Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth

Gilad Gabay; Hanchao Wang; Junli Zhang; Jorge I. Moriconi; German F. Burguener; Leonardo D. Gualano; Tyson Howell; Adam Lukaszewski; Brian Staskawicz; Myeong Je Cho; Jaclyn Tanaka; Tzion Fahima; Haiyan Ke; Katayoon Dehesh; Guo Liang Zhang; Jin Ying Gou; Mats Hamberg; Guillermo E. Santa-María; Jorge Dubcovsky

doi:10.1038/s41467-023-36248-y

Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth

Gilad Gabay, Hanchao Wang, Junli Zhang, Jorge I. Moriconi, German F. Burguener, Leonardo D. Gualano, Tyson Howell, Adam Lukaszewski, Brian Staskawicz, Myeong Je Cho, Jaclyn Tanaka, Tzion Fahima, Haiyan Ke, Katayoon Dehesh, Guo Liang Zhang, Jin Ying Gou, Mats Hamberg, Guillermo E. Santa-María, Jorge Dubcovsky

Department of Evolutionary and Environmental Biology

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

Abstract

Wheat, an essential crop for global food security, is well adapted to a wide variety of soils. However, the gene networks shaping different root architectures remain poorly understood. We report here that dosage differences in a cluster of monocot-specific 12-OXOPHYTODIENOATE REDUCTASE genes from subfamily III (OPRIII) modulate key differences in wheat root architecture, which are associated with grain yield under water-limited conditions. Wheat plants with loss-of-function mutations in OPRIII show longer seminal roots, whereas increased OPRIII dosage or transgenic over-expression result in reduced seminal root growth, precocious development of lateral roots and increased jasmonic acid (JA and JA-Ile). Pharmacological inhibition of JA-biosynthesis abolishes root length differences, consistent with a JA-mediated mechanism. Transcriptome analyses of transgenic and wild-type lines show significant enriched JA-biosynthetic and reactive oxygen species (ROS) pathways, which parallel changes in ROS distribution. OPRIII genes provide a useful entry point to engineer root architecture in wheat and other cereals.

Original language	English
Article number	539
Pages (from-to)	539
Journal	Nature Communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-36248-y
State	Published - 1 Feb 2023

Bibliographical note

Funding Information:
J.D. and T.F. acknowledge support from USA-Israel BARD grants US-5191-19C and US-5515-22C. J.D. also acknowledges support from the USDA National Institute of Food and Agriculture the Agriculture and Food Research Initiative Competitive Grant 2022-68013-36439 (WheatCAP), and from the Howard Hughes Medical Institute. G.G. acknowledges support from Vaadia-BARD fellowship number FI-585-2019. G.E.S.-M. acknowledges support from CONICET and the ANPCYT (PICT 2018-02159) Argentina. J.G. acknowledges support from the National Natural Science Foundation of China Grant 31972350. We thank the UC Riverside Metabolomics Core Facility for their help with the Jasmonic Acid determinations and the UC Davis transformation facility for the Fielder transgenic plants. We also thank Yanpeng Wang for his help with the transformation vectors; Rudi Appels for his help with the 1RS gene names in AK58; and Neelima Sinha and Kristina Zumstein for their assistance with the amplicon sequencing to detect induced CRISPR-Cas9 mutations.

Funding Information:
J.D. and T.F. acknowledge support from USA-Israel BARD grants US-5191-19C and US-5515-22C. J.D. also acknowledges support from the USDA National Institute of Food and Agriculture the Agriculture and Food Research Initiative Competitive Grant 2022-68013-36439 (WheatCAP), and from the Howard Hughes Medical Institute. G.G. acknowledges support from Vaadia-BARD fellowship number FI-585-2019. G.E.S.-M. acknowledges support from CONICET and the ANPCYT (PICT 2018-02159) Argentina. J.G. acknowledges support from the National Natural Science Foundation of China Grant 31972350. We thank the UC Riverside Metabolomics Core Facility for their help with the Jasmonic Acid determinations and the UC Davis transformation facility for the Fielder transgenic plants. We also thank Yanpeng Wang for his help with the transformation vectors; Rudi Appels for his help with the 1RS gene names in AK58; and Neelima Sinha and Kristina Zumstein for their assistance with the amplicon sequencing to detect induced CRISPR-Cas9 mutations.

Publisher Copyright:
© 2023, The Author(s).

