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
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

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

ASJC Scopus subject areas

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

UN SDGs

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10.1038/s41467-023-36248-y

Cite this

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), Article 539. https://doi.org/10.1038/s41467-023-36248-y

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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",

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

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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. https://doi.org/10.1038/s41467-023-36248-y

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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

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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SN - 2041-1723

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JO - Nature Communications

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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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