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

doi:10.1038/s41467-022-33300-1

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 (Lead / Corresponding author)

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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 CO ₂ 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 language	English
Article number	6050
Number of pages	18
Journal	Nature Communications
Volume	13
DOIs	https://doi.org/10.1038/s41467-022-33300-1
Publication status	Published - 13 Oct 2022

Keywords

Cell fate
Plant genetics
Stomata

ASJC Scopus subject areas

General
General Physics and Astronomy
General Chemistry
General Biochemistry,Genetics and Molecular Biology

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10.1038/s41467-022-33300-1Licence: CC BY

Final Published VersionFinal published version, 3.19 MBLicence: CC BY

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Liu, L., Jose, S. B., Campoli, C., Bayer, M. M., Sánchez-Diaz, M. A., Mcallister, T., Zhou, Y., Eskan, M., Milne, L., Schreiber, M., Batstone, T., Bull, I. D., Ramsay, L., von Wettstein-Knowles, P., Waugh, R., Hetherington, A. M., & McKim, S. M. (2022). Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley. Nature Communications, 13, Article 6050. https://doi.org/10.1038/s41467-022-33300-1

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title = "Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley",

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{\textquoteright}s distinctive epicuticular wax blooms, as well as stomatal patterning in elevated CO 2 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.",

keywords = "Cell fate, Plant genetics, Stomata",

author = "Linsan Liu and Jose, {Sarah B.} and Chiara Campoli and Bayer, {Micha M.} and S{\'a}nchez-Diaz, {Miguel A.} and Trisha Mcallister and Yichun Zhou and Mhmoud Eskan and Linda Milne and Miriam Schreiber and Thomas Batstone and Bull, {Ian D.} and Luke Ramsay and {von Wettstein-Knowles}, Penny and Robbie Waugh and Hetherington, {Alistair M.} and McKim, {Sarah M.}",

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 (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 Biological and Biotechnological Research Council with additional funding from James Hutton Limited. R.W., L.R., L.M. and M.B. were funded from the Scottish Government{\textquoteright}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. S.J. acknowledges a postgraduate studentship from the Biological and Biotechnological Research Council. 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.",

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doi = "10.1038/s41467-022-33300-1",

language = "English",

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journal = "Nature Communications",

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Liu, L, Jose, SB, Campoli, C, Bayer, MM, Sánchez-Diaz, MA, Mcallister, T, Zhou, Y, Eskan, M, Milne, L, Schreiber, M, Batstone, T, Bull, ID, Ramsay, L, von Wettstein-Knowles, P, Waugh, R, Hetherington, AM & McKim, SM 2022, 'Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley', Nature Communications, vol. 13, 6050. https://doi.org/10.1038/s41467-022-33300-1

TY - JOUR

T1 - Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley

AU - Liu, Linsan

AU - Jose, Sarah B.

AU - Campoli, Chiara

AU - Bayer, Micha M.

AU - Sánchez-Diaz, Miguel A.

AU - Mcallister, Trisha

AU - Zhou, Yichun

AU - Eskan, Mhmoud

AU - Milne, Linda

AU - Schreiber, Miriam

AU - Batstone, Thomas

AU - Bull, Ian D.

AU - Ramsay, Luke

AU - von Wettstein-Knowles, Penny

AU - Waugh, Robbie

AU - Hetherington, Alistair M.

AU - McKim, Sarah M.

N1 - 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 (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 Biological and Biotechnological Research Council 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. S.J. acknowledges a postgraduate studentship from the Biological and Biotechnological Research Council. 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.

PY - 2022/10/13

Y1 - 2022/10/13

N2 - 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 CO 2 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.

AB - 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 CO 2 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.

KW - Cell fate

KW - Plant genetics

KW - Stomata

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U2 - 10.1038/s41467-022-33300-1

DO - 10.1038/s41467-022-33300-1

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SN - 2041-1723

VL - 13

JO - Nature Communications

JF - Nature Communications

M1 - 6050

ER -

Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

16 ERA-CAPS Barley Yield Associated Networks (Joint with IPK Gatersleben as lead and University of Minnesota)

Mechanisms Underlying Variation in Barley Hull Adhesion

Genetic networks controlling cuticle specialisations in barley

Cite this

Conserved signalling components coordinate epidermal patterning and cuticle deposition in barley

Abstract

Keywords

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Projects

16 ERA-CAPS Barley Yield Associated Networks (Joint with IPK Gatersleben as lead and University of Minnesota)

Mechanisms Underlying Variation in Barley Hull Adhesion

Student theses

Genetic networks controlling cuticle specialisations in barley

Cite this