Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism

Riccardo Fusi; Serena Rosignoli; Haoyu Lou; Giuseppe Sangiorgi; Riccardo Bovina; Jacob K. Pattem; Aditi N. Borkar; Marco Lombardi; Cristian Forestan; Sara G. Milner; Jayne L. Davis; Aneesh Lale; Gwendolyn K. Kirschner; Ranjan Swarup; Alberto Tassinari; Bipin K. Pandey; Larry M. York; Brian S. Atkinson; Craig J. Sturrock; Sacha J. Mooney; Frank Hochholdinger; Matthew R. Tucker; Axel Himmelbach; Nils Stein; Martin Mascher; Kerstin A. Nagel; Laura De Gara; James Simmonds; Cristobal Uauy; Roberto Tuberosa; Jonathan P. Lynch; Gleb E. Yakubov; Malcolm J. Bennett; Rahul Bhosale; Silvio Salvi

doi:10.1073/pnas.2201350119

Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism

Riccardo Fusi, Serena Rosignoli, Haoyu Lou, Giuseppe Sangiorgi, Riccardo Bovina, Jacob K. Pattem, Aditi N. Borkar, Marco Lombardi, Cristian Forestan, Sara G. Milner, Jayne L. Davis, Aneesh Lale, Gwendolyn K. Kirschner, Ranjan Swarup, Alberto Tassinari, Bipin K. Pandey, Larry M. York, Brian S. Atkinson, Craig J. Sturrock, Sacha J. MooneyFrank Hochholdinger, Matthew R. Tucker, Axel Himmelbach, Nils Stein, Martin Mascher, Kerstin A. Nagel, Laura De Gara, James Simmonds, Cristobal Uauy, Roberto Tuberosa, Jonathan P. Lynch, Gleb E. Yakubov, Malcolm J. Bennett, Rahul Bhosale, Silvio Salvi

Molecular and Cellular Imaging

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

29 Scopus citations

Abstract

Root angle in crops represents a key trait for efficient capture of soil resources. Root angle is determined by competing gravitropic versus antigravitropic offset (AGO) mechanisms. Here we report a root angle regulatory gene termed ENHANCED GRAVITROPISM1 (EGT1) that encodes a putative AGO component, whose loss-of-function enhances root gravitropism. Mutations in barley and wheat EGT1 genes confer a striking root phenotype, where every root class adopts a steeper growth angle. EGT1 encodes an F-box and Tubby domain-containing protein that is highly conserved across plant species. Haplotype analysis found that natural allelic variation at the barley EGT1 locus impacts root angle. Gravitropic assays indicated that Hvegt1 roots bend more rapidly than wild-type. Transcript profiling revealed Hvegt1 roots deregulate reactive oxygen species (ROS) homeostasis and cell wall-loosening enzymes and cofactors. ROS imaging shows that Hvegt1 root basal meristem and elongation zone tissues have reduced levels. Atomic force microscopy measurements detected elongating Hvegt1 root cortical cell walls are significantly less stiff than wild-type. In situ analysis identified HvEGT1 is expressed in elongating cortical and stele tissues, which are distinct from known root gravitropic perception and response tissues in the columella and epidermis, respectively. We propose that EGT1 controls root angle by regulating cell wall stiffness in elongating root cortical tissue, counteracting the gravitropic machinery’s known ability to bend the root via its outermost tissues. We conclude that root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism.

Original language	English
Article number	e2201350119
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	119
Issue number	31
DOIs	https://doi.org/10.1073/pnas.2201350119
State	Published - Aug 2 2022

