Gene regulatory network analysis of silver birch reveals the ancestral state of secondary cell wall biosynthesis in core eudicots

Author:

Ilievska Maja1ORCID,Chong Sun‐Li23ORCID,Lim Kean‐Jin3ORCID,Immanen Juha14ORCID,Nieminen Kaisa14ORCID,Maaheimo Hannu5ORCID,Helariutta Yrjö16ORCID,Wurman‐Rodrich Joel7ORCID,Dupree Paul7ORCID,Ord James1ORCID,Tenkanen Maija2ORCID,Salojärvi Jarkko189ORCID

Affiliation:

1. Faculty of Biological and Environmental Sciences, Organismal and Evolutionary Biology Research Programme and Viikki Plant Science Centre University of Helsinki Helsinki FI‐00014 Finland

2. Department of Food and Nutrition University of Helsinki Helsinki FI‐00014 Finland

3. State Key Laboratory of Subtropical Silviculture, College of Forestry and Biotechnology Zhejiang A&F University Hangzhou 311300 China

4. Natural Resources Institute Finland (Luke) Helsinki FI‐00791 Finland

5. VTT Technical Research Centre PO Box 1000 Espoo FI‐02044 Finland

6. Sainsbury Laboratory University of Cambridge Cambridge CB2 1LR UK

7. Department of Biochemistry University of Cambridge Cambridge CB2 1QW UK

8. School of Biological Sciences Nanyang Technological University Singapore 637551 Singapore

9. Singapore Centre for Environmental Life Sciences Engineering Nanyang Technological University Singapore 637551 Singapore

Abstract

Summary The compact genome and lack of recent whole‐genome multiplication (WGM) events make the boreal pioneer tree silver birch (Betula pendula) a promising model for primary and secondary cell wall (PCW and SCW) regulation in forest trees. Here, we constructed regulatory networks through combined co‐expression and promoter motif analysis and carried out a tissue‐wide analysis of xylan using mass spectrometry. Analyses confirm the evolutionarily conserved model of superimposed layers of regulation and suggest a relatively simple ancestral state still retained in birch. Multispecies network analysis, including birch, poplar, and eucalyptus, identified conserved regulatory interactions, highlighting lignin biosynthesis as least conserved. The SCW biosynthesis co‐expression module was enriched with WGM duplicates. While regulator genes were under positive selection, others evolved under relaxed purifying selection, possibly linked with diversification, as indicated by expression and regulatory motif differences. Xylan composition varied between PCW and SCW, revealing unique acetylation patterns. PCW xylan biosynthesis genes showed distinct expression and regulatory motifs, with a novel acetyl transferase potentially involved. This work highlights birch as a valuable model for understanding wood formation, vascular development, and cell wall composition in eudicots.

Funder

Helsingin Yliopisto

Biotieteiden ja Ympäristön Tutkimuksen Toimikunta

Ympäristö-, elintarvike- ja biotieteellinen tutkijakoulu, Helsingin Yliopisto

Publisher

Wiley

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