ASJC Scopus subject areas

Chemistry (all)
Biochemistry, Genetics and Molecular Biology (all)
General
Physics and Astronomy (all)

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10.1038/s41467-023-36248-y

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Gabay, G., Wang, H., Zhang, J., Moriconi, J. I., Burguener, G. F., Gualano, L. D., Howell, T., Lukaszewski, A., Staskawicz, B., Cho, M. J., Tanaka, J., Fahima, T., Ke, H., Dehesh, K., Zhang, G. L., Gou, J. Y., Hamberg, M., Santa-María, G. E., & Dubcovsky, J. (2023). Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth. Nature Communications, 14(1), 539. Article 539. https://doi.org/10.1038/s41467-023-36248-y

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title = "Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth",

abstract = "Wheat, an essential crop for global food security, is well adapted to a wide variety of soils. However, the gene networks shaping different root architectures remain poorly understood. We report here that dosage differences in a cluster of monocot-specific 12-OXOPHYTODIENOATE REDUCTASE genes from subfamily III (OPRIII) modulate key differences in wheat root architecture, which are associated with grain yield under water-limited conditions. Wheat plants with loss-of-function mutations in OPRIII show longer seminal roots, whereas increased OPRIII dosage or transgenic over-expression result in reduced seminal root growth, precocious development of lateral roots and increased jasmonic acid (JA and JA-Ile). Pharmacological inhibition of JA-biosynthesis abolishes root length differences, consistent with a JA-mediated mechanism. Transcriptome analyses of transgenic and wild-type lines show significant enriched JA-biosynthetic and reactive oxygen species (ROS) pathways, which parallel changes in ROS distribution. OPRIII genes provide a useful entry point to engineer root architecture in wheat and other cereals.",

author = "Gilad Gabay and Hanchao Wang and Junli Zhang and Moriconi, {Jorge I.} and Burguener, {German F.} and Gualano, {Leonardo D.} and Tyson Howell and Adam Lukaszewski and Brian Staskawicz and Cho, {Myeong Je} and Jaclyn Tanaka and Tzion Fahima and Haiyan Ke and Katayoon Dehesh and Zhang, {Guo Liang} and Gou, {Jin Ying} and Mats Hamberg and Santa-Mar{\'i}a, {Guillermo E.} and Jorge Dubcovsky",

note = "Funding Information: J.D. and T.F. acknowledge support from USA-Israel BARD grants US-5191-19C and US-5515-22C. J.D. also acknowledges support from the USDA National Institute of Food and Agriculture the Agriculture and Food Research Initiative Competitive Grant 2022-68013-36439 (WheatCAP), and from the Howard Hughes Medical Institute. G.G. acknowledges support from Vaadia-BARD fellowship number FI-585-2019. G.E.S.-M. acknowledges support from CONICET and the ANPCYT (PICT 2018-02159) Argentina. J.G. acknowledges support from the National Natural Science Foundation of China Grant 31972350. We thank the UC Riverside Metabolomics Core Facility for their help with the Jasmonic Acid determinations and the UC Davis transformation facility for the Fielder transgenic plants. We also thank Yanpeng Wang for his help with the transformation vectors; Rudi Appels for his help with the 1RS gene names in AK58; and Neelima Sinha and Kristina Zumstein for their assistance with the amplicon sequencing to detect induced CRISPR-Cas9 mutations. Funding Information: J.D. and T.F. acknowledge support from USA-Israel BARD grants US-5191-19C and US-5515-22C. J.D. also acknowledges support from the USDA National Institute of Food and Agriculture the Agriculture and Food Research Initiative Competitive Grant 2022-68013-36439 (WheatCAP), and from the Howard Hughes Medical Institute. G.G. acknowledges support from Vaadia-BARD fellowship number FI-585-2019. G.E.S.-M. acknowledges support from CONICET and the ANPCYT (PICT 2018-02159) Argentina. J.G. acknowledges support from the National Natural Science Foundation of China Grant 31972350. We thank the UC Riverside Metabolomics Core Facility for their help with the Jasmonic Acid determinations and the UC Davis transformation facility for the Fielder transgenic plants. We also thank Yanpeng Wang for his help with the transformation vectors; Rudi Appels for his help with the 1RS gene names in AK58; and Neelima Sinha and Kristina Zumstein for their assistance with the amplicon sequencing to detect induced CRISPR-Cas9 mutations. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

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month = feb,

day = "1",

doi = "10.1038/s41467-023-36248-y",

language = "English",

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Gabay, G, Wang, H, Zhang, J, Moriconi, JI, Burguener, GF, Gualano, LD, Howell, T, Lukaszewski, A, Staskawicz, B, Cho, MJ, Tanaka, J, Fahima, T, Ke, H, Dehesh, K, Zhang, GL, Gou, JY, Hamberg, M, Santa-María, GE & Dubcovsky, J 2023, 'Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth', Nature Communications, vol. 14, no. 1, 539, pp. 539. https://doi.org/10.1038/s41467-023-36248-y

TY - JOUR

T1 - Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth

AU - Gabay, Gilad

AU - Wang, Hanchao

AU - Zhang, Junli

AU - Moriconi, Jorge I.

AU - Burguener, German F.

AU - Gualano, Leonardo D.