Funding

We thank Simona Corneti, Anne Fiebig, Sandra Stefanelli, and Alessandro Tondelli for technical support. R.F. acknowledges ARPA-E DEEPER (US Department of Energy [DOE] ARPA-E ROOTS Award DE-AR0000821) and 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 294729), Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom, and The Wolfson Foundation. R. Bhosale thanks Future Food Beacon Nottingham Research and BBSRC Discovery Fellowship (BB/S011102/1). The rhizotron study received funding from the European Union’s Horizon 2020 research and innovation programme under Grant 731013 (EPPN2020). Work described here is supported in part by the project ‘Rooty—A root ideotype toolbox to support improved wheat yields’ funded by the IWYP Consortium (project IWYP122) via the BBSRC in the United Kingdom (BB/S012826/1). H.L. was supported by a joint University of Adelaide/University of Nottingham PhD scholarship. A.N.B. acknowledges the Anne McLaren Fellowship at University of Nottingham. B.K.P acknowledges the challenge Grant (CHG\R1\170040) and BBSRC Discovery Fellowship (BB/V00557X/1). G.E.Y. acknowledges the financial support from BBSRC Grant (BB/T006404/1). We acknowledge Francesco Loreto (National Research Council-Department of Agriculture, Biology, and Food Science, Italy) for supporting M.L.’s visit to Nottingham. This manuscript has been authored in part by L.M.Y. at UT-Battelle, LLC, under Contract DE-AC05-00OR22725 with the US DOE. The publisher acknowledges the US government license to provide public access under the DOE Public Access Plan (https://energy.gov/downloads/doe-public-access-plan). F. H. received funding from the German Research Foundation (DFG) under grant HO 2249/21-1. acknowledges the challenge Grant (CHG\R1\170040) and BBSRC Discovery Fellowship (BB/V00557X/1). G.E.Y. acknowledges the financial support from BBSRC Grant (BB/T006404/1). We acknowledge Francesco Loreto (National Research Council-Department of Agriculture, Biology, and Food Science, Italy) for supporting M.L.’s visit to Nottingham. This manuscript has been authored in part by L.M.Y. at UT-Battelle, LLC, under Contract DE-AC05-00OR22725 with the US DOE. The publisher acknowledges the US government license to provide public access under the DOE Public Access Plan (https://energy.gov/downloads/doe-public-access-plan). F. H. received funding from the German Research Foundation (DFG) under grant HO 2249/21-1. ACKNOWLEDGMENTS. We thank Simona Corneti, Anne Fiebig, Sandra Stefa-nelli, and Alessandro Tondelli for technical support. R.F. acknowledges ARPA-E DEEPER (US Department of Energy [DOE] ARPA-E ROOTS Award DE-AR0000821) and 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 294729), Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom, and The Wolfson Foundation. R. Bhosale thanks Future Food Beacon Nottingham Research and BBSRC Discovery Fellowship (BB/S011102/1). The rhizotron study received funding from the European Union’s Horizon 2020 research and innovation programme under Grant 731013 (EPPN2020). Work described here is supported in part by the project ‘Rooty—A root ideotype toolbox to support improved wheat yields’ funded by the IWYP Consortium (project IWYP122) via the BBSRC in the United Kingdom (BB/S012826/1). H.L. was supported by a joint University of Adelaide/University of Nottingham PhD scholarship. A.N.B. acknowledges the Anne McLaren Fellowship at University of Nottingham. B.K.P

Funders	Funder number
DOE Public Access Plan
Future Food Beacon Nottingham Research	BB/S011102/1
Hounsfield Facility Center at the University of Nottingham
IWYP Consortium	BB/S012826/1, IWYP122
National Research Council-Department of Agriculture
Simona Corneti
University of Adelaide/University of Nottingham
U.S. Department of Energy	DE-AR0000821
Advanced Research Projects Agency - Energy
Horizon 2020 Framework Programme	EPPN2020, 731013
Biotechnology and Biological Sciences Research Council	DE-AC05-00OR22725
European Research Council	294729
University of Nottingham	CHG\R1\170040, BB/T006404/1, BB/V00557X/1
Wolfson Foundation
Deutsche Forschungsgemeinschaft	HO 2249/21-1

Keywords

antigravitropic
barley
cell-wall
root angle
wheat

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10.1073/pnas.2201350119

Cite this

Fusi, R., Rosignoli, S., Lou, H., Sangiorgi, G., Bovina, R., Pattem, J. K., Borkar, A. N., Lombardi, M., Forestan, C., Milner, S. G., Davis, J. L., Lale, A., Kirschner, G. K., Swarup, R., Tassinari, A., Pandey, B. K., York, L. M., Atkinson, B. S., Sturrock, C. J., ... Salvi, S. (2022). Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism. Proceedings of the National Academy of Sciences of the United States of America, 119(31), Article e2201350119. https://doi.org/10.1073/pnas.2201350119

