The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots

Riccardo Fusi; Sara Giulia Milner; Serena Rosignoli; Riccardo Bovina; Cristovão De Jesus Vieira Teixeira; Haoyu Lou; Brian S. Atkinson; Aditi N. Borkar; Larry M. York; Dylan H. Jones; Craig J. Sturrock; Nils Stein; Martin Mascher; Roberto Tuberosa; Devin O'Connor; Malcolm J. Bennett; Anthony Bishopp; Silvio Salvi; Rahul Bhosale

doi:10.1111/nph.19777

The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots

Riccardo Fusi, Sara Giulia Milner, Serena Rosignoli, Riccardo Bovina, Cristovão De Jesus Vieira Teixeira, Haoyu Lou, Brian S. Atkinson, Aditi N. Borkar, Larry M. York, Dylan H. Jones, Craig J. Sturrock, Nils Stein, Martin Mascher, Roberto Tuberosa, Devin O'Connor, Malcolm J. Bennett, Anthony Bishopp, Silvio Salvi, Rahul Bhosale

Molecular and Cellular Imaging

Research output: Contribution to journal › Article › peer-review

Abstract

Barley (Hordeum vulgare) is an important global cereal crop and a model in genetic studies. Despite advances in characterising barley genomic resources, few mutant studies have identified genes controlling root architecture and anatomy, which plays a critical role in capturing soil resources. Our phenotypic screening of a TILLING mutant collection identified line TM5992 exhibiting a short-root phenotype compared with wild-type (WT) Morex background. Outcrossing TM5992 with barley variety Proctor and subsequent SNP array-based bulk segregant analysis, fine mapped the mutation to a cM scale. Exome sequencing pinpointed a mutation in the candidate gene HvPIN1a, further confirming this by analysing independent mutant alleles. Detailed analysis of root growth and anatomy in Hvpin1a mutant alleles exhibited a slower growth rate, shorter apical meristem and striking vascular patterning defects compared to WT. Expression and mutant analyses of PIN1 members in the closely related cereal brachypodium (Brachypodium distachyon) revealed that BdPIN1a and BdPIN1b were redundantly expressed in root vascular tissues but only Bdpin1a mutant allele displayed root vascular defects similar to Hvpin1a. We conclude that barley PIN1 genes have sub-functionalised in cereals, compared to Arabidopsis (Arabidopsis thaliana), where PIN1a sequences control root vascular patterning.

Original language	English
Pages (from-to)	104-115
Number of pages	12
Journal	New Phytologist
Volume	244
Issue number	1
DOIs	https://doi.org/10.1111/nph.19777
State	Published - Oct 2024

Funding

We acknowledge the technical support of Simona Corneti, Anne Fiebig, Sandra Stefanelli. RF acknowledges the Hounsfield Facility Center at the University of Nottingham for all the support provided for this work. The Hounsfield Facility received funding from European Research Council (Futureroots Project, Grant agreement ID: 294729), Biotechnology and Biological Sciences Research Council of the United Kingdom and The Wolfson Foundation. HL was supported by a joint University of Adelaide\u2009\u2013\u2009University of Nottingham PhD scholarship. This manuscript has been authored in part by LMY at UT\u2010Battelle, LLC, under contract DE\u2010AC05\u201000OR22725 with the US Department of Energy (DOE). The publisher acknowledges the US government licence to provide public access under the DOE Public Access Plan ( http://energy.gov/downloads/doe-public-access\u2010plan ). R. Bhosale acknowledges support from BBSRC Discovery Fellowship (BB/S011102/1), BBSRC New Investigator grant (BB/X014843/1), and BBSRC\u2010funded Delivering Sustainable Wheat (DSW) Partner Grant (BB/X018806/1).

Funders	Funder number
Biotechnology and Biological Sciences Research Council of the United Kingdom and The Wolfson Foundation
BBSRC‐funded Delivering Sustainable Wheat
U.S. Department of Energy
Hounsfield Facility Center at the University of Nottingham
joint University of Adelaide – University of Nottingham	DE‐AC05‐00OR22725
European Research Council	294729
European Research Council
Biotechnology and Biological Sciences Research Council	BB/S011102/1, BB/X014843/1
Biotechnology and Biological Sciences Research Council
DSW	BB/X018806/1

Keywords

PIN1
auxin efflux carrier
barley
root
vascular development

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10.1111/nph.19777

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Fusi, R., Milner, S. G., Rosignoli, S., Bovina, R., De Jesus Vieira Teixeira, C., Lou, H., Atkinson, B. S., Borkar, A. N., York, L. M., Jones, D. H., Sturrock, C. J., Stein, N., Mascher, M., Tuberosa, R., O'Connor, D., Bennett, M. J., Bishopp, A., Salvi, S., & Bhosale, R. (2024). The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots. New Phytologist, 244(1), 104-115. https://doi.org/10.1111/nph.19777

