Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley

Linsan Liu, Sarah B. Jose, Chiara Campoli, Micha M. Bayer, Miguel A. Sánchez-Diaz, Trisha McAllister, Yichun Zhou, Mhmoud Eskan, Linda Milne, Miriam Schreiber, Thomas Batstone, Ian D. Bull, Luke Ramsay, Penny von Wettstein-Knowles, Robbie Waugh, Alistair M. Hetherington, Sarah M. McKim*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

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Abstract

Faced with terrestrial threats, land plants seal their aerial surfaces with a lipid-rich cuticle. To breathe, plants interrupt their cuticles with adjustable epidermal pores, called stomata, that regulate gas exchange, and develop other specialised epidermal cells such as defensive hairs. Mechanisms coordinating epidermal features remain poorly understood. Addressing this, we studied two loci whose allelic variation causes both cuticular wax-deficiency and misarranged stomata in barley, identifying the underlying genes, Cer-g/ HvYDA1, encoding a YODA-like (YDA) MAPKKK, and Cer-s/ HvBRX-Solo, encoding a single BREVIS-RADIX (BRX) domain protein. Both genes control cuticular integrity, the spacing and identity of epidermal cells, and barley’s distinctive epicuticular wax blooms, as well as stomatal patterning in elevated CO2 conditions. Genetic analyses revealed epistatic and modifying relationships between HvYDA1 and HvBRX-Solo, intimating that their products participate in interacting pathway(s) linking epidermal patterning with cuticular properties in barley. This may represent a mechanism for coordinating multiple adaptive features of the land plant epidermis in a cultivated cereal.

Original languageEnglish
Article number6050
Number of pages18
JournalNature Communications
Volume13
Issue number1
Early online date13 Oct 2022
DOIs
Publication statusE-pub ahead of print - 13 Oct 2022

Bibliographical note

Funding Information:
We are greatly indebted to Dr. Sandy Hetherington (University of Edinburgh) for advice on phylogenetic analyses and land plant evolution, as well as to Drs Joanne Russell and Ian K Dawson for guidance on genetic variation analyses. S.M. and C.C. acknowledge funding from the Biological and Biotechnological Research Council (BBSRC, BB/R010315/1). M.S-D acknowledges support by the ERASMUS+ programme and his home university, Hogeschool van Arnhem en Nijmegen. L.L. was supported by the China Scholarship Council and the University of Dundee. T.M. was supported by a Carnegie-Cant-Morgan PhD Scholarship and the University of Dundee. S.J. acknowledges a CASE postgraduate studentship from the BBSRC with additional funding from James Hutton Limited. R.W., L.R., L.M. and M.B. were funded from the Scottish Government’s Rural and Environment Science and Analytical Services Division Theme 2 Work Program 2.1. M.S. is funded by BBSRC ERA-CAPS BB/S004610/1. A.H. is grateful for support from the Leverhulme Trust (RPG-2019-004). The NERC is thanked for partial funding of the mass spectrometry facilities at Bristol (R8/H10/63). The authors acknowledge the Research/Scientific Computing teams at The James Hutton Institute and NIAB for providing computational resources and technical support for the "UK’s Crop Diversity Bioinformatics HPC" (BBSRC grant BB/S019669/1), use of which has contributed to the results reported within this paper.

Funding Information:
We are greatly indebted to Dr. Sandy Hetherington (University of Edinburgh) for advice on phylogenetic analyses and land plant evolution, as well as to Drs Joanne Russell and Ian K Dawson for guidance on genetic variation analyses. S.M. and C.C. acknowledge funding from the Biological and Biotechnological Research Council (BBSRC, BB/R010315/1). M.S-D acknowledges support by the ERASMUS+ programme and his home university, Hogeschool van Arnhem en Nijmegen. L.L. was supported by the China Scholarship Council and the University of Dundee. T.M. was supported by a Carnegie-Cant-Morgan PhD Scholarship and the University of Dundee. S.J. acknowledges a CASE postgraduate studentship from the BBSRC with additional funding from James Hutton Limited. R.W., L.R., L.M. and M.B. were funded from the Scottish Government’s Rural and Environment Science and Analytical Services Division Theme 2 Work Program 2.1. M.S. is funded by BBSRC ERA-CAPS BB/S004610/1. A.H. is grateful for support from the Leverhulme Trust (RPG-2019-004). The NERC is thanked for partial funding of the mass spectrometry facilities at Bristol (R8/H10/63). The authors acknowledge the Research/Scientific Computing teams at The James Hutton Institute and NIAB for providing computational resources and technical support for the "UK’s Crop Diversity Bioinformatics HPC" (BBSRC grant BB/S019669/1), use of which has contributed to the results reported within this paper.

Publisher Copyright:
© 2022, The Author(s).

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