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title = "Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism",

abstract = "Root angle in crops represents a key trait for efficient capture of soil resources. Root angle is determined by competing gravitropic versus antigravitropic offset (AGO) mechanisms. Here we report a root angle regulatory gene termed ENHANCED GRAVITROPISM1 (EGT1) that encodes a putative AGO component, whose loss-of-function enhances root gravitropism. Mutations in barley and wheat EGT1 genes confer a striking root phenotype, where every root class adopts a steeper growth angle. EGT1 encodes an F-box and Tubby domain-containing protein that is highly conserved across plant species. Haplotype analysis found that natural allelic variation at the barley EGT1 locus impacts root angle. Gravitropic assays indicated that Hvegt1 roots bend more rapidly than wild-type. Transcript profiling revealed Hvegt1 roots deregulate reactive oxygen species (ROS) homeostasis and cell wall-loosening enzymes and cofactors. ROS imaging shows that Hvegt1 root basal meristem and elongation zone tissues have reduced levels. Atomic force microscopy measurements detected elongating Hvegt1 root cortical cell walls are significantly less stiff than wild-type. In situ analysis identified HvEGT1 is expressed in elongating cortical and stele tissues, which are distinct from known root gravitropic perception and response tissues in the columella and epidermis, respectively. We propose that EGT1 controls root angle by regulating cell wall stiffness in elongating root cortical tissue, counteracting the gravitropic machinery{\textquoteright}s known ability to bend the root via its outermost tissues. We conclude that root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism.",

keywords = "antigravitropic, barley, cell-wall, root angle, wheat",

author = "Riccardo Fusi and Serena Rosignoli and Haoyu Lou and Giuseppe Sangiorgi and Riccardo Bovina and Pattem, {Jacob K.} and Borkar, {Aditi N.} and Marco Lombardi and Cristian Forestan and Milner, {Sara G.} and Davis, {Jayne L.} and Aneesh Lale and Kirschner, {Gwendolyn K.} and Ranjan Swarup and Alberto Tassinari and Pandey, {Bipin K.} and York, {Larry M.} and Atkinson, {Brian S.} and Sturrock, {Craig J.} and Mooney, {Sacha J.} and Frank Hochholdinger and Tucker, {Matthew R.} and Axel Himmelbach and Nils Stein and Martin Mascher and Nagel, {Kerstin A.} and {De Gara}, Laura and James Simmonds and Cristobal Uauy and Roberto Tuberosa and Lynch, {Jonathan P.} and Yakubov, {Gleb E.} and Bennett, {Malcolm J.} and Rahul Bhosale and Silvio Salvi",

note = "Publisher Copyright: Copyright {\textcopyright} 2022 the Author(s). Published by PNAS.",

year = "2022",

month = aug,

day = "2",

doi = "10.1073/pnas.2201350119",

language = "English",

volume = "119",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "31",

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Fusi, R, Rosignoli, S, Lou, H, Sangiorgi, G, Bovina, R, Pattem, JK, Borkar, AN, Lombardi, M, Forestan, C, Milner, SG, Davis, JL, Lale, A, Kirschner, GK, Swarup, R, Tassinari, A, Pandey, BK, York, LM, Atkinson, BS, Sturrock, CJ, Mooney, SJ, Hochholdinger, F, Tucker, MR, Himmelbach, A, Stein, N, Mascher, M, Nagel, KA, De Gara, L, Simmonds, J, Uauy, C, Tuberosa, R, Lynch, JP, Yakubov, GE, Bennett, MJ, Bhosale, R & Salvi, S 2022, 'Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism', Proceedings of the National Academy of Sciences of the United States of America, vol. 119, no. 31, e2201350119. https://doi.org/10.1073/pnas.2201350119

TY - JOUR

T1 - Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism

AU - Fusi, Riccardo

AU - Rosignoli, Serena

AU - Lou, Haoyu

AU - Sangiorgi, Giuseppe

AU - Bovina, Riccardo

AU - Pattem, Jacob K.

AU - Borkar, Aditi N.

AU - Lombardi, Marco

AU - Forestan, Cristian

AU - Milner, Sara G.

AU - Davis, Jayne L.

AU - Lale, Aneesh

AU - Kirschner, Gwendolyn K.