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title = "The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots",

abstract = "Barley (Hordeum vulgare) is an important global cereal crop and a model in genetic studies. Despite advances in characterising barley genomic resources, few mutant studies have identified genes controlling root architecture and anatomy, which plays a critical role in capturing soil resources. Our phenotypic screening of a TILLING mutant collection identified line TM5992 exhibiting a short-root phenotype compared with wild-type (WT) Morex background. Outcrossing TM5992 with barley variety Proctor and subsequent SNP array-based bulk segregant analysis, fine mapped the mutation to a cM scale. Exome sequencing pinpointed a mutation in the candidate gene HvPIN1a, further confirming this by analysing independent mutant alleles. Detailed analysis of root growth and anatomy in Hvpin1a mutant alleles exhibited a slower growth rate, shorter apical meristem and striking vascular patterning defects compared to WT. Expression and mutant analyses of PIN1 members in the closely related cereal brachypodium (Brachypodium distachyon) revealed that BdPIN1a and BdPIN1b were redundantly expressed in root vascular tissues but only Bdpin1a mutant allele displayed root vascular defects similar to Hvpin1a. We conclude that barley PIN1 genes have sub-functionalised in cereals, compared to Arabidopsis (Arabidopsis thaliana), where PIN1a sequences control root vascular patterning.",

keywords = "PIN1, auxin efflux carrier, barley, root, vascular development",

author = "Riccardo Fusi and Milner, {Sara Giulia} and Serena Rosignoli and Riccardo Bovina and {De Jesus Vieira Teixeira}, Cristov{\~a}o and Haoyu Lou and Atkinson, {Brian S.} and Borkar, {Aditi N.} and York, {Larry M.} and Jones, {Dylan H.} and Sturrock, {Craig J.} and Nils Stein and Martin Mascher and Roberto Tuberosa and Devin O'Connor and Bennett, {Malcolm J.} and Anthony Bishopp and Silvio Salvi and Rahul Bhosale",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s). New Phytologist {\textcopyright} 2024 New Phytologist Foundation.",

year = "2024",

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doi = "10.1111/nph.19777",

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Fusi, R, Milner, SG, Rosignoli, S, Bovina, R, De Jesus Vieira Teixeira, C, Lou, H, Atkinson, BS, Borkar, AN, York, LM, Jones, DH, Sturrock, CJ, Stein, N, Mascher, M, Tuberosa, R, O'Connor, D, Bennett, MJ, Bishopp, A, Salvi, S & Bhosale, R 2024, 'The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots', New Phytologist, vol. 244, no. 1, pp. 104-115. https://doi.org/10.1111/nph.19777

TY - JOUR

T1 - The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots

AU - Fusi, Riccardo

AU - Milner, Sara Giulia

AU - Rosignoli, Serena

AU - Bovina, Riccardo

AU - De Jesus Vieira Teixeira, Cristovão

AU - Lou, Haoyu

AU - Atkinson, Brian S.

AU - Borkar, Aditi N.

AU - York, Larry M.

AU - Jones, Dylan H.

AU - Sturrock, Craig J.

AU - Stein, Nils

AU - Mascher, Martin

AU - Tuberosa, Roberto

AU - O'Connor, Devin

AU - Bennett, Malcolm J.

AU - Bishopp, Anthony

AU - Salvi, Silvio

AU - Bhosale, Rahul

PY - 2024/10

Y1 - 2024/10

N2 - Barley (Hordeum vulgare) is an important global cereal crop and a model in genetic studies. Despite advances in characterising barley genomic resources, few mutant studies have identified genes controlling root architecture and anatomy, which plays a critical role in capturing soil resources. Our phenotypic screening of a TILLING mutant collection identified line TM5992 exhibiting a short-root phenotype compared with wild-type (WT) Morex background. Outcrossing TM5992 with barley variety Proctor and subsequent SNP array-based bulk segregant analysis, fine mapped the mutation to a cM scale. Exome sequencing pinpointed a mutation in the candidate gene HvPIN1a, further confirming this by analysing independent mutant alleles. Detailed analysis of root growth and anatomy in Hvpin1a mutant alleles exhibited a slower growth rate, shorter apical meristem and striking vascular patterning defects compared to WT. Expression and mutant analyses of PIN1 members in the closely related cereal brachypodium (Brachypodium distachyon) revealed that BdPIN1a and BdPIN1b were redundantly expressed in root vascular tissues but only Bdpin1a mutant allele displayed root vascular defects similar to Hvpin1a. We conclude that barley PIN1 genes have sub-functionalised in cereals, compared to Arabidopsis (Arabidopsis thaliana), where PIN1a sequences control root vascular patterning.

AB - Barley (Hordeum vulgare) is an important global cereal crop and a model in genetic studies. Despite advances in characterising barley genomic resources, few mutant studies have identified genes controlling root architecture and anatomy, which plays a critical role in capturing soil resources. Our phenotypic screening of a TILLING mutant collection identified line TM5992 exhibiting a short-root phenotype compared with wild-type (WT) Morex background. Outcrossing TM5992 with barley variety Proctor and subsequent SNP array-based bulk segregant analysis, fine mapped the mutation to a cM scale. Exome sequencing pinpointed a mutation in the candidate gene HvPIN1a, further confirming this by analysing independent mutant alleles. Detailed analysis of root growth and anatomy in Hvpin1a mutant alleles exhibited a slower growth rate, shorter apical meristem and striking vascular patterning defects compared to WT. Expression and mutant analyses of PIN1 members in the closely related cereal brachypodium (Brachypodium distachyon) revealed that BdPIN1a and BdPIN1b were redundantly expressed in root vascular tissues but only Bdpin1a mutant allele displayed root vascular defects similar to Hvpin1a. We conclude that barley PIN1 genes have sub-functionalised in cereals, compared to Arabidopsis (Arabidopsis thaliana), where PIN1a sequences control root vascular patterning.

KW - PIN1

KW - auxin efflux carrier

KW - barley

KW - root

KW - vascular development

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U2 - 10.1111/nph.19777

DO - 10.1111/nph.19777

M3 - Article

AN - SCOPUS:85191309220

SN - 0028-646X

VL - 244

SP - 104

EP - 115

JO - New Phytologist

JF - New Phytologist

IS - 1

ER -

The auxin efflux carrier PIN1a regulates vascular patterning in cereal roots

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