proteins and a role of the SWI3B subunit of the SWI/SNF chromatin remodeling complex in gibberellin signaling

Author:

Sarnowska Elzbieta1,Kubala Szymon2,Cwiek Pawel2,Sacharowski Sebastian2ORCID,Oksinska Paulina2,Steciuk Jaroslaw2,Zaborowska Magdalena2,Szurmak Jakub M.2,Dubianski Roman1,Maassen Anna2,Stachowiak Malgorzata1,Huettel Bruno3,Ciesla Monika2,Nowicka Klaudia2,Rolicka Anna T.24,Alseekh Saleh56ORCID,Bucior Ernest2,Franzen Rainer7,Skoneczna Anna2,Domagalska Malgorzata A.7,Amar Samija7,Hajirezaei Mohammad‐Reza8,Siedlecki Janusz A.1,Fernie Alisdair R.56ORCID,Davis Seth J.7910,Sarnowski Tomasz J.27ORCID

Affiliation:

1. Maria Sklodowska‐Curie National Research Institute of Oncology Roentgena 5 Warsaw Poland

2. Institute of Biochemistry and Biophysics Polish Academy of Sciences Pawinskiego 5A Warsaw Poland

3. Max Planck Genome Centre Cologne D‐50820 Cologne Germany

4. Faculty of Biology University of Warsaw Warsaw Poland

5. Max Planck Institute of Molecular Plant Physiology 14476 Potsdam‐Golm Germany

6. Center for Plant Systems Biology and Biotechnology 4000 Plovdiv Bulgaria

7. Max‐Planck Institute for Plant Breeding Research D‐50829 Cologne Germany

8. Leibniz‐Institut für Pflanzengenetik und Kulturplfanzenforschung Corrensstraße 3 D‐06466 Seeland OT Gatersleben Germany

9. State Key Laboratory of Crop Stress Biology School of Life Sciences, Henan University 13 Kaifeng 475004 China

10. Department of Biology University of York York YO10 5DD UK

Abstract

SUMMARYThe Arabidopsis ERECTA family (ERf) of leucine‐rich repeat receptor‐like kinases (LRR‐RLKs) comprising ERECTA (ER), ERECTA‐LIKE 1 (ERL1), and ERECTA‐LIKE 2 (ERL2) controls epidermal patterning, inflorescence architecture, and stomata development and patterning. These proteins are reported to be plasma membrane associated. Here we show that the er/erl1/erl2 mutant exhibits impaired gibberellin (GA) biosynthesis and perception alongside broad transcriptional changes. The ERf kinase domains were found to localize to the nucleus where they interact with the SWI3B subunit of the SWI/SNF chromatin remodeling complex (CRCs). The er/erl1/erl2 mutant exhibits reduced SWI3B protein level and affected nucleosomal chromatin structure. Similar to swi3c and brm plants with inactivated subunits of SWI/SNF CRCs, it also does not accumulate DELLA RGA and GAI proteins. The ER kinase phosphorylates SWI3B in vitro, and the inactivation of all ERf proteins leads to the decreased phosphorylation of SWI3B protein in vivo. The identified correlation between DELLA overaccumulation and SWI3B proteasomal degradation, and the physical interaction of SWI3B with DELLA proteins indicate an important role of SWI3B‐containing SWI/SNF CRCs in gibberellin signaling. Co‐localization of ER and SWI3B on GID1 (GIBBERELLIN INSENSITIVE DWARF 1) DELLA target gene promoter regions and abolished SWI3B binding to GID1 promoters in er/erl1/erl2 plants supports the conclusion that ERf‐SWI/SNF CRC interaction is important for transcriptional control of GA receptors. Thus, the involvement of ERf proteins in the transcriptional control of gene expression, and observed similar features for human HER2 (epidermal growth family receptor member), indicate an exciting target for further studies of evolutionarily conserved non‐canonical functions of eukaryotic membrane receptors.

Funder

Biotechnology and Biological Sciences Research Council

Deutsche Forschungsgemeinschaft

Fundacja na rzecz Nauki Polskiej

Horizon 2020 Framework Programme

Ministerstwo Nauki i Szkolnictwa Wyższego

Narodowe Centrum Nauki

Publisher

Wiley

Subject

Cell Biology,Plant Science,Genetics

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