AU - Howell, Tyson

AU - Lukaszewski, Adam

AU - Staskawicz, Brian

AU - Cho, Myeong Je

AU - Tanaka, Jaclyn

AU - Fahima, Tzion

AU - Ke, Haiyan

AU - Dehesh, Katayoon

AU - Zhang, Guo Liang

AU - Gou, Jin Ying

AU - Hamberg, Mats

AU - Santa-María, Guillermo E.

AU - Dubcovsky, Jorge

N1 - Funding Information: J.D. and T.F. acknowledge support from USA-Israel BARD grants US-5191-19C and US-5515-22C. J.D. also acknowledges support from the USDA National Institute of Food and Agriculture the Agriculture and Food Research Initiative Competitive Grant 2022-68013-36439 (WheatCAP), and from the Howard Hughes Medical Institute. G.G. acknowledges support from Vaadia-BARD fellowship number FI-585-2019. G.E.S.-M. acknowledges support from CONICET and the ANPCYT (PICT 2018-02159) Argentina. J.G. acknowledges support from the National Natural Science Foundation of China Grant 31972350. We thank the UC Riverside Metabolomics Core Facility for their help with the Jasmonic Acid determinations and the UC Davis transformation facility for the Fielder transgenic plants. We also thank Yanpeng Wang for his help with the transformation vectors; Rudi Appels for his help with the 1RS gene names in AK58; and Neelima Sinha and Kristina Zumstein for their assistance with the amplicon sequencing to detect induced CRISPR-Cas9 mutations. Funding Information: J.D. and T.F. acknowledge support from USA-Israel BARD grants US-5191-19C and US-5515-22C. J.D. also acknowledges support from the USDA National Institute of Food and Agriculture the Agriculture and Food Research Initiative Competitive Grant 2022-68013-36439 (WheatCAP), and from the Howard Hughes Medical Institute. G.G. acknowledges support from Vaadia-BARD fellowship number FI-585-2019. G.E.S.-M. acknowledges support from CONICET and the ANPCYT (PICT 2018-02159) Argentina. J.G. acknowledges support from the National Natural Science Foundation of China Grant 31972350. We thank the UC Riverside Metabolomics Core Facility for their help with the Jasmonic Acid determinations and the UC Davis transformation facility for the Fielder transgenic plants. We also thank Yanpeng Wang for his help with the transformation vectors; Rudi Appels for his help with the 1RS gene names in AK58; and Neelima Sinha and Kristina Zumstein for their assistance with the amplicon sequencing to detect induced CRISPR-Cas9 mutations. Publisher Copyright: © 2023, The Author(s).

PY - 2023/2/1

Y1 - 2023/2/1

N2 - Wheat, an essential crop for global food security, is well adapted to a wide variety of soils. However, the gene networks shaping different root architectures remain poorly understood. We report here that dosage differences in a cluster of monocot-specific 12-OXOPHYTODIENOATE REDUCTASE genes from subfamily III (OPRIII) modulate key differences in wheat root architecture, which are associated with grain yield under water-limited conditions. Wheat plants with loss-of-function mutations in OPRIII show longer seminal roots, whereas increased OPRIII dosage or transgenic over-expression result in reduced seminal root growth, precocious development of lateral roots and increased jasmonic acid (JA and JA-Ile). Pharmacological inhibition of JA-biosynthesis abolishes root length differences, consistent with a JA-mediated mechanism. Transcriptome analyses of transgenic and wild-type lines show significant enriched JA-biosynthetic and reactive oxygen species (ROS) pathways, which parallel changes in ROS distribution. OPRIII genes provide a useful entry point to engineer root architecture in wheat and other cereals.

AB - Wheat, an essential crop for global food security, is well adapted to a wide variety of soils. However, the gene networks shaping different root architectures remain poorly understood. We report here that dosage differences in a cluster of monocot-specific 12-OXOPHYTODIENOATE REDUCTASE genes from subfamily III (OPRIII) modulate key differences in wheat root architecture, which are associated with grain yield under water-limited conditions. Wheat plants with loss-of-function mutations in OPRIII show longer seminal roots, whereas increased OPRIII dosage or transgenic over-expression result in reduced seminal root growth, precocious development of lateral roots and increased jasmonic acid (JA and JA-Ile). Pharmacological inhibition of JA-biosynthesis abolishes root length differences, consistent with a JA-mediated mechanism. Transcriptome analyses of transgenic and wild-type lines show significant enriched JA-biosynthetic and reactive oxygen species (ROS) pathways, which parallel changes in ROS distribution. OPRIII genes provide a useful entry point to engineer root architecture in wheat and other cereals.

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Dosage differences in 12-OXOPHYTODIENOATE REDUCTASE genes modulate wheat root growth

Abstract

Bibliographical note

ASJC Scopus subject areas

UN SDGs

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