AU - Swarup, Ranjan

AU - Tassinari, Alberto

AU - Pandey, Bipin K.

AU - York, Larry M.

AU - Atkinson, Brian S.

AU - Sturrock, Craig J.

AU - Mooney, Sacha J.

AU - Hochholdinger, Frank

AU - Tucker, Matthew R.

AU - Himmelbach, Axel

AU - Stein, Nils

AU - Mascher, Martin

AU - Nagel, Kerstin A.

AU - De Gara, Laura

AU - Simmonds, James

AU - Uauy, Cristobal

AU - Tuberosa, Roberto

AU - Lynch, Jonathan P.

AU - Yakubov, Gleb E.

AU - Bennett, Malcolm J.

AU - Bhosale, Rahul

AU - Salvi, Silvio

PY - 2022/8/2

Y1 - 2022/8/2

N2 - Root angle in crops represents a key trait for efficient capture of soil resources. Root angle is determined by competing gravitropic versus antigravitropic offset (AGO) mechanisms. Here we report a root angle regulatory gene termed ENHANCED GRAVITROPISM1 (EGT1) that encodes a putative AGO component, whose loss-of-function enhances root gravitropism. Mutations in barley and wheat EGT1 genes confer a striking root phenotype, where every root class adopts a steeper growth angle. EGT1 encodes an F-box and Tubby domain-containing protein that is highly conserved across plant species. Haplotype analysis found that natural allelic variation at the barley EGT1 locus impacts root angle. Gravitropic assays indicated that Hvegt1 roots bend more rapidly than wild-type. Transcript profiling revealed Hvegt1 roots deregulate reactive oxygen species (ROS) homeostasis and cell wall-loosening enzymes and cofactors. ROS imaging shows that Hvegt1 root basal meristem and elongation zone tissues have reduced levels. Atomic force microscopy measurements detected elongating Hvegt1 root cortical cell walls are significantly less stiff than wild-type. In situ analysis identified HvEGT1 is expressed in elongating cortical and stele tissues, which are distinct from known root gravitropic perception and response tissues in the columella and epidermis, respectively. We propose that EGT1 controls root angle by regulating cell wall stiffness in elongating root cortical tissue, counteracting the gravitropic machinery’s known ability to bend the root via its outermost tissues. We conclude that root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism.

AB - Root angle in crops represents a key trait for efficient capture of soil resources. Root angle is determined by competing gravitropic versus antigravitropic offset (AGO) mechanisms. Here we report a root angle regulatory gene termed ENHANCED GRAVITROPISM1 (EGT1) that encodes a putative AGO component, whose loss-of-function enhances root gravitropism. Mutations in barley and wheat EGT1 genes confer a striking root phenotype, where every root class adopts a steeper growth angle. EGT1 encodes an F-box and Tubby domain-containing protein that is highly conserved across plant species. Haplotype analysis found that natural allelic variation at the barley EGT1 locus impacts root angle. Gravitropic assays indicated that Hvegt1 roots bend more rapidly than wild-type. Transcript profiling revealed Hvegt1 roots deregulate reactive oxygen species (ROS) homeostasis and cell wall-loosening enzymes and cofactors. ROS imaging shows that Hvegt1 root basal meristem and elongation zone tissues have reduced levels. Atomic force microscopy measurements detected elongating Hvegt1 root cortical cell walls are significantly less stiff than wild-type. In situ analysis identified HvEGT1 is expressed in elongating cortical and stele tissues, which are distinct from known root gravitropic perception and response tissues in the columella and epidermis, respectively. We propose that EGT1 controls root angle by regulating cell wall stiffness in elongating root cortical tissue, counteracting the gravitropic machinery’s known ability to bend the root via its outermost tissues. We conclude that root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism.

KW - antigravitropic

KW - barley

KW - cell-wall

KW - root angle

KW - wheat

UR - http://www.scopus.com/inward/record.url?scp=85135103399&partnerID=8YFLogxK

U2 - 10.1073/pnas.2201350119

DO - 10.1073/pnas.2201350119

M3 - Article

C2 - 35881796

AN - SCOPUS:85135103399

SN - 0027-8424

VL - 119

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 31

M1 - e2201350119

ER -

Